An attempt to search for the common cellular mechanism of ovulation across all metazoans

in Reproduction
Authors:
Takayuki Takahashi Laboratory of Reproductive and Developmental Biology, Faculty of Science, Hokkaido University, Sapporo, Japan

Search for other papers by Takayuki Takahashi in
Current site
Google Scholar
PubMed Close
https://orcid.org/0009-0009-5721-3705
and
Katsueki Ogiwara Laboratory of Reproductive and Developmental Biology, Faculty of Science, Hokkaido University, Sapporo, Japan

Search for other papers by Katsueki Ogiwara in
Current site
Google Scholar
PubMed Close

Correspondence should be addressed to T Takahashi: ttakaha@sci.hokudai.ac.jp or ezono4321syubun@yahoo.co.jp
DOI:
https://doi.org/10.1530/REP-24-0184
Volume/Issue:
Volume 169: Issue 1
Article ID:
e240184
Article Type:
Review Article
Online Publication Date:
02 Jan 2025
Copyright:
© the author(s) 2025
Restricted access
Rent on DeepDyve

Sign up for journal news

In brief

Ovulation, the female reproductive process whereby fertilizable oocytes are released from a mature ovarian follicle, is widely seen in all animals that sexually reproduce. This paper reveals that, despite the remarkably diverse styles of ovulation among animal taxa, most ovulate via follicle rupture and suggests that the rupture process may operate via similar cellular mechanisms across animals.

Abstract

Ovulation is the process by which a fertilizable oocyte is extruded from the interior of the follicle. Herein, we conducted a literature survey to explore the ovulation patterns of 11 sexually reproducing species belonging to 10 animal phyla. These results indicate a large variety of ovulation patterns. Further comparative biological and evolutionary considerations of these results led us to conclude that most female animals ovulate via follicle rupture. We propose that in all animals that ovulate by follicle rupture, two cellular events may be critically involved in the process: i) the disintegration of cell junctional systems leading to intracellular cytoskeleton rearrangement in the follicle cells and ii) the degradation of extracellular matrix (ECM) proteins filled between follicle cells. These events may result in follicular cell deformation and increased motility, both of which are necessary for the formation of a path through which an oocyte escapes from the follicle. In addition to the requirement of ECM degradation for disintegrating cell junctions, intensive ECM protein degradation at the apical region of the follicle probably became increasingly important in late-evolving animals, such as vertebrates, in which a thick follicle wall containing a large abundance of ECM proteins is formed. We also considered hypothetical scenarios for the evolution of ovulation in these animals. Furthermore, this article discusses future problems that need to be solved for a more comprehensive understanding of ovulation in the animal kingdom.

Reproduction is committed to supporting researchers in demonstrating the impact of their articles published in the journal.

The two types of article metrics we measure are (i) more traditional full-text views and pdf downloads, and (ii) Altmetric data, which shows the wider impact of articles in a range of non-traditional sources, such as social media.

More information is on the Reasons to publish page.

Sept 2018 onwards Past Year Past 30 Days
Full Text Views 89 89 3
PDF Downloads 115 115 5

 

  • Collapse
  • Expand
Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Amiel A, Leclere L, Robert L, et al. 2009 Conserved functions for Mos in eumetazoan oocyte maturation revealed by studies in a cnidarian. Curr Biol 19 305–311. (https://doi.org/10.1016/j.cub.2008.12.054)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Artigas GQ, Lapébie P, Leclère L, et al. 2020 A G-protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia. PLoS Biol 18 e3000614. (https://doi.org/10.1371/journal.pbio.3000614)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Baker SJC & Van Der Kraak G 2019 Investigating the role of prostaglandin receptor isoform EP4B in zebrafish ovulation. Gen Comp Endocrinol 283 113228. (https://doi.org/10.1016/j.ygcen.2019.113228)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Baker SJC, Corrigan E, Melnyk N, et al. 2021 Nuclear progesterone receptor regulates ptger4b and PLA2G4A expression in zebrafish (Danio rerio) ovulation. Gen Comp Endocrinol 311 113842. (https://doi.org/10.1016/j.ygcen.2021.113842)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Barthel D & Detmer A 1990 The spermatogenesis of Halichondria panicea (Porifera, Demospongia). Zoomorphology 110 9–15. (https://doi.org/10.1007/BF01632807)

  • Barua A, Yoshimura Y & Tamura T 1998 The effects of age and sex steroids on the macrophage population in the ovary of the chicken, Gallus domosticus. J Reprod Fertil 114 253–258. (https://doi.org/10.1530/jrf.0.1140253)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Beams HW & Kessel RG 1983 Cnidaria. In Reproductive Biology of Invertebrates, Vol. 1, Oogenesis, Oviposition, and Oosorption, pp 31–66. Eds KG Adiyodi & RG Adiyodi. New York: John Wiley and Sons.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Beijnink FB, Walker CW & Voogt PA 1984 An ultrastructural study of relationships between the ovarian haemal system, follicle cells, and primary oocytes in the sea star, Asterias rubens. Cell Tissue Res 238 339–347. (https://doi.org/10.1007/BF00217306)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Berrier AL & Yamada KM 2007 Cell-matrix adhesion. J Cell Physiol 213 565–573. (https://doi.org/10.1002/jcp.21237)

  • Bivic AL 2013 Evolution and cell physiology. 4. Why invent yet another protein complex to build junctions in epithelial cells? Am J Physiol Cell Physiol 305 C1193–C1201. (https://doi.org/10.1152/ajpcell.00272.2013)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bloch Qazi MC, Heifetz Y & Wolfner MF 2003 The developments between gametogenesis and fertilization: ovulation and female sperm storage in Drosophila melanogaster. Dev Biol 256 195–211. (https://doi.org/10.1016/s0012-1606(02)00125-2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Boute N, Exposito JY, Boury-Esnault N, et al. 1996 Type IV collagen in sponges, the missing link in basement membrane ubiquity. Biol Cell 88 37–44. (https://doi.org/10.1016/s0248-4900(97)86829-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Brännström M & Enskog A 2002 Leukocyte networks and ovulation. J Reprod Immunol 57 47–60. (https://doi.org/10.1016/s0165-0378(02)00009-8)

  • Brinkhurst RO 1982 Evolution in the Annelida. Can J Zoolog 60 1043–1059. (https://doi.org/10.1139/z82-145)

  • Bui YK & Sternberg PW 2002 Caenorhabditis elegans inositol 5-phosphatase homolog negatively regulates inositol 1,4,5-trisphosphate signaling in ovulation. Mol Biol Cell 13 1641–1651. (https://doi.org/10.1091/mbc.02-01-0008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Caputi L, Andreakis N, Mastrototaro F, et al. 2007 Cryptic speciation in a model invertebrate chordate. Proc Natl Acad Sci U S A 104 9364–9369. (https://doi.org/10.1073/pnas.0610158104)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Casellato S, Martinucci G & Zoja E 1987 Ultrastructural features of gametogenesis during the life cycle in Branchiura sowerbyi Beddard (Oligochaeta, Tubificidae). Hydrobiogia 155 145–154. (https://doi.org/10.1007/BF00025640)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Channing CP, Schaerf FW, Anderson LD, et al. 1980 Ovarian follicular and luteal physiology. Int Rev Physiol 22 117–201.

  • Chen PS, Stumm-Zollinger E, Aigaki T, et al. 1988 A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell 54 291–298. (https://doi.org/10.1016/0092-8674(88)90192-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cheng H, Govindan JA & Greenstein D 2008 Regulated trafficking of the MSP/Eph receptor during oocyte meiotic maturation in C. elegans. Curr Biol 18 705–714. (https://doi.org/10.1016/j.cub.2008.04.043)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chiba K 2011 Evolution of the acquisition of fertilization competenceand polyspermy blocks during meiotic maturation. Mol Reprod Dev 78 808–813. (https://doi.org/10.1002/mrd.21378)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chiba K 2020 Oocyte maturation in starfish. Cells 9 476. (https://doi.org/10.3390/cells9020476)

  • Cho SE, Li W, Beard AM, et al. 2024 Actomyosin contraction in the follicular epithelium provides the major mechanical force for follicle rupture during Drosophila ovulation. Proc Natl Acad Sci U S A 121 e2407083121. (https://doi.org/10.1073/pnas.2407083121)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Clandinin TR, DeModena JA & Sternberg PW 1998 Inositol trisphosphate mediates a RAS-independent response to LET-23 receptor tyrosine kinase activation in C. elegans. Cell 92 523–533. (https://doi.org/10.1016/s0092-8674(00)80945-9)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Clelland E & Peng C 2009 Endocrine/paracrine control of zebrafish ovarian development. Mol Cell Endocrinol 312 42–52. (https://doi.org/10.1016/j.mce.2009.04.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Collins JJ, III 2017 Platyhelminthes. Curr Biol 27 R252–R256. (https://doi.org/10.1016/j.cub.2017.02.016)

  • Collins C & Nelson WJ 2015 Running with neighbors: coordinating cell migration and cell-cell adhesion. Curr Opin Cell Biol 36 62–70. (https://doi.org/10.1016/j.ceb.2015.07.004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Collins AG, Schuchert P, Marques AC, et al. 2006 Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol 55 97–115. (https://doi.org/10.1080/106351500433615)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Conn DB 2000a Phylum Porifera. In Atlas of Invertebrate Reproduction and Development, 2nd ed, pp 7–16. New York: Wiley-Liss.

  • Conn DB 2000b Phylum Cnidaria. In Atlas of Invertebrate Reproduction and Development, 2nd ed, pp 17–34. New York: Wiley-Liss.

  • Conn DB 2000c Phylum Platyhelminthes. In Atlas of Invertebrate Reproduction and Development, 2nd ed, pp 35–62. New York: Wiley-Liss.

  • Conn DB 2000d Phylum Annelida. In Atlas of Invertebrate Reproduction and Development, 2nd ed, pp 117–134. New York: Wiley-Liss.

  • Conn DB 2000e Phylum Mollusca. In Atlas of Invertebrate Reproduction and Development, 2nd ed, pp 93–115. New York: Wiley-Liss.

  • Conn DB 2000f Phylum nematoda. In Atlas of Invertebrate Reproduction and Development, 2nd ed, pp 73–92. New York: Wiley-Liss.

  • Conn DB 2000g Phylum Arthropoda. In Atlas of Invertebrate Reproduction and Development, 2nd ed, pp 135–169. New York: Wiley-Liss.

  • Conn DB 2000h Phylum Echinodermata. In Atlas of Invertebrate Reproduction and Development, 2nd ed, pp 171–197. New York: Wiley-Liss.

  • Conn DB 2000i Phylum chordata. In Atlas of Invertebrate Reproduction and Development, 2nd ed, pp 199–212. New York: Wiley-Liss.

  • Coutellec MA & Lagadic L 2006 Effects of self-fertilization, environmental stress and exposure to xenobiotics on fitness-related traits of the freshwater snail Lymnaea stagnalis. Ecotoxicology 15 199–213. (https://doi.org/10.1007/s10646-005-0049-x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Das D & Arur S 2022 Regulation of oocyte maturation: role of conserved ERK signaling. Mol Reprod Dev 89 353–374. (https://doi.org/10.1002/mrd.23637)

  • Deady LD & Sun J 2015 A follicle rupture assay reveals an essential role for follicular adrenergic signaling in Drosophila ovulation. PLoS Genet 11 e1005604. (https://doi.org/10.1371/journal.pgen.1005604)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Deady LD, Shen W, Mosure SA, et al. 2015 Matrix metalloproteinase 2 is required for ovulation and corpus luteum formation in Drosophila. PLoS Genet 11 e1004989. (https://doi.org/10.1371/journal.pgen.1004989)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Deady LD, Li W & Sun J 2017 The zinc-finger transcription factor Hindsight regulates ovulation competency of Drosophila follicles. Elife 6 e29887. (https://doi.org/10.7554/eLife.29887)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Delsuc F, Brinkmann H, Chourrout D, et al. 2006 Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439 965–968. (https://doi.org/10.1038/nature04336)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Duffy DM, Ko C, Jo M, et al. 2019 Ovulation: parallels with inflammatory processes. Endocr Rev 40 369–416. (https://doi.org/10.1210/er.2018-00075)

  • Dumollard R, Levasseur M, Hebras C, et al. 2011 Mos limits the number of meiotic divisions in urochordate eggs. Development 138 885–895. (https://doi.org/10.1242/dev.057133)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dunn CW, Hejnol A, Matus DQ, et al. 2008 Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452 745–749. (https://doi.org/10.1038/nature06614)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dunn CW, Giribet G, Edgecombe GD, et al. 2014 Animal phylogeny and its evolutionary implication. Annu Rev Ecol Evol Syst 45 374–395. (https://doi.org/10.1146/annurev-ecolsys-120213-091627)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ehrlich H, Wysokowski M, Żółtowska-Aksamitowska S, et al. 2018 Collagens of poriferan origin. Mar Drugs 16 79. (https://doi.org/10.3390/md126030079)

  • Emery A, Dunning KR, Dinh DT, et al. 2023 Dynamic regulation of semaphorin 7A and adhesion receptors in ovarian follicle remodeling and ovulation. Front Cell Dev Biol 11 1261038. (https://doi.org/10.3389/fcell.2023.1261038)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ereskovsky AV, Renard E & Borchiellini C 2013 Cellular and molecular processes leading to embryo formation in sponges: evidences for high conservation of processes throughout animal evolution. Dev Genes Evol 223 5–22. (https://doi.org/10.1007/s00427-012-0399-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Espey LL 1980 Ovulation as an inflammatory reaction—A hypothesis. Biol Reprod 22 73–106. (https://doi.org/10.1095/biolreprod22.1.73)

  • Espey LL 1999 Ovulation. In Encyclopedia of Reproduction, vol III, pp 605–614. Eds E Knoil & JD Neill. San Diego: Academic Press.

  • Espey LL & Lipner H 1963 Measurements of intrafollicular pressures in the rabbit ovary. Am J Physiol 205 1067–1072. (https://doi.org/10.1152/ajplegacy.1963.205.6.1067)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Espey LL & Richards JS 2006 Ovulation. In Physiology of Reproduction, 3rd ed, vol 1, pp 425–474. Ed JD Neill. Amsterdam: Academic Press. (https://doi.org/10.1016/b978-012515400-0/50016-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Extavour C 2009 Oogenesis: making the mos of meiosis. Curr Biol 19 R489–R491. (https://doi.org/10.1016/j.cub.2009.05.015)

  • Fahey B & Degnan BM 2012 Origin and evolution of laminin gene family diversity. Mol Biol Evol 29 1823–1836. (https://doi.org/10.1093/molbev/mss060)

  • Fan HY, Liu Z, Shimada M, et al. 2009 MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324 938–941. (https://doi.org/10.1126/science.1171396)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fell PE 1983 Porifera. In Reproductive Biology of Invertebrates, Vol. 1, Oogenesis, Oviposition, and Oosorption, pp 1–29. Eds KG Adiyodi & RG Adiyodi. New York: John Wiley and Sons.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fincher CT, Wurtzel O, de Hoog T, et al. 2018 Cell type transcriptome atlas for the planarian Schmidtea mediterranea. Science 360 eaaq1736. (https://doi.org/10.1126/science.aaq1736)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Foor WE 1983 Nematoda. In Reproductive Biology of Invertebrates, Vol. 1, Oogenesis, Oviposition, and Oosorption, pp 223–256. Eds KG Adiyodi & RG Adiyodi. New York: John Wiley and Sons.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fox AS & Brust RA 1996 Parity diagnosis and ovulation in Culiseta inornata (Diptera: Culicidae). J Med Entomol 33 402–412. (https://doi.org/10.1093/jmedent/33.3.402)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Freeman G 1987 The role of oocyte maturation in the ontogeny of the fertilization site in the hydrogoan Hydractinia echinate. Rouxs Arch Dev Biol 196 83–92. (https://doi.org/10.1007/BF00402029)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fujimori C, Ogiwara K, Hagiwara A, et al. 2012 New evidence for the involvement of prostaglandin receptor EP4b in ovulation of the medaka, Oryzias latipes. Mol Cell Endocrinol 362 76–84. (https://doi.org/10.1016/j.mce.2012.05.013)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Funayama N 2010 The stem cell system in demosponges: insights into the origin of somatic stem cells. Dev Growth Differ 52 1–14. (https://doi.org/10.1111/j.1440-169X.2009.01162.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Funayama N 2018 The cellular and molecular bases of the sponge stem cell systems underlying reproduction, homeostasis and regeneration. Int J Dev Biol 62 513–525. (https://doi.org/10.1387/ijdb.180016nf)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Garcia MA, Nelson WJ & Chavez N 2018 Cell–cell junctions organize structural and signaling networks. Cold Spring Harb Perspect Biol 10 a029181. (https://doi.org/10.1101/cshperspect.a029181)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gilchrist RB, Luciano AM, Richani D, et al. 2016 Oocyte maturation and quality: role of cyclic nucleotides. Reproduction 152 R143–R157. (https://doi.org/10.1530/REP-15-0606)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Goodenough U & Heitman J 2014 Origins of eukaryotic sexual reproduction. Cold Spring Harb Perspect Biol 6 a016154. (https://doi.org/10.1101/cshperspect.a016154)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Greenwald I 2005 LIN-12/notch signaling in C. elegans. WormBook 8 1–16. (https://doi.org/10.1895/wormbook.1.10.1)

  • Gremigni V 1983 Platyhelminthes–Turbellaria. In Reproductive Biology of Invertebrates, Vol. 1, Oogenesis, Oviposition, and Oosorption, pp 67–107. Eds KG Adiyodi & RG Adiyodi. New York: John Wiley and Sons.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gremigni V & Nigro M 1983 An ultrastructural study of oogenesis in a marine triclad. Tissue Cell 15 405–415. (https://doi.org/10.1016/0040-8166(83)90072-1)

  • Grier HJ, Aranzábal MCU & Patiño R 2009 The ovary, folliculogenesis, and oogenesis in teleosts. In Reproductive Biology and Phylogeny of Fishes (Agnathans and Bony fishes), pp 25–84. Ed BGM Jamieson. Enfield, NH: Science Publications.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hagiwara A, Ogiwara K, Katsu Y, et al. 2014 Luteinizing hormone-induced expression of Ptger4b, a prostaglandin E2 receptor indispensable for ovulation of the medaka, Oryzias latipes, is regulated by a genomic mechanism involving nuclear progestin receptor. Biol Reprod 90 126. (https://doi.org/10.1095/biolreprod.113.115485)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hajna A & Berset T 2002 The C. elegans MAPK phosphatase LIP-1 is required for the G2/M meiotic arrest of developing oocytes. EMBO J 21 4317–4326. (https://doi.org/10.1093/emboj/cdf430)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Han SM, Cottee PA & Miller MA 2009 Sperm and oocyte communication mechanisms controlling C. elegans fertility. Dev Biol 239 1265–1281. (https://doi.org/10.1002/dvdy.22202)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Haraguchi S, Ikeda N, Abe M, et al. 2016 Nucleotide sequence and expression of relaxin-like gonad-stimulating peptide in starfish Asterina pectinifera. Gen Comp Endocrinol 227 115–119. (https://doi.org/10.1016/j.ygcen.2015.06.017)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Harrath AH, Alwasal SH, Alhazza I, et al. 2011 An ultrastructural study of oogenesis in the planarian Schmidtea mediterranea (Platyhlminthe, Paludicola). C R Biol 334 516–525. (https://doi.org/10.1016/j.crvi.2011.03.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Harrath AH, Ahmed M, Sayed SR, et al. 2013 An ultrastructural study of oogenesis and cell dynamics during cocoon shell secretion in the subterranean freshwater planarian Dendrocoelum constricum (Plateyhelminthes, Tricladida). Tissue Cell 45 39–46. (https://doi.org/10.1016/j.tice.2012.09.003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hartsock A & Nelson WJ 2008 Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778 660–669. (https://doi.org/10.1016/j.bbamem.2007.07.012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hashmi S, Zhang J, Oksov Y, et al. 2006 The Caenorhabditis elegans CPI-2a cystatin-like inhibitor has an essential regulatory role during oogenesis and fertilization. J Biol Chem 281 28415–28429. (https://doi.org/10.1074/jbc.M600254200)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hegsted A, Wright FA, Votra S, et al. 2016 INF2- and FHOD-related formins promote ovulation in the somatic gonad of C. elegans. Cytoskeleton 73 712–728. (https://doi.org/10.1002/cm.21341)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Heifetz Y, Lung O, Frongillo EA, et al. 2000 The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr Biol 10 99–102. (https://doi.org/10.1016/s0960-9822(00)00288-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Heifetz Y, Vandenberg LN, Cohn HI, et al. 2005 Two cleavage products of the Drosophila accessory gland protein ovulin can independently induce ovulation. Proc Natl Acad Sci U S A 102 743–748. (https://doi.org/10.1073/pnas.0407692102)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Helfman GS, Collette BB, Facey DE, et al. 2009 The Diversity of Fishes, 2nd ed. West Sussex: John Wiley & Sons.

  • Herndon LA & Wolfner MF 1995 A Drosophila seminal fluid protein, Acp26Aa, stimulates egg-laying in female for one day following mating. Proc Natl Acad Sci U S A 92 10114–10118. (https://doi.org/10.1073/pnas.92.22.10114)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hiatt SM, Duren HM, Shyu YJ, et al. 2009 Caenorhabditis elegans FOS-1 and JUN-1 regulate plc-1 expression in the spermatheca to control ovulation. Mol Biol Cell 20 3888–3895. (https://doi.org/10.1091/mbc.E08-08-0833)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hirsh D, Oppenheim D & Klass M 1976 Development of the reproductive system of Caenorhabditis elegans. Dev Biol 49 200–219. (https://doi.org/10.1016/0012-1606(76)90267-0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hoshino Z & Nishikawa T 1985 Taxonomic studies of Ciona intestinalis (L.) and its allies. Publ Seto Mar Biol Lab 15 3061–3079. (https://doi.org/10.5134/175476)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hotta K, Dauga D & Manni L 2020 The ontology of the anatomy and development of the solitary ascidian Ciona: the swimming larva and its metamorphosis. Sci Rep 10 17916. (https://doi.org/10.1038/s41598-020-73544-9)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hrabia A 2021 Matrix met alloproteinases (MMPs) and inhibitors of MMPs in the avian reproductive system: an overview. Int J Mol Sci 22 8056. (https://doi.org/10.3390/ijms22158056)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hubbard EJA & Greenstein D 2000 The Caenorhabditis elegans gonad: a test tube for cell developmental biology. Dev Dyn 218 2–22. (https://doi.org/10.1002/(SICI)1097-0177(200005)218:1<2::AID-DVDY2>3.0.CO;2-W)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Huelgas-Morales G & Greenstein D 2018 Control of oocyte meiotic maturation in C. elegans. Semin Cell Dev Biol 84 90–99. (https://doi.org/10.1016/j.semcdb.2017.12.005)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hunter RHF 2003 Physiology of the Graafian Follicle and Ovulation. Cambridge: Cambridge University Press.

  • Hunzicker-Dunn M & Mayo K 2015 Gonadotropin signaling in the ovary. In Physiology of Reproduction, 4th ed, vol 1, pp 895–945. Eds TM Plant & AJ Zeleznik. Amsterdam: Academic Press. (https://doi.org/10.1016/B978-0-12-397175-3.00020-X).

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hynes RO 2002 Integrins: bidirectional, allosteric signaling machines. Cell 110 673–687. (https://doi.org/10.1016/s0092-8674(02)00971-6)

  • Hynes RO & Zhao Q 2000 The evolution of cell adhesion. J Cell Biol 150 F89–F96. (https://doi.org/10.1083/jcb.150.2.f89)

  • Jarne P, David P, Pointier JP, et al. 2010 Basommatophoran gastropods. In The Evolution of Primary Sexual Characters in Animals, pp 173–196. Eds A Cordoba-Aguilar & JL Leonard. Oxford: Oxford University Press.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jessus C, Munro C & Houliston E 2020 Managing the oocyte meiotic arrest—lessons from frogs and jellyfish. Cells 9 1150. (https://doi.org/10.3390/cells9051150)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jiang Y, He Y, Pan X, et al. 2023 Advances in oocyte maturation in vivo and in vitro in mammals. Int J Mol Sci 24 9059. (https://doi.org/10.3390/ijms24109059)

  • Johnsen AH & Rehfeld JF 1990 Cionin: a disulfotyrosyl hybrid of cholecystokinin and gastrin from the neural ganglion of the protochordate Ciona intestinalis. J Biol Chem 265 3054–3058. (https://doi.org/10.1016/s0021-9258(19)39732-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • de Jong-Brink M & Geraerts WPM 1982 Oogenesis in gastropods. Malacologia 22 145–149.

  • de Jong-Brink M, Boer HH & Joosse J 1983 Mollusca. In Reproductive Biology of Invertebrates, Vol. 1, Oogenesis, Oviposition, and Oosorption, pp 297–355. Eds KG Adiyodi & RG Adiyodi. New York: John Wiley and Sons.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • de Jong-Brink M, de With ND, Hurkmans PJM, et al. 1984 A morphological, enzyme-cytochemical, and physiological study of the blood-gonad barrier in the hermaphroditic snail Lymnaea stagnalis. Cell Tissue Res 235 593–600. (https://doi.org/10.1007/BF00226957)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Joosse J & Reitz D 1969 Functional anatomical aspects of the ovotestis of Lymnaea stagnalis. Malacologia 9 101–109.

  • Kalachev AV & Dyachuk VA 2022 Are myoepithelial cells confined to genital coelomic sinus in the gonads of sea stars? Tissue Cell 76 101757. (https://doi.org/10.1016/j.tice.2022.101757)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kanda S 2019 Evolution of the regulatory mechanisms for the hypothalamic–pituitary–gonadal axis in vertebrates—hypothesis from a comparative view. Gen Comp Endocrinol 284 113075. (https://doi.org/10.1016/j.ygcen.2018.11.014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kanatani H & Shirai H 1970 Mechanism of starfish spawning. III. Properties and action of meiosis-inducing substance produced in gonad under influence of gonad-stimulating substance. Development, Growth and Differentiation 12 119–140. (https://doi.org/10.1111/j.1440-169x.1970.00119.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kanatani H & Nagahama Y 1983 Echinodermata. In Reproductive Biology of Invertebrates, Vol. 1, Oogenesis, Oviposition, and Oosorption, pp 611–654. Eds KG Adiyodi & RG Adiyodi. New York: John Wiley and Sons.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kanatani H, Shirai H, Nakanishi K, et al. 1969 Isolation and identification on meiosis inducing substance in starfish Asterias amurensis. Nature 221 273–274. (https://doi.org/10.1038/221273a0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kawamura K, Tiozzo S, Manni L, et al. 2011 Germline cell formation and gonad regeneration in solitary and colonial ascidians. Dev Dynam 240 299–308. (https://doi.org/10.1002/dvdy.22542)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kelley CA & Cram EJ 2019 Regulation of actin dynamics in the C. elegans somatic gonad. J Dev Biol 7 6. (https://doi.org/10.3390/jdb7010006)

  • Kessel RG 1983 Urochordata-ascidiacea. In Reproductive Biology of Invertebrates, vol. 1, Oogenesis, Oviposition, and Oosorption, pp 655–734. Eds KG Adiyodi & RG Adiyodi. New York: John Wiley and Sons.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kim S, Spike C & Greenstein D 2013 Control of oocyte growth and meiotic maturation in C. elegans. Adv Exp Med Biol 757 277–320. (https://doi.org/10.1007/978-1-4614-4015-4_10)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kimble J & Hirsh D 1979 The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol 70 396–417. (https://doi.org/10.1016/0012-1606(79)90035-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • King RC 1970a The meiotic behavior of the Drosophila oocyte. Int Rev Cytol 28 125–168. (https://doi.org/10.1016/s0074-7696(08)62542-5)

  • King RC 1970b Ovarian Development in Drosophila Melanogaster, pp 149–188. New York: Academic Press.

  • Kishimoto T 2011 A primer on meiotic resumption in starfish oocytes: the proposed signaling pathway triggered by maturation-inducing hormone. Mol Reprod Dev 78 704–707. (https://doi.org/10.1002/mrd.21343)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kishimoto T 2015 Entry into mitosis: a solution to the decades-long enigma of MPF. Chromosoma 124 417–428. (https://doi.org/10.1007/s00412-015-0508-y)

  • Kishimoto T, Usui N & Kanatani H 1984 Breakdown of starfish ovarian follicle induced by maturation-promoting factor. Dev Biol 101 28–34. (https://doi.org/10.1016/0012-1606(84)90113-1)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Knapp E & Sun J 2017 Steroid signaling in mature follicles is important for Drosophila ovulation. Proc Natl Acad Sci U S A 114 699–704. (https://doi.org/10.1073/pnas.1614383114)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Knapp EM, Li W & Sun J 2019 Downregulation of homeodomain protein cut is essential for Drosophila follicle maturation and ovulation. Development 146 dev179002. (https://doi.org/10.1242/dev.179002)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Knapp EM, Li W, Singh V, et al. 2020 Nuclear receptor Ftz-f1 promotes follicle maturation and ovulation partly via bHLH/PAS transcription factor Sim. Elife 9 e54568. (https://doi.org/10.7554/eLife.54568)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Koene JM 2010 Neuro-endocrine control of reproduction in hermaphroditic freshwater snail: mechanisms and evolution. Front Behav Neurosci 4 167. (https://doi.org/10.3389/fnbeh.2010.00167)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Koutsouveli V, Taboada S, Moles J, et al. 2018 Insights into the reproduction of some Antarctic dendroceratid, poecilosclerid, and haplosclerid demosponges. PLoS One 13 e0192267. (https://doi.org/10.1371/journal.pone.0192267)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Koutsouveli V, Cárdenas P, Santodomingo N, et al. 2020 The molecular machinery of gametogenesis in Geodia demosponges (Porifera): evolutionary origins of a conserved toolkit across animals. Mol Cell Biol 37 3485–3506. (https://doi.org/10.1093/molbev/msaa183)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kovacevic I & Cram EJ 2010 FLN-1/Filamin is required for maintenance of actin and exit of fertilized oocytes from the spermatheca in C. elegans. Dev Biol 347 247–257. (https://doi.org/10.1016/j.ydbio.2010.08.005)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kovacevic I, Orozco JM & Cram EJ 2013 Filamin and phospholipase C-ɛ are required for calcium signaling in the Caenorhabditis elegans spermatheca. PLoS Genet 9 e1003510. (https://doi.org/10.1371/journal.pgen.1003510)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lambert CC 2009 Ascidian follicle cells: multifunctional adjuncts to maturation and development. Dev Growth Differ 51 677–686. (https://doi.org/10.1111/j.1440-169X.2009.01127.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lebouvier M, Miramón-Puértolas P & Steinmetz PRH 2022 Evolutionarily conserved aspects of animal nutrient uptake and transport in sea anemone vitellogenesis. Curr Biol 32 4620–4630.e5. (https://doi.org/10.1016/j.cub.2022.08.039)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lee HG, Seong CS, Kim YC, et al. 2003 Octopamine receptor OAMB is required for ovulation in Drosophila melanogaster. Dev Biol 264 179–190. (https://doi.org/10.1016/j.ydbio.2003.07.018)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lee HG, Rohila S & Han KA 2009 The octopamine receptor OAMB mediates via Ca2+/calmodulin-dependent protein kinase II in the Drosophila oviduct epithelium. PLoS One 4 e4716. (https://doi.org/10.1371/journal.pone.0004716)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Leys SP & Riesgo A 2011 Epithelia, an evolutionary novelty of metazoans. J Exp Zoolog B Mol Dev Evol 318 438–447. (https://doi.org/10.1002/jez.b.21442)

  • Leys SP, Nchols SA & Adams EDM 2009 Epithelia and integration in sponges. Integr Comp Biol 49 167–177. (https://doi.org/10.1093/icb/icp038)

  • Li R & Albertini DF 2013 The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol 14 141–152. (https://doi.org/10.1038/nrm3531)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Li Y, Shen XX, Evans B, et al. 2021 Rooting the animal tree of life. Mol Biol Evol 38 4322–4333. (https://doi.org/10.1093/molbev/msab170)

  • Liao S & Nässel DR 2020 Drosophila insulin-like peptide 8 (DILP8) in ovarian follicle cells regulates ovulation and metabolism. Front Endocrinol 11 461. (https://doi.org/10.3389/fendo.2020.00461)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lim J, Sabandal PR, Fernandez A, et al. 2014 The octopamine receptor Octβ2R regulates ovulation in Drosophila melanogaster. PLoS One 9 e104441. (https://doi.org/10.1371/journal.pone.0104441)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Luo W, Liu S, Zhang W, et al. 2021 Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes. Proc Natl Acad Sci U S A 118 e2104461118. (https://doi.org/10.1073/pnas.2104461118)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Magie CR & Martindale MQ 2008 Cell–cell adhesion in the Cnidaria: insights into the evolution of tissue morphogenesis. Biol Bull 214 218–232. (https://doi.org/10.2307/25470665)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mahowald AP, Goralski TJ & Caulton JH 1983 In vitro activation of Drosophila eggs. Dev Biol 98 437–445. (https://doi.org/10.1016/0012-1606(83)90373-1)

  • Masui Y 2001 From oocyte maturation to the in vitro cell cycle: the history of discoveries of maturation-promoting factor (MPF) and cytostatic factor (CSF). Differentiation 69 1–17. (https://doi.org/10.1046/j.1432-0436.2001.690101.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Matsubara S, Shiraishi A, Osugi T, et al. 2019 The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates. Elife 8 e49062. (https://doi.org/10.7554/eLife.49062)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • McCarter J, Bartlett B, Dang T, et al. 1999 On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205 111–128. (https://doi.org/10.1006/dbio.1998.9109)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • McGovern M, Castaneda PG, Pekar O, et al. 2018 The DSL ligand APX-1 is required for normal ovulation in C. elegans. Dev Biol 435 162–169. (https://doi.org/10.1016/j.ydbio.2018.01.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Meethal SV & Atwood CS 2005 The role of hypothalamic-pituitary-gonadal hormones in the normal structure and functioning of the brain. Cell Mol Life Sci 62 257–270. (https://doi.org/10.1007/s00018-004-4381-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mesnier M 1981 Study of the ovulation process in the stick insect, Clitumnus extradentatus. J Insect Physiol 27 425–433. (https://doi.org/10.1016/0022-1910(81)90022-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Meyer A & Van de Peer Y 2005 From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27 937–945. (https://doi.org/10.1002/bies.20293)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Middleton CA, Nongthomba U, Parry K, et al. 2006 Neruomuscular organization and aminergic modulation of contractions in the Drosophila ovary. BMC Biol 4 17. (https://doi.org/10.1186/1741-7007-4-17)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Miller A 1994 The internal anatomy and histology of the imago of Drosophila melanogaster. In Biology of Drosophila, ch 6, pp 420–534. Ed M Demerec. Long Island, New York: Cold Spring Harbor Laboratory Press.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Miller MA, Nguyen VQ, Lee MH, et al. 2001 A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291 2144–2147. (https://doi.org/10.1126/science.1057586)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mita M 2019 Starfish gonadotropic hormone: from gamete-shedding substance to relaxin-like gonad-stimulating peptide. Front Endocrinol 10 182. (https://doi.org/10.3389/fendo.2019.00182)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mita M, Yoshikuni M, Ohno K, et al. 2009 A relaxin-like peptide purified from radial nerves induces oocyte maturation and ovulation in the starfish, Asterina pectinifera. Proc Natl Acad Sci U S A 106 9507–9512. (https://doi.org/10.1073/pnas.0900243106)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mita M, Matsubara S, Osugi T, et al. 2020 A novel G protein-coupled receptor for starfish gonadotropic hormone, relaxin-like gonad-stimulating peptide. PLoS One 15 e0242877. (https://doi.org/10.1371/journal.pone.0242877)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mokhtar DM & Hussein MM 2020 Microanalysis of fish ovarian follicular atresia: a possible synergic action of somatic and immune cells. Microsc Microanal 26 599–608. (https://doi.org/10.1017/S1431927620001567)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Monastirioti M 2003 Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. Dev Biol 264 38–49. (https://doi.org/10.1016/j.ydbio.2003.07.019)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Monastirioti M, Linn CE Jr & White K 1996 Characterization of Drosophila tyramine β-hudroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci 16 3900–3911. (https://doi.org/10.1523/JNEUROSCI.16-12-03900.1996)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mora JM, Fenwick MA, Castle L, et al. 2012 Characterization and significance of adhesion and junction-related proteins in mouse ovarian follicles. Biol Reprod 86 1–14. (https://doi.org/10.1095/biolreprod.111.096156)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Moser M, Legate KR, Zent R, et al. 2009 The tail of integrins, talin, and kindlins. Science 324 895–899. (https://doi.org/10.1126/science.1163865)

  • Müller WEG 2006 The stem cell concept in sponges (Porifera): metazoan traits. Semin Cell Dev Biol 17 481–491. (https://doi.org/10.1016/j.semcdb.2006.05.006)

  • Müller WEG, Korzhev M, Le Pennec G, et al. 2003 Origin of metazoan stem cell system in sponges: first approach to establish the model (Suberites domuncula). Biomol Eng 20 369–379. (https://doi.org/10.1016/S1389-0344(03)00055-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nagahama Y 1983 The functional morphology of teleost gonads. In Fish Physiology, vol IX, pp 223–275. Eds WS Hoar, DJ Randall & EM Donaldson. New York: Academic Press.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nagahama Y & Yamashita M 2008 Regulation of oocyte maturation in fish. Dev Growth Differ 50 S195–S-219. (https://doi.org/10.1111/j.1440-169X.2008.01019.x)

  • Nagyova E 2015 Organization of the expanded cumulus-extracellular matrix in preovulatory follicles: a role for inter-alpha-trypsin inhibitor. Endocr Regul 49 37–45. (https://doi.org/10.4149/endo_2015_01_37)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Newmark PA & Alvarado AS 2002 Not your father's planarian: a classic model enters the era of functional genomics. Nat Rev Genet 3 210–219. (https://doi.org/10.1038/nrg759)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Newmark PA, Wang Y & Chong T 2008 Germ cell specification and regeneration in planarians. Cold Spring Harb Symp Quant Biol 73 573–581. (https://doi.org/10.1101/sqb.2008.73.022)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nili H & Kelly WR 1996 Form and function of lacunae in the ovary of the laying hen. Anat Rec 244 165–174. (https://doi.org/10.1002/(SICI)1097-0185(199602)244:2<165::AID-AR4>3.0.CO;2-0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nilsson IBM, Svensson SP & Monstein HJ 2003 Molecular cloning of a putative Ciona intestinalis cionin receptor, a new member of the CCK/gastrin receptor family. Gene 323 79–88. (https://doi.org/10.1016/j.gene.2003.09.002)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nishiyama T, Tachibana K & Kishimoto T 2010 Cytostatic arrest: post-ovulation arrest until fertilization in metazoan oocytes. In Oogenesis: The Universal Process, ch 14, pp 357–384. Eds M-H Verlhac & A Villeneuve. Wiley-Blackwell. (https://doi.org/10.1002/9780470687970.ch14)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Noma N, Kawashima I, Fan HY, et al. 2011 LH-induced neuregulin 1 (NRG1) type III transcripts control granulosa cell differentiation and oocyte maturation. Mol Endocrinol 25 104–116. (https://doi.org/10.1210/me.2010-0225)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Norris DO & Carr JA 2013 The hypothalamus-pituitary system in non-mammalian vertebrates. In Vertebrate Endocrinology, 5th ed. pp 151–205. Amsterdam: Elsevier.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • O’shea JD 1981 Structure–function relationships in the wall of the ovarian follicle. Aust J Biol Sci 34 379–394. (https://doi.org/10.1071/bi9810379)

  • Ogiwara K & Takahashi T 2016 A dual role for melatonin in medaka ovulation: ensuring prostaglandin synthesis and actin cytoskeleton rearrangement in follicular cells. Biol Reprod 94 64. (https://doi.org/10.1095/biolreprod.115.133827)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ogiwara K & Takahashi T 2017 Involvement of the nuclear progestin receptor in LH-induced expression of membrane type 2-matrix metalloproteinase required for follicle rupture during ovulation in the medaka, Oryzias latipes. Mol Cell Endocrinol 450 54–63. (https://doi.org/10.1016/j.mce.2017.04.016)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ogiwara K, Takano N, Shinohara M, et al. 2005 Gelatinase A and membrane-type matrix met alloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka. Proc Natl Acad Sci U S A 102 8442–8447. (https://doi.org/10.1073/pnas.0502423102)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ogiwara K, Hagiwara A, Rajapakse S, et al. 2015 The role of urokinase plasminogen activator and plasminogen activator inhibitor-1 in follicle rupture during ovulation in the teleost medaka. Biol Reprod 92 10. (https://doi.org/10.1095/biolreprod.114.121442)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ogiwara K, Hoyagi M & Takahashi T 2021 A central role for cAMP/EPAC/RAP/PI3K/AKT/CREB signaling in LH-induced follicular Pgr expression at medaka ovulation. Biol Reprod 105 413–426. (https://doi.org/10.1093/biolre/ioab077)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ogiwara K, Fujimori C & Takahashi T 2023 The PGE2/Ptger4b pathway regulates ovulation by inducing intracellular actin cytoskeleton rearrangement via the rho/rock pathway in the granulosa cells of periovulatory follicles in the teleost medaka. Mol Cell Endocrinol 560 111816. (https://doi.org/10.1016/j.mec.2022.111816)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Okada T & Yamamoto M 1993 Identification of early oogenetic cells in the solitary ascidians, Ciona savignyi and Ciona intestinalis: an immunoelectron microscopic study. Dev Growth Differ 35 495–506. (https://doi.org/10.1111/j.1440-169X.1993.00495.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Olive PJW 1983 Annelida. In Reproductive Biology of Invertebrates, Vol. 1, Oogenesis, Oviposition, and Oosorption, pp 357–422. Eds KG Adiyodi & RG Adiyodi. New York: John Wiley and Sons.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ono K, Yu R & Ono S 2007 Structural components of the nonstriated contractile apparatuses in the Caenorhabditis elegans gonadal myoepithelial sheath and their essential roles for ovulation. Dev Dyn 236 1093–1105. (https://doi.org/10.1002/dvdy.21091)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Osugi T, Miyasaka N, Shiraishi A, et al. 2021 Cionin, a vertebrate cholecystokinin/gastrin homolog, induces ovulation in the ascidian Ciona intestinalis type A. Sci Rep 11 10911. (https://doi.org/10.1038/s41598-021-90295-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pan B & Li J 2019 The art of oocyte meiotic arrest regulation. Reprod Biol Endocrinol 17 8. (https://doi.org/10.1186/s12958-018-0445-8)

  • Pennati R, Ficetola GF, Brunetti R, et al. 2015 Morphological differences between larvae of the Ciona intestinalis species complex: hints for a valid taxonomic definition of distinct species. PLoS One 10 e0122879. (https://doi.org/10.1371/journal.pone.0122879)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Park JY, Su YQ, Ariga M, et al. 2004 EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303 682–684. (https://doi.org/10.1126/science.1092463)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Parrinello D, Sanfratello MA, Parisi MG, et al. 2018 In the ovary of Ciona intestinalis (type A), immune-related galectin and phenoloxidase genes are differentially expressed by the follicle accessory cells. Fish Shellfish Immunol 72 452–458. (https://doi.org/10.1016/j.fsi.2017.11.023)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Paulus W 1989 Ultrastructural investigation of spermatogenesis in Spongilla lacustris and Ephydatia fluviatilis (Porifera, Spongillidae). Zoomorphology 109 123–130. (https://doi.org/10.1007/BF00312264)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pendergrass P & Schroeder PC 1976 The ultrastructure of the thecal cells of the teleost, Oryzias latipes, during ovulation in vitro. J Reprod Fertil 47 229–233. (https://doi.org/10.1530/jrf.0.0470229)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pinder AM & Ohtaka A 2004 Annelida: Clitellata, Oligochaeta. In Freshwater Invertebrates of the Malaysian Region, pp 162–174. Eds CM Yule & HS Yong. Kuala Lumpur, Malyasia: Academy of Sciences Malaysia.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pongratz N, Storhas M, Carranza S, et al. 2003 Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations. BMC Evol Biol 3 23. (https://doi.org/10.1186/1471-2148-3-23)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rajkovic A, Pangas SA & Matzuk MM 2006 Follicular development: mouse, sheep, and human models. In Physiology of Reproduction, vol 1, 3rd ed, pp 383–423. Ed JD Neill. Amsterdam: Academic Press. (https://doi.org/10.1016/b978-012515400-0/50015-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ravi V & Venkatesh B 2008 Rapidly evolving fish genomes and teleost diversity. Curr Opin Genet Dev 18 544–550. (https://doi.org/10.1016/j.gde.2008.11.001)

  • Reddien PW 2018 The cellular and molecular basis for planarian regeneration. Cell 175 327–345. (https://doi.org/10.1016/j.cell.2018.09.021)

  • Redmond AK & McLysaght A 2021 Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding. Nat Commun 12 1783. (https://doi.org/10.1038/s41467-021-22074-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Richards JS & Ascoli M 2018 Endocrine, paracrine, and autocrine signaling pathways that regulate ovulation. Trends Endocrinol Metab 29 313–325. (https://doi.org/10.1016/j.tem.2018.02.012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Richards JS, Russell DL, Ochsner S, et al. 2002 Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu Rev Physiol 64 69–92. (https://doi.org/10.1146/annurev.physiol.64.081501.131029)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Richards JS, Liu Z & Shimada M 2015 Ovulation. In Physiology of Reproduction, 4th ed, vol 1, pp 997–1021. Eds TM Plant & AJ Zeleznik. Amsterdam: Academic Press. (https://doi.org/10.1016/B978-0-12-397175-3.00022-3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Riddiford LM, Cherbas P & Truman JW 2000 Ecdysone receptors and their biological actions. Vitam Horm 60 1–73. (https://doi.org/10.1016/s0083-6729(00)60016-x)

  • Riesgo A & Maldonado M 2009 Ultrastructure of oogenesis of two oviparous demonsponges: Axinella damicornis and Raspaciona aculeata (Porifera). Tissue Cell 41 51–65. (https://doi.org/10.1016/j.tice.2008.07.004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Riesgo A, Taylor C & Leys SP 2007 Reproduction in a carnivorous sponge: the significance of the absence of an aquiferous system to the sponge body plan. Evol Dev 9 618–631. (https://doi.org/10.1111/j.1525-142X.2007.00200.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Robker RL, Akison LK & Russell DL 2009 Control of oocyte release by progesterone receptor-regulated gene expression. Nucl Recept Signal 7 e012. (https://doi.org/10.1621/nrs.07012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Robker RL, Hennebold JD & Russell DL 2018 Coordination of ovulation and oocyte maturation: a good egg at the right time. Endocrinology 159 3209–3218. (https://doi.org/10.1210/en.2018-00485)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rodriguez-Pascual F & Slatter DA 2016 Collagen cross-linking: insights on the evolution of metazoan extracellular matrix. Sci Rep 6 37374. (https://doi.org/10.1038/srep37374)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rodgers LS & Fanning AS 2011 Regulation of epithelial permeability by the actin cytoskeleton. Cytoskeleton 68 653–660. (https://doi.org/10.1002/cm.20547)

  • Rubinstein CD & Wolfner MF 2013 Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling. Proc Natl Acad Sci U S A 110 17420–17425. (https://doi.org/10.1073/pnas.1220018110)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rübsam M, Broussard JA, Wickström SA, et al. 2018 Adherens junctions and desmosomes coordinate mechanics and signaling to orchestrate tissue morphogenesis and function: an evolutionary perspective. Cold Spring Harb Perspect Biol 10 a029207. (https://doi.org/10.1101/cshperspect.a029207)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ruppert EE 2005 Key characters uniting hemichordates and chordates: homologies or homoplasies? Can J Zoolog 83 8–23. (https://doi.org/10.1139/z04-158)

  • Russo GL, Kyozuka K, Antonazzo L, et al. 1996 Maturation promoting factor in ascidian oocytes is regulated by different intracellular signals at meiosis I and II. Development 122 1995–2003. (https://doi.org/10.1242/dev.122.7.1995)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ryan JF, Pang K, Schnitzler CE, et al. 2013 The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342 1242592. (https://doi.org/10.1126/science.1242592)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Saller U 1988 Oogenesis and larval development of Ephydatia fluviatilis (Porifera, Spongillidae). Zoomorphology 108 23–28. (https://doi.org/10.1007/BF00312211)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Satake H & Sasakura Y 2024 The neuroendocrine system of Ciona intestinalis type A, a deuterostome invertebrate and the closest relative of vertebrates. Mol Cell Endocrinol 582 112122. (https://doi.org/10.1016/j.mce.2023.112122)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Satake H, Kawada T, Osugi T, et al. 2024 Ovarian follicle development in ascidians. Zoolog Sci 41 60–67. (https://doi.org/10.2108/zs230054)

  • Sato Y, Terakado K & Morisawa M 1997 Test cell migration and tunic formation during post-hatching development of the larva of the ascidian, Ciona intestinalis. Dev Growth Differ 39 117–126. (https://doi.org/10.1046/j.1440-169x.1997.00013.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sato A, Satoh N & Bishop JDD 2012 Field identification of ‘types’ A and B of the ascidian Ciona intestinalis in a region of sympatry. Mar Biol 159 1611–1619. (https://doi.org/10.1007/s00227-012-1898-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Satoh N, Numakunai T & Hori R 1982 Behavior and cellular morphology of the test cells during embryogenesis of the ascidian Halocynthia roretzi. J Morphol 171 219–223. (https://doi.org/10.1002/jmor.1051710209)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Schoenmakers HJ, Colenbrander PH, Peute J, et al. 1981 Anatomy of the ovaries of the starfish Asterias rubens (Echinoermata). A histological and ultrastructural study. Cell Tissue Res 217 577–597. (https://doi.org/10.1007/BF00219366)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Schroeder PC 1971 Active contraction of starfish oocyte follicle cells after treatment with 1-methyladenine. Naturwissenschaften 58 270–272. (https://doi.org/10.1007/BF00602999)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Schroeder TE & Stricker SA 1983 Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev Biol 98 373–384. (https://doi.org/10.1016/0012-1606(83)90366-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Schroeder PC & Talbot P 1985 Ovulation in the animal kingdom: a review with an emphasis on the role of contractile processes. Gamete Res 11 191–221. (https://doi.org/10.1002/mrd.1120110209)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Schroeder PC, Larsen JH Jr & Waldo AE 1979 Oocyte–follicle cell relationships in a starfish. Cell Tissue Res 203 249–256. (https://doi.org/10.1007/BF00237239)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sciscioli M, Liaci LS, Lepore E, et al. 1991 Ultrastructural study of the mature eggs of the marine sponge Stelletta grubii (Porifera Demospongiae). Mol Reprod Dev 28 346–350. (https://doi.org/10.1002/mrd.1080280406)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sekiguchi T, Ogasawara M & Satake H 2012 Molecular and functional characterization of cionin receptors in the ascidian, Ciona intestinalis: the evolutionary origin of the vertebrate cholecystokinin/gastrin family. J Endocrinol 213 99–106. (https://doi.org/10.1530/JOE-11-0410)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Senthilkumaran B 2011 Recent advances in meiotic maturation and ovulation: comparing mammals and pisces. Front Biosci 16 1898–1914. (https://doi.org/10.2741/3829)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Seybold A, Salvenmoser W & Hobmayer B 2016 Sequential development of apical-basal and planar polarities in aggregating epitheliomuscular cells of Hydra. Dev Biol 412 148–159. (https://doi.org/10.1016/j.ydbio.2016.02.022)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, et al. 2006 Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol 20 1352–1365. (https://doi.org/10.1210/me.2005-0504)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shimizu T 1976 The fine structure of the Tubifex egg before and after fertilization. J Fac Sci Hokkaido Univ Ser VI, Zoolog 20 253–262.

  • Siebert S & Juliano CE 2017 Sex, polyps, and medusae: determination and maintenance of sex in cnidarians. Mol Reprod Dev 84 105–119. (https://doi.org/10.1002/mrd.22690)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Siekierska E 2003 The structure of the ovary and oogenesis in the earthworm, Dendrobaena veneta (Annelida, Clitellata). Tissue Cell 35 252–259. (https://doi.org/10.1016/s0040-8166(03)00038-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Silvestre F, Cuomo A & Tosti E 2009 Ion current activity and molecules modulating maturation and growth stages of ascidian (Ciona intestinalis) oocytes. Mol Reprod Dev 76 1084–1093. (https://doi.org/10.1002/mrd.21073)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Simpson TL 1984 Gamete, embryo, larval development. In The Cell Biology of Sponges, pp 341–413. Ed TL Simpson. Berlin: Springer Verlag.

  • Spradling AC 1993 Developmental genetics of oogenesis. In The Development of Drosophila melanogaster, pp 1–70. Eds M Bate & AM Arias. Long Island, New York: Cold Spring Harbor Laboratory Press.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Starich TA, Hall DH & Greenstein D 2014 Two classes of gap junction channels mediate soma-germline interactions essential for germline proliferation and gametogenesis in Caenorhabditis elegans. Genetics 198 1127–1153. (https://doi.org/10.1534/genetics.114.168815)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Steele RE 2022 Vitellogenesis: the evolutionary origins of nutrient uptake in animals. Curr Biol 32 R1233–R1235. (https://doi.org/10.1016/j.cub.2022.09.020)

  • Strączyńska P, Papis K, Morawiec E, et al. 2022 Signaling mechanisms and their regulation during in vivo or in vitro maturation of mammalian oocytes. Reprod Biol Endocrinol 20 37. (https://doi.org/10.1186/s12958-022-00906-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Strand NS, Allen JM & Zayas RM 2019 Post-translational regulation of planarian regeneration. Semin Cell Dev Biol 87 58–68. (https://doi.org/10.1016/j.semcdb.2018.04.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Strome S 1986 Fluorescence visualization of the distribution of microfilaments in gonads and early embryos of the nematode Caenorhabditis elegans. J Cell Biol 103 2241–2252. (https://doi.org/10.1083/jcb.103.6.2241)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sugino YM, Tomonaga A & Takashima Y 1987 Differentiation of the accessory cells and structural regionalization of the oocyte in the ascidinan Ciona savignyi during early oogenesis. J Exp Zoolog 242 205–214. (https://doi.org/10.1002/jez.1402420212)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sugino YM, Tomonaga A, Takashima Y, et al. 1990 Early oogenesis in the ascidian Ciona savignyi. Invertebr Reprod Dev 17 165–170.

  • Sun J & Spradling AC 2013 Ovulation in Drosophila is controlled by secretory cells of the female reproductive tract. ELife 2 e00415. (https://doi.org/10.7554/eLife.00415)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sundaresan NR, Saxena VK, Sastry KVH, et al. 2008 Cytokines and chemokines in postovulatory follicle regression of domestic chicken (Gallus gallus domesticus). Dev Comp Immunol 32 253–264. (https://doi.org/10.1016/j.dci.2007.05.011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Świątek P, Kubrakiewicz J & Klag J 2009 Formation of germ-line cysts with a central cytoplasmic core is accompanied by specific orientation of mitotic spindles and partitioning of existing intercellular bridges. Cell Tissue Res 337 137–148. (https://doi.org/10.1007/s00441-009-0788-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Świątek P, Pinder A & Gajda Ł 2019 Description of ovary organization and oogenesis in a phreodrilid clitellate. J Morphol 281 81–94. (https://doi.org/10.1002/jmor.21081)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Takahashi T & Ogiwara K 2021 Roles of melatonin in the teleost ovary: a review of the current status. Comp Biochem Physiol A Mol Integr Physiol 254 110907. (https://doi.org/10.1016/j.cbpa.2021.110907)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Takahashi T & Ogiwara K 2022 Signal pathway of LH-induced expression of nuclear progestin receptor in vertebrate ovulation. Gen Comp Endocrinol 321–322 114025. (https://doi.org/10.1016/j.ygcen.2022.114025)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Takahashi T & Ogiwara K 2023 cAMP signaling in ovarian physiology in teleosts: a review. Cell Signal 101 110499. (https://doi.org/10.1016/j.cellsig.2022.110499)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Takahashi T, Hagiwara A & Ogiwara K 2018 Prostaglandins in teleost ovulation: a review of the roles with a view to comparison with prostaglandins in mammalian ovulation. Mol Cell Endocrinol 461 236–247. (https://doi.org/10.1016/j.mce.2017.09.019)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Takahashi T, Hagiwara A & Ogiwara K 2019 Follicle rupture during ovulation with an emphasis on recent progress in fish models. Reproduction 157 R1–R13. (https://doi.org/10.1530/REP-18-0251)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Takeda N, Kon Y, Quiroga Artigas G, et al. 2018 Identification of jellyfish neuropeptides that act directly as oocyte maturation-inducing hormones. Development 145 156786. (https://doi.org/10.1242/dev.156786)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tang H, Liu Y, Li J, et al. 2016 Gene knockout of nuclear progesterone receptor provides insights into the regulation of ovulation by LH signaling in zebrafish. Sci Rep 6 28545. (https://doi.org/10.1038/srep28545)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tardent P & Holstein T 1982 Morphology and morphodynamics of the stenotele nematocyte of Hydra attenuata Pall. (Hydrozoa, Cnidaria). Cell Tissue Res 224 269–290. (https://doi.org/10.1007/BF00216873)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Technau U & Steele RE 2011 Evolutionary crossroads in developmental biology: Cnidaria. Development 138 1447–1458. (https://doi.org/10.1242/dev.048959)

  • Telford MJ, Budd GE & Philippe H 2015 Phylogenomic insights into animal evolution. Curr Biol 25 R876–R887. (https://doi.org/10.1016/j.cub.2015.07.060)

  • Telford MJ, Moroz LL & Halanych K 2016 Evolution: a sisterly dispute. Nature 529 286–287. (https://doi.org/10.1038/529286a)

  • Thibault C & Levasseur MC 1988 Ovulation. Hum Reprod 3 513–523. (https://doi.org/10.1093/oxfordjournals.humrep.a136737)

  • Thomas P 2012 Rapid steroid hormone actions initiated at the cell surface and the receptors that mediate them with an emphasis on recent progress in fish models. Gen Comp Endocrinol 175 367–383. (https://doi.org/10.1016/j.ygcen.2011.11.032)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Thompson H & Shimeld SM 2015 Transmission and scanning electron microscopy of the accessory cells and chorion during development of Ciona intestinalis type B embryos and the impact of their removal on cell morphology. Zoolog Sci 32 217–222. (https://doi.org/10.2108/zs140231)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Thummel CS 1996 Flies on steroids – Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet 12 306–310. (https://doi.org/10.1016/0168-9525(96)10032-9)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tingaud-Sequeira A, Chauvigné F, Lozano J, et al. 2009 New insights into molecular pathways associated with flatfish ovarian development and atresia revealed by transcriptional analysis. BMC genomics 10 434. (https://doi.org/10.1186/1471-2164-10-434)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tokmakov AA, Matsumoto Y, Isobe T, et al. 2019 In vitro reconstitution of Xenopus oocyte ovulation. Int J Mol Sci 20 4766. (https://doi.org/10.3393/ijms20194766)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tucker RP & Adams JC 2014 Adhesion networks of Cnidarians: a postgenomic view. Int Rev Cell Mol Biol 308 323–377. (https://doi.org/10.1016/B978-0-12-800097-7.00008-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tunquist BJ & Maller JL 2003 Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev 17 683–710. (https://doi.org/10.1101/gad.1071303)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Turathum B, Gao EM & Chian RC 2021 The function of cumulus cells in oocyte growth and maturation and in subsequent ovulation and fertilization. Cells 10 2292. (https://doi.org/10.3390/cells10092292)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Urbisz AZ, Krodkiewska M & Świątek P 2010 Ovaries of Tubificinae (Clitellata, Naididae) resemble ovary cords found in Hirudinea (Clitellata). Zoomorphology 129 235–247. (https://doi.org/10.1007/s00435-010-0116-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Urbisz AZ, Świątek P & Chajec Ł 2015 The ovary of Tubifex tubifex (Clitellata, Naididae, Tubificinae) is composed of one, huge germ-line cyst that is enriched with cytoskeletal components. PLoS One 10 e0126173. (https://doi.org/10.1371/journal.pone.0126173)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Urbisz AZ, Martin P, Lagnika M, et al. 2020 Microorganization of ovaries and oogenesis of Haplotaxis sp. (Clitellata: Haplotaxidae). J Morphol 282 98–114. (https://doi.org/10.1002/jmor.21285)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Van Minnen J, Smit AB & Joosse J 1989 Central and peripheral expression of genes coding for egg-laying inducing and insulin-related peptides in a snail. Arch Histology Cytol 52 (Supplement) 241–252. (https://doi.org/10.1679/aohc.52.suppl_241)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vanni V, Ballarin L, Gasparini F, et al. 2022 Studying regeneration in ascidians: an historical overview. Methods Mol Biol 2450 27–48. (https://doi.org/10.1007/978-1-0716-2172-1_2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Villa LA & Patricolo E 2000 The follicle cells of Styela plicata (Ascidiacea Tunicata): a sem study. Zoolog Sci 17 1115–1121. (https://doi.org/10.2018/zsj.17.1115)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Von Stetina JR & Orr-Weaver TL 2011 Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harbor Perspect Biol 3 a005553. (https://doi.org/10.1101/cshperspect.a005553)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Walker CW 1974 Studies on the reproductive systems of sea-stars. I. The morphology and histology of the gonad of Asterias vulgaris. Biol Bull 147 661–677. (https://doi.org/10.2307/1540749)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Walker CW 1975 Studies on the reproductive systems of sea-stars. II. The morphology and histology of the gonoduct of Asterias vulgaris. Biol Bull 148 461–471. (https://doi.org/10.2307/1540522)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Walzem RL & Chen SE 2014 Obesity-induced dysfunctions in female reproduction; lessons from birds and mammals. Adv Nutr 5 199–206. (https://doi.org/10.3945/an.113.004747)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ward S & Carrel JS 1979 Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73 304–321. (https://doi.org/10.1016/0012-1606(79)90069-1)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Watanabe Y 1978 The development of two species of Tetilla (Demosponge). In Natural Science Report of the Ochanomizu University, vol 29, pp 71–106. Ochanomizu, Tokyo, Japan: Ochanomizu University.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Weber GF, Bjerke MA & DeSimone DW 2011 Integrins and cadherins join forces to form adhesive networks. J Cell Sci 124 1183–1193. (https://doi.org/10.1242/jcs.064618)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • West DL 1978 The epitheliomuscular cell of hydra: its fine structure, three-dimensional architecture and relation to morphogenesis. Tissue Cell 10 629–646. (https://doi.org/10.1016/0040-8166(78)90051-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • White A, Fearon A & Johnson CM 2012 HLH-29 regulates ovulation in C. elegans by targeting genes in the inositol triphosphate signaling pathway. Biol Open 1 261–268. (https://doi.org/10.1242/bio.2012046)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wörheide G, Dohrmann M, Erpenbeck D, et al. 2012 Deep phylogny and evolution of sponges (phylum Porifera). Adv Mar Biol 61 1–78. (https://doi.org/10.1016/B978-0-12-387787-1.00007-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wu X, Tanwar PS & Raftery LA 2008 Drosophila follicle cells: morphogenesis in an eggshell. Semin Cell Dev Biol 19 271–282. (https://doi.org/10.1016/j.semcdb.2008.01.004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yamashita Y & Shimada M 2010 The release of EGF domain from EGF-like factors by a specific cleavage enzyme activates EGFR-MAPK3/1 pathway in both granulosa cells and cumulus cells during the ovulatory process. J Reprod Dev 58 510–514. (https://doi.org/10.1262/jrd.2012-056)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yamashita Y, Hishinuma M & Shimada M 2009 Activation of PKA, p38 MAPK and ERK1/2 by gonadotropins in cumulus cells is critical for induction of EGF like factor and TACE/ADAM17 gene expression during in vitro maturation of porcine COCs. J Ovarian Res 2 20. (https://doi.org/10.1186/1757-2215-2-20)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yap AS, Gomez GA & Parton RG 2015 Adherens junctions revisualized: organizing cadherins as nanoassemblies. Dev Cell 35 12–20. (https://doi.org/10.1016/j.devcel.2015.09.012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yin X, Gower NJD, Baylis HA, et al. 2004 Inositol 1,4,5-trisphosphate signaling regulates rhythmic contractile activity of myoepithelial sheath cells in Caenorhabditis elegans. Mol Biol Cell 15 3938–3949. (https://doi.org/10.1091/mbc.E04-03-0198)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhang M, Su YQ, Sugiura K, et al. 2010 Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330 366–369. (https://doi.org/10.1126/science.1193573)

    • PubMed
    • Search Google Scholar
    • Export Citation