Age-dependent high-yield isolation of primordial, primary, and early secondary follicles from the bovine ovarian cortex

in Reproduction
Authors:
Noemi Monferini Reproductive and Developmental Biology Laboratory (ReDBioLab), Department of Veterinary Medicine and Animal Sciences, University of Milan, Milan, Italy

Search for other papers by Noemi Monferini in
Current site
Google Scholar
PubMed
Close
,
Pritha Dey Reproductive and Developmental Biology Laboratory (ReDBioLab), Department of Veterinary Medicine and Animal Sciences, University of Milan, Milan, Italy

Search for other papers by Pritha Dey in
Current site
Google Scholar
PubMed
Close
,
Ludovica Donadini Reproductive and Developmental Biology Laboratory (ReDBioLab), Department of Veterinary Medicine and Animal Sciences, University of Milan, Milan, Italy

Search for other papers by Ludovica Donadini in
Current site
Google Scholar
PubMed
Close
,
Niki Katsakoglou Reproductive and Developmental Biology Laboratory (ReDBioLab), Department of Veterinary Medicine and Animal Sciences, University of Milan, Milan, Italy

Search for other papers by Niki Katsakoglou in
Current site
Google Scholar
PubMed
Close
,
Federica Franciosi Reproductive and Developmental Biology Laboratory (ReDBioLab), Department of Veterinary Medicine and Animal Sciences, University of Milan, Milan, Italy

Search for other papers by Federica Franciosi in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0001-8742-0291
,
Valentina Lodde Reproductive and Developmental Biology Laboratory (ReDBioLab), Department of Veterinary Medicine and Animal Sciences, University of Milan, Milan, Italy

Search for other papers by Valentina Lodde in
Current site
Google Scholar
PubMed
Close
, and
Alberto Maria Luciano Reproductive and Developmental Biology Laboratory (ReDBioLab), Department of Veterinary Medicine and Animal Sciences, University of Milan, Milan, Italy

Search for other papers by Alberto Maria Luciano in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-8016-9919

Correspondence should be addressed to A M Luciano; Email: alberto.luciano@unimi.it

*(N Monferini and P Dey contributed equally to this work)

Restricted access
Rent on DeepDyve

Sign up for journal news

In brief

Preantral follicles constitute the largest follicle reserve in the mammalian ovary. This study assesses a mechanical isolation method to maximize the number of follicles retrieved from a defined cortex volume.

Abstract

Primordial, primary, and secondary follicles (collectively defined as preantral follicles) constitute the most abundant source of gametes inside the mammalian ovarian cortex. The massive isolation of preantral follicles and the refinement of stage-specific protocols for in vitro follicle growth would provide a powerful tool to boost the rescue and restoration of fertility in assisted reproduction interventions in human medicine, animal breeding, and vulnerable species preservation. Nevertheless, together with an efficient culture system, the most significant limitation to implementing in vitro follicle growth is the lack of an efficient method to isolate viable and homogeneous subpopulations of primordial, primary, and secondary follicles suitable for in vitro culture. Our study provides a strategy for high-yielding mechanical isolation of primordial, primary, and early secondary follicles from a limited portion of the ovarian cortex in the bovine animal model. In the first part of the study, we refined a mechanical isolation protocol of preantral follicles, adopting specific methodological strategies to separate viable and distinct subpopulations of primordial (oblate and prolate forms), primary, and early secondary follicles from 0.16 cm3 of the ovarian cortex. In the second part of the study, we tested the effectiveness of the isolation protocol, considering the individual’s age as a critical factor, bearing in mind the progressive decrease in the ovarian reserve that naturally accompanies the reproductive life span. Our study provides a way for designing quantitative and conservative fertility preservation approaches to preserve organ function and minimize the invasiveness of the interventions, also considering age-related differences.

 

  • Collapse
  • Expand
  • Adams GP & & Pierson RA 1995 Bovine model for study of ovarian follicular dynamics in humans. Theriogenology 43 113120. (https://doi.org/10.1016/0093-691X(9400015-M)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Adeniran BV, Bjarkadottir BD, Appeltant R, Lane S & & Williams SA 2021 Improved preservation of ovarian tissue morphology that is compatible with antigen detection using a fixative mixture of formalin and acetic acid. Human Reproduction 36 18711890. (https://doi.org/10.1093/humrep/deab075)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Aerts JM, Oste M & & Bols PE 2005 Development and practical applications of a method for repeated transvaginal, ultrasound-guided biopsy collection of the bovine ovary. Theriogenology 64 947957. (https://doi.org/10.1016/j.theriogenology.2005.01.011)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Aerts J, Martinez-Madrid B, Flothmann K, De Clercq J, Van Aelst S & & Bols P 2008 Quantification and viability assessment of isolated bovine primordial and primary ovarian follicles retrieved through a standardized biopsy pick-up procedure. Reproduction in Domestic Animals 43 360366. (https://doi.org/10.1111/j.1439-0531.2007.00915.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Alves BG, Alves KA, Gastal GDA, Gastal MO, Figueiredo JR & & Gastal EL 2018 Spatial distribution of preantral follicles in the equine ovary. PLoS One 13 e0198108. (https://doi.org/10.1371/journal.pone.0198108)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Amargant F, Manuel SL, Tu Q, Parkes WS, Rivas F, Zhou LT, Rowley JE, Villanueva CE, Hornick JE, Shekhawat GS, et al.2020 Ovarian stiffness increases with age in the mammalian ovary and depends on collagen and hyaluronan matrices. Aging Cell 19 e13259. (https://doi.org/10.1111/acel.13259)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Amin RU, Chandrashekar Reddy K, Sadasiva Rao K, Raghavender KBP, Teja A, Ramesh T & & Arunakumari G 2013 In vitro culture of goat preantral follicles from fetal ovaries. Small Ruminant Research 115 7176. (https://doi.org/10.1016/j.smallrumres.2013.08.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Araujo VR, Gastal MO, Figueiredo JR & & Gastal EL 2014 In vitro culture of bovine preantral follicles: a review. Reproductive Biology and Endocrinology: RB&E 12 78. (https://doi.org/10.1186/1477-7827-12-78)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Araujo VR, Gastal MO, Wischral A, Figueiredo JR & & Gastal EL 2015 Long-term in vitro culture of bovine preantral follicles: effect of base medium and medium replacement methods. Animal Reproduction Science 161 2331. (https://doi.org/10.1016/j.anireprosci.2015.07.006)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Barboni B, Russo V, Cecconi S, Curini V, Colosimo A, Garofalo ML, Capacchietti G, Di Giacinto O & & Mattioli M 2011 In vitro grown sheep preantral follicles yield oocytes with normal nuclear-epigenetic maturation. PLoS One 6 e27550. (https://doi.org/10.1371/journal.pone.0027550)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Barros VRP, Monte APO, Lins TLBG, Santos JM, Menezes VG, Cavalcante AYP, Araujo VR, Gouveia BB & & Matos MHT 2019 In vitro survival, growth, and maturation of sheep oocytes from secondary follicles cultured in serum-free conditions: impact of a constant or a sequential medium containing recombinant human FSH. Domestic Animal Endocrinology 67 7179. (https://doi.org/10.1016/j.domaniend.2018.12.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bezerra FTG, Lima FEO, Paulino LRFM, Silva BR, Silva AWB, Souza ALP, van den Hurk R & & Silva JRV 2019 In vitro culture of secondary follicles and prematuration of cumulus-oocyte complexes from antral follicles increase the levels of maturation-related transcripts in bovine oocytes. Molecular Reproduction and Development 86 18741886. (https://doi.org/10.1002/mrd.23284)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bjarkadottir BD, Walker CA, Fatum M, Lane S & & Williams SA 2021 Analysing culture methods of frozen human ovarian tissue to improve follicle survival. Reproduction and Fertility 2 5968. (https://doi.org/10.1530/RAF-20-0058)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Borges MA, Curcio BR, Gastal GDA, Gheno L, Junior ASV, Corcini CD, Nogueira CEW, Aguiar FLN & & Gastal EL 2023 Ethanol, Carnoy, and paraformaldehyde as fixative solutions for histological evaluation of preantral follicles in equine ovarian tissue. Reproductive Biology 23 100814. (https://doi.org/10.1016/j.repbio.2023.100814)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Braw-Tal R & & Yossefi S 1997 Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. Journal of Reproduction and Fertility 109 165171. (https://doi.org/10.1530/jrf.0.1090165)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bus A, Langbeen A, Martin B, Leroy JLMR & & Bols PEJ 2019 Is the pre-antral ovarian follicle the ‘holy grail’ for female fertility preservation? Animal Reproduction Science 207 119130. (https://doi.org/10.1016/j.anireprosci.2019.05.017)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Campbell BK, Souza C, Gong J, Webb R, Kendall N, Marsters P, Robinson G, Mitchell A, Telfer EE & & Baird DT 2003 Domestic ruminants as models for the elucidation of the mechanisms controlling ovarian follicle development in humans. Reproduction 61 429443. (https://doi.org/10.1530/biosciprocs.5.032)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Candelaria JI & & Denicol AC 2020 Characterization of isolated bovine preantral follicles based on morphology, diameter and cell number. Zygote 28 16. (https://doi.org/10.1017/S0967199419000832)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Candelaria JI, Rabaglino MB & & Denicol AC 2020 Ovarian preantral follicles are responsive to FSH as early as the primary stage of development. Journal of Endocrinology 247 153168. (https://doi.org/10.1530/JOE-20-0126)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chatterjee S 2014 Artefacts in histopathology. Journal of Oral and Maxillofacial Pathology 18(Supplement 1) S111S116. (https://doi.org/10.4103/0973-029X.141346)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Converse A, Zaniker EJ, Amargant F & & Duncan FE 2023 Recapitulating folliculogenesis and oogenesis outside the body: encapsulated in vitro follicle growthdagger. Biology of Reproduction 108 522. (https://doi.org/10.1093/biolre/ioac176)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dey P & & Luciano AM 2022 A century of programmed cell death in the ovary: a commentary. Journal of Assisted Reproduction and Genetics 39 6366. (https://doi.org/10.1007/s10815-021-02389-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dey P, Monferini N, Donadini L, Lodde V, Franciosi F & & Luciano AM 2024 Method of isolation and in vitro culture of primordial follicles in bovine animal model. Methods in Molecular Biology 2770 171182. (https://doi.org/10.1007/978-1-0716-3698-5_13)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dolmans MM, Michaux N, Camboni A, Martinez-Madrid B, Van Langendonckt A, Nottola SA & & Donnez J 2006 Evaluation of Liberase, a purified enzyme blend, for the isolation of human primordial and primary ovarian follicles. Human Reproduction 21 413420. (https://doi.org/10.1093/humrep/dei320)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Duncan FE, Zelinski M, Gunn AH, Pahnke JE, O’Neill CL, Songsasen N, Woodruff RI & & Woodruff TK 2016 Ovarian tissue transport to expand access to fertility preservation: from animals to clinical practice. Reproduction 152 R201R210. (https://doi.org/10.1530/REP-15-0598)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Erickson BH 1966a Development and radioresponse of the prenatal bovine ovary. Reproduction 11 97105. (https://doi.org/10.1530/jrf.0.0110097)

  • Erickson BH 1966b Development and senescence of the postnatal bovine ovary. Journal of Animal Science 25 800805. (https://doi.org/10.2527/jas1966.253800x)

  • Faddy MJ & & Gosden RG 1996 A model conforming the decline in follicle numbers to the age of menopause in women. Human Reproduction 11 14841486. (https://doi.org/10.1093/oxfordjournals.humrep.a019422)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Faddy MJ, Gosden RG & & Edwards RG 1983 Ovarian follicle dynamics in mice: a comparative study of three inbred strains and an F1 hybrid. Journal of Endocrinology 96 2333. (https://doi.org/10.1677/joe.0.0960023)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fair T, Hulshof SC, Hyttel P, Greve T & & Boland M 1997 Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anatomy and Embryology (Berl) 195 327336. (https://doi.org/10.1007/s004290050052)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Figueiredo JR, Hulshof SC, Van den Hurk R, Ectors FJ, Fontes RS, Nusgens B, Bevers MM & & Beckers JF 1993 Development of a combined new mechanical and enzymatic method for the isolation of intact preantral follicles from fetal, calf and adult bovine ovaries. Theriogenology 40 789799. (https://doi.org/10.1016/0093-691x(9390214-p)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Findlay JK, Hutt KJ, Hickey M & & Anderson RA 2015 How is the number of primordial follicles in the ovarian reserve established? Biology of Reproduction 93 111. (https://doi.org/10.1095/biolreprod.115.133652)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Forabosco A & & Sforza C 2007 Establishment of ovarian reserve: a quantitative morphometric study of the developing human ovary. Fertility and Sterility 88 675683. (https://doi.org/10.1016/j.fertnstert.2006.11.191)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ford EA, Beckett EL, Roman SD, McLaughlin EA & & Sutherland JM 2020 Advances in human primordial follicle activation and premature ovarian insufficiency. Reproduction 159 R15R29. (https://doi.org/10.1530/REP-19-0201)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Garcia Barros R, Lodde V, Franciosi F & & Luciano AM 2023 A refined culture system of oocytes from early antral follicles promotes oocyte maturation and embryo development in cattle. Reproduction 165 221233. (https://doi.org/10.1530/REP-22-0277)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gonzalez SM, Cerezetti MB, Bergamo LZ, Morotti F & & Seneda MM 2023 Spatial distribution of preantral follicles in ovarian parenchyma of bovine species. Zygote 31 195200. (https://doi.org/10.1017/S0967199423000023)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gosden RG & & Telfer E 1987 Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships. Journal of Zoology 211 169175. (https://doi.org/10.1111/j.1469-7998.1987.tb07460.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gosden R & & Yin H 2013 In vitro growth and differentiation of oocytes. In Biology and Pathology of the Oocyte: Role in Fertility, Medicine and Nuclear Reprograming, 2nd ed. Eichenlaub-Ritter U, Gosden R, & Trounson A Eds. Cambridge: Cambridge University Press, pp. 187199. (https://doi.org/10.1017/CBO9781139135030.017)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gougeon A 1986 Dynamics of follicular growth in the human: a model from preliminary results. Human Reproduction 1 8187. (https://doi.org/10.1093/oxfordjournals.humrep.a136365)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gougeon A & & Chainy GB 1987 Morphometric studies of small follicles in ovaries of women at different ages. Journal of Reproduction and Fertility 81 433442. (https://doi.org/10.1530/jrf.0.0810433)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gougeon A, Ecochard R & & Thalabard JC 1994 Age-related changes of the population of human ovarian follicles: increase in the disappearance rate of non-growing and early-growing follicles in aging women. Biology of Reproduction 50 653663. (https://doi.org/10.1095/biolreprod50.3.653)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Grubliauskaite M, Vlieghe H, Moghassemi S, Dadashzadeh A, Camboni A, Gudleviciene Ž & & Amorim CA 2024 Influence of ovarian stromal cells on human ovarian follicle growth in a 3D environment. Human Reproduction Open 2024 hoad052. (https://doi.org/10.1093/hropen/hoad052)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Haag KT, Magalhaes-Padilha DM, Fonseca GR, Wischral A, Gastal MO, King SS, Jones KL, Figueiredo JR & & Gastal EL 2013a Equine preantral follicles obtained via the Biopsy Pick-Up method: histological evaluation and validation of a mechanical isolation technique. Theriogenology 79 735743. (https://doi.org/10.1016/j.theriogenology.2012.10.023)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Haag KT, Magalhaes-Padilha DM, Fonseca GR, Wischral A, Gastal MO, King SS, Jones KL, Figueiredo JR & & Gastal EL 2013b Quantification, morphology, and viability of equine preantral follicles obtained via the Biopsy Pick-Up method. Theriogenology 79 599609. (https://doi.org/10.1016/j.theriogenology.2012.11.012)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR & & Klein NA 2008 A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Human Reproduction 23 699708. (https://doi.org/10.1093/humrep/dem408)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hornick JE, Duncan FE, Shea LD & & Woodruff TK 2013 Multiple follicle culture supports primary follicle growth through paracrine-acting signals. Reproduction 145 1932. (https://doi.org/10.1530/REP-12-0233)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hulshof SC, Figueiredo JR, Beckers JF, Bevers MM & & van den Hurk R 1994 Isolation and characterization of preantral follicles from foetal bovine ovaries. Veterinary Quarterly 16 7880. (https://doi.org/10.1080/01652176.1994.9694423)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hummitzsch K, Anderson RA, Wilhelm D, Wu J, Telfer EE, Russell DL, Robertson SA & & Rodgers RJ 2015 Stem cells, progenitor cells, and lineage decisions in the ovary. Endocrine Reviews 36 6591. (https://doi.org/10.1210/er.2014-1079)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hyde KA, Aguiar FLN, Alves BG, Alves KA, Gastal GDA, Gastal MO & & Gastal EL 2022 Preantral follicle population and distribution in the horse ovary. Reproduction and Fertility 3 90102. (https://doi.org/10.1530/RAF-21-0100)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ireland JL, Scheetz D, Jimenez-Krassel F, Themmen AP, Ward F, Lonergan P, Smith GW, Perez GI, Evans AC & & Ireland JJ 2008 Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biology of Reproduction 79 12191225. (https://doi.org/10.1095/biolreprod.108.071670)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Jachter SL, Simmons WP, Estill C, Xu J & & Bishop CV 2022 Matrix-free three-dimensional culture of bovine secondary follicles to antral stage: impact of media formulation and epidermal growth factor (EGF). Theriogenology 181 8994. (https://doi.org/10.1016/j.theriogenology.2022.01.013)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Jimenez CR, Araujo VR, Penitente-Filho JM, de Azevedo JL, Silveira RG & & Torres CA 2016 The base medium affects ultrastructure and survival of bovine preantral follicles cultured in vitro. Theriogenology 85 10191029. (https://doi.org/10.1016/j.theriogenology.2015.11.007)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Jorssen EP, Langbeen A, Marei WF, Fransen E, De porte HF, Leroy JL & & Bols PE 2015 Morphologic characterization of isolated bovine early preantral follicles during short-term individual in vitro culture. Theriogenology 84 301311. (https://doi.org/10.1016/j.theriogenology.2015.03.020)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kagawa N, Silber S & & Kuwayama M 2009 Successful vitrification of bovine and human ovarian tissue. Reproductive Biomedicine Online 18 568577. (https://doi.org/10.1016/s1472-6483(1060136-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Langbeen A, Jorssen EP, Granata N, Fransen E, Leroy JL & & Bols PE 2014 Effects of neutral red assisted viability assessment on the cryotolerance of isolated bovine preantral follicles. Journal of Assisted Reproduction and Genetics 31 17271736. (https://doi.org/10.1007/s10815-014-0340-y)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Langbeen A, Jorssen EP, Fransen E, Rodriguez AP, Garcia MC, Leroy JL & & Bols PE 2015 Characterization of freshly retrieved preantral follicles using a low-invasive, mechanical isolation method extended to different ruminant species. Zygote 23 683694. (https://doi.org/10.1017/S0967199414000331)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lazzari G, Galli C & & Moor RM 1992 Centrifugal elutriation of porcine oocytes isolated from the ovaries of newborn piglets. Analytical Biochemistry 200 3135. (https://doi.org/10.1016/0003-2697(9290272-9)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lonergan P & & Fair T 2008 In vitro-produced bovine embryos: dealing with the warts. Theriogenology 69 1722. (https://doi.org/10.1016/j.theriogenology.2007.09.007)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Luciano AM, Corbani D, Lodde V, Tessaro I, Franciosi F, Peluso JJ & & Modina S 2011 Expression of progesterone receptor membrane component-1 in bovine reproductive system during estrous cycle. European Journal of Histochemistry 55 e27. (https://doi.org/10.4081/ejh.2011.e27)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Luciano AM, Franciosi F, Barros RG, Dieci C & & Lodde V 2018 The variable success of in vitro maturation: can we do better? Animal Reproduction 15(Supplement 1) 727736. (https://doi.org/10.21451/1984-3143-AR2018-0021)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Luciano AM & & Sirard MA 2018 Successful in vitro maturation of oocytes: a matter of follicular differentiation. Biology of Reproduction 98 162169. (https://doi.org/10.1093/biolre/iox149)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Luciano AM, Barros RG, Soares ACS, Buratini J, Lodde V & & Franciosi F 2021 Recreating the follicular environment: A customized approach for in vitro culture of bovine oocytes based on the origin and differentiation state. Methods in Molecular Biology 2273 115. (https://doi.org/10.1007/978-1-0716-1246-0_1)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lussier JG, Matton P & & Dufour JJ 1987 Growth rates of follicles in the ovary of the cow. Journal of Reproduction and Fertility 81 301307. (https://doi.org/10.1530/jrf.0.0810301)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marcozzi S, Rossi V, Salustri A, De Felici M & & Klinger FG 2018 Programmed cell death in the human ovary. Minerva Ginecologica 70 549560. (https://doi.org/10.23736/S0026-4784.18.04274-0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • McDonnell SP, Candelaria JI, Morton AJ & & Denicol AC 2022 Isolation of small preantral follicles from the bovine ovary using a combination of fragmentation, homogenization, and serial filtration. Journal of Visualized Experiments (187). (https://doi.org/10.3791/64423)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • McGee EA & & Hsueh AJ 2000 Initial and cyclic recruitment of ovarian follicles. Endocrine Reviews 21 200214. (https://doi.org/10.1210/edrv.21.2.0394)

  • McLaughlin M, Bromfield JJ, Albertini DF & & Telfer EE 2010 Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Molecular Human Reproduction 16 644653. (https://doi.org/10.1093/molehr/gaq021)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • McLaughlin M, Albertini DF, Wallace WHB, Anderson RA & & Telfer EE 2018 Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system. Molecular Human Reproduction 24 135142. (https://doi.org/10.1093/molehr/gay002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Meredith S, Dudenhoeffer G & & Jackson K 2000 Classification of small type B/C follicles as primordial follicles in mature rats. Journal of Reproduction and Fertility 119 4348. (https://doi.org/10.1530/jrf.0.1190043)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Modina SC, Tessaro I, Lodde V, Franciosi F, Corbani D & & Luciano AM 2014 Reductions in the number of mid-sized antral follicles are associated with markers of premature ovarian senescence in dairy cows. Reproduction, Fertility, and Development 26 235244. (https://doi.org/10.1071/RD12295)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nikniaz H, Zandieh Z, Nouri M, Daei-Farshbaf N, Aflatoonian R, Gholipourmalekabadi M & & Jameie SB 2021 Comparing various protocols of human and bovine ovarian tissue decellularization to prepare extracellular matrix-alginate scaffold for better follicle development in vitro. BMC Biotechnology 21 8. (https://doi.org/10.1186/s12896-020-00658-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • O’Brien MJ, Pendola JK & & Eppig JJ 2003 A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biology of Reproduction 68 16821686. (https://doi.org/10.1095/biolreprod.102.013029)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ouni E, Peaucelle A, Haas KT, Van Kerk O, Dolmans MM, Tuuri T, Otala M & & Amorim CA 2021 A blueprint of the topology and mechanics of the human ovary for next-generation bioengineering and diagnosis. Nature Communications 12 5603. (https://doi.org/10.1038/s41467-021-25934-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Paulino LRFM, de Assis EIT, Azevedo VAN, Silva BR, da Cunha EV & & Silva JRV 2022 Why is it so difficult to have competent oocytes from in vitro cultured preantral follicles? Reproductive Sciences 29 33213334. (https://doi.org/10.1007/s43032-021-00840-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rice S, Ojha K & & Mason H 2008 Human ovarian biopsies as a viable source of pre-antral follicles. Human Reproduction 23 600605. (https://doi.org/10.1093/humrep/dem390)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Roberts JF & & Huang CCJ 2022 Bovine models for human ovarian diseases. Progress in Molecular Biology and Translational Science 189 101154. (https://doi.org/10.1016/bs.pmbts.2022.02.001)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rodgers RJ & & Irving-Rodgers HF 2010a Formation of the ovarian follicular antrum and follicular fluid. Biology of Reproduction 82 10211029. (https://doi.org/10.1095/biolreprod.109.082941)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rodgers RJ & & Irving-Rodgers HF 2010b Morphological classification of bovine ovarian follicles. Reproduction 139 309318. (https://doi.org/10.1530/REP-09-0177)

  • Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET & & Eliceiri KW 2017 ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics 18 529. (https://doi.org/10.1186/s12859-017-1934-z)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Santos SS, Ferreira MA, Pinto JA, Sampaio RV, Carvalho AC, Silva TV, Costa NN, Cordeiro MS, Miranda MS, Ribeiro HF, et al.2013 Characterization of folliculogenesis and the occurrence of apoptosis in the development of the bovine fetal ovary. Theriogenology 79 344350. (https://doi.org/10.1016/j.theriogenology.2012.09.026)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sarma UC, Winship AL & & Hutt KJ 2020 Comparison of methods for quantifying primordial follicles in the mouse ovary. Journal of Ovarian Research 13 121. (https://doi.org/10.1186/s13048-020-00724-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Schmidt KL, Byskov AG, Nyboe Andersen A, Muller J & & Yding Andersen C 2003 Density and distribution of primordial follicles in single pieces of cortex from 21 patients and in individual pieces of cortex from three entire human ovaries. Human Reproduction 18 11581164. (https://doi.org/10.1093/humrep/deg246)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Schneider CA, Rasband WS & & Eliceiri KW 2012 NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9 671675. (https://doi.org/10.1038/nmeth.2089)

  • Shen L, Liu J, Luo A & & Wang S 2023 The stromal microenvironment and ovarian aging: mechanisms and therapeutic opportunities. Journal of Ovarian Research 16 237. (https://doi.org/10.1186/s13048-023-01300-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Silva-Santos KC, Santos GM, Siloto LS, Hertel MF, Andrade ER, Rubin MI, Sturion L, Melo-Sterza FA & & Seneda MM 2011 Estimate of the population of preantral follicles in the ovaries of Bos taurus indicus and Bos taurus taurus cattle. Theriogenology 76 10511057. (https://doi.org/10.1016/j.theriogenology.2011.05.008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Simon LE, Kumar TR & & Duncan FE 2020 In vitro ovarian follicle growth: a comprehensive analysis of key protocol variables. Biology of Reproduction 103 455470. (https://doi.org/10.1093/biolre/ioaa073)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sirard MA 2017 The ovarian follicle of cows as a model for human. In Animal Models and Human Reproduction: Cell and Molecular Approaches with Reference to Human Reproduction. Schatten H, & Constantinescu GM Eds. Wiley-Blackwell, pp. 127144. (https://doi.org/10.1002/9781118881286.ch6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stansfield FJ, Picton HM & & Nothling JO 2011 Early primary--rather than primordial follicles constitute the main follicular reserve in the African elephant (Loxodonta africana). Animal Reproduction Science 123 112118. (https://doi.org/10.1016/j.anireprosci.2010.11.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stubbs SA, Stark J, Dilworth SM, Franks S & & Hardy K 2007 Abnormal preantral folliculogenesis in polycystic ovaries is associated with increased granulosa cell division. Journal of Clinical Endocrinology and Metabolism 92 44184426. (https://doi.org/10.1210/jc.2007-0729)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Telfer EE 2019 FERTILITY PRESERVATION: progress and prospects for developing human immature oocytes in vitro. Reproduction 158 F45F54. (https://doi.org/10.1530/REP-19-0077)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Telfer EE, Sakaguchi K, Clarkson YL & & McLaughlin M 2019 In vitro growth of immature bovine follicles and oocytes. Reproduction, Fertility, and Development 32 16. (https://doi.org/10.1071/RD19270)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Telfer EE, Grosbois J, Odey YL, Rosario R & & Anderson RA 2023 Making a good egg: human oocyte health, aging, and in vitro development. Physiological Reviews 103 26232677. (https://doi.org/10.1152/physrev.00032.2022)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tessaro I, Luciano AM, Franciosi F, Lodde V, Corbani D & & Modina SC 2011 The endothelial nitric oxide synthase/nitric oxide system is involved in the defective quality of bovine oocytes from low mid-antral follicle count ovaries. Journal of Animal Science 89 23892396. (https://doi.org/10.2527/jas.2010-3714)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tilly JL 2001 Commuting the death sentence: how oocytes strive to survive. Nature Reviews. Molecular Cell Biology 2 838848. (https://doi.org/10.1038/35099086)

  • van den Hurk R & & Zhao J 2005 Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63 17171751. (https://doi.org/10.1016/j.theriogenology.2004.08.005)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • van Wezel IL & & Rodgers RJ 1996 Morphological characterization of bovine primordial follicles and their environment in vivo. Biology of Reproduction 55 10031011. (https://doi.org/10.1095/biolreprod55.5.1003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vanacker J, Camboni A, Dath C, Van Langendonckt A, Dolmans MM, Donnez J & & Amorim CA 2011 Enzymatic isolation of human primordial and primary ovarian follicles with Liberase DH: protocol for application in a clinical setting. Fertility and Sterility 96 379383.e3. (https://doi.org/10.1016/j.fertnstert.2011.05.075)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vilela JMV, Dolmans MM & & Amorim CA 2021 Ovarian tissue transportation: a systematic review. Reproductive Biomedicine Online 42 351365. (https://doi.org/10.1016/j.rbmo.2020.11.001)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Walker CA, Bjarkadottir BD, Fatum M, Lane S & & Williams SA 2021 Variation in follicle health and development in cultured cryopreserved ovarian cortical tissue: a study of ovarian tissue from patients undergoing fertility preservation. Human Fertility 24 188198. (https://doi.org/10.1080/14647273.2019.1616118)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Westergaard CG, Byskov AG & & Andersen CY 2007 Morphometric characteristics of the primordial to primary follicle transition in the human ovary in relation to age. Human Reproduction 22 22252231. (https://doi.org/10.1093/humrep/dem135)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wright CS, Hovatta O, Margara R, Trew G, Winston RM, Franks S & & Hardy K 1999 Effects of follicle-stimulating hormone and serum substitution on the in-vitro growth of human ovarian follicles. Human Reproduction 14 15551562. (https://doi.org/10.1093/humrep/14.6.1555)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Xu J & & Zelinski MB 2022 Oocyte quality following in vitro follicle development. Biology of Reproduction 106 291315. (https://doi.org/10.1093/biolre/ioab242)