Balanced Notch-Wnt signaling interplay is required for mouse embryo and fetal development

in Reproduction
Authors:
Mariana R Batista CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Reproduction and Development Laboratory, Lisboa, Portugal

Search for other papers by Mariana R Batista in
Current site
Google Scholar
PubMed
Close
,
Patrícia Diniz CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Reproduction and Development Laboratory, Lisboa, Portugal

Search for other papers by Patrícia Diniz in
Current site
Google Scholar
PubMed
Close
,
Daniel Murta CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Reproduction and Development Laboratory, Lisboa, Portugal
CBIOS – Faculdade de Medicina Veterinária, Universidade Lusófona de Humanidades e Tecnologias, Lisboa, Portugal

Search for other papers by Daniel Murta in
Current site
Google Scholar
PubMed
Close
,
Ana Torres CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Reproduction and Development Laboratory, Lisboa, Portugal

Search for other papers by Ana Torres in
Current site
Google Scholar
PubMed
Close
,
Luís Lopes-da-Costa CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Reproduction and Development Laboratory, Lisboa, Portugal

Search for other papers by Luís Lopes-da-Costa in
Current site
Google Scholar
PubMed
Close
, and
Elisabete Silva CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Reproduction and Development Laboratory, Lisboa, Portugal

Search for other papers by Elisabete Silva in
Current site
Google Scholar
PubMed
Close

Correspondence should be addressed to L Lopes-da-Costa; Email: lcosta@fmv.ulisboa.pt
Restricted access
Rent on DeepDyve

Sign up for journal news

This study investigated the role of Notch and Wnt cell signaling interplay in the mouse early embryo, and its effects on fetal development. Developmental kinetics was evaluated in embryos in vitro cultured from the 8-16-cell to the hatched blastocyst stage in the presence of signaling inhibitors of Notch (DAPT) and/or Wnt (DKK1). An embryo subset was evaluated for differential cell count and gene transcription of Notch (receptors Notch1-4, ligands Dll1, Dll4, Jagged1-2, effectors Hes1-2) and Wnt (Wnt3a, Lrp6, Gsk3β, C-myc, Tcf4, β-catenin) components, E-cadherin and pluripotency and differentiation markers (Sox2, Oct4, Klf4, Cdx2), whereas a second subset was evaluated for implantation ability and development to term following transfer into recipients. Notch and Wnt blockades had significant opposing effects on developmental kinetics – Notch blockade retarded while Wnt blockade fastened development. This evidences that Notch and Wnt regulate the pace of embryo kinetics by respectively speeding and braking development. Blockades significantly changed the transcription profile of Sox2, Oct4, Klf4 and Cdx2, and Notch and double blockades significantly changed embryonic cell numbers and cell ratio. The double blockade induced more severe phenotypes than those expected from the cumulative effects of single blockades. Implantation ability was unaffected, but Notch and double blockades significantly decreased fetal development to term. Compared to control embryos, Notch blockade and Wnt blockade embryos originated, respectively, significantly lighter and heavier fetuses. In conclusion, Notch and Wnt signaling interplay in the regulation of the pace of early embryo kinetics, and their actions at this stage have significant carry-over effects on later fetal development to term.

 

  • Collapse
  • Expand
  • Aghajanova L, Shen S, Rojas AM, Fisher SJ, Irwin JC & Giudice LC 2012 Comparative transcriptome analysis of human trophectoderm and embryonic stem cell-derived trophoblasts reveal key participants in early implantation. Biology of Reproduction 86 121. (https://doi.org/)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Almagor M, Harir Y, Fieldust S, Or Y & Shoham Z 2016 Ratio between inner cell mass diameter and blastocyst diameter is correlated with successful pregnancy outcomes of single blastocyst transfers. Fertility and Sterility 106 13861391. (https://doi.org/10.1016/j.fertnstert.2016.08.009)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • AVMA Panel on Euthanasia 2020 AVMA Guidelines for the Euthanasia of Animals: 2020 Edition. American Veterinary Medical Association, edn Version 2020.0.1.

  • Andersen P, Uosaki H, Shenje LT & Kwon C 2012 Non-canonical Notch signaling: emerging role and mechanism. Trends in Cell Biology 22 257265. (https://doi.org/10.1016/j.tcb.2012.02.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Batchuluun K, Azuma M, Fujiwara K, Yashiro T & Kikuchi M 2017 Notch signaling and maintenance of SOX2 expression in rat anterior pituitary cells. Acta Histochemica et Cytochemica 50 6369. (https://doi.org/10.1267/ahc.17002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Batista MR, Diniz P, Torres A, Murta D, Lopes-da-Costa L & Silva E 2020 Notch signaling in mouse blastocyst development and hatching. BMC Developmental Biology 20 9. (https://doi.org/10.1186/s12861-020-00216-2)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Borggrefe T & Oswald F 2009 The Notch signaling pathway: transcriptional regulation at Notch target genes. Cellular and Molecular Life Sciences 66 16311646. (https://doi.org/10.1007/s00018-009-8668-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA & Yoshinaga K 2000 Embryo implantation. Developmental Biology 223 217237. (https://doi.org/10.1006/dbio.2000.9767)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chu PW, Wang YP, Chen IC, Pan HM & Wu GJ 2011 Notch 1 signaling pathway effect on implantation competency. Fertility and Sterility 96 12251229. (https://doi.org/10.1016/j.fertnstert.2011.08.032)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Clapcote SJ & Roder JC 2005 Simplex PCR assay for sex determination in mice. BioTechniques 38 702706. (https://doi.org/10.2144/05385BM05)

  • Collu GM, Hidalgo-Sastre A & Brennan K 2014 Wnt-Notch signalling crosstalk in development and disease. Cellular and Molecular Life Sciences 71 35533567. (https://doi.org/10.1007/s00018-014-1644-x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cormier S, Vandormael-Pournin S, Babinet C & Cohen-Tannoudji M 2004 Developmental expression of the Notch signaling pathway genes during mouse preimplantation development. Gene Expression Patterns 4 713717. (https://doi.org/10.1016/j.modgep.2004.04.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Denicol AC, Dobbs KB, McLean KM, Carambula SF, Loureiro B & Hansen PJ 2013 Canonical WNT signaling regulates development of bovine embryos to the blastocyst stage. Scientific Reports 3 1266. (https://doi.org/10.1038/srep01266)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Denicol AC, Block J, Kelley DE, Pohler KG, Dobbs KB, Mortensen CJ, Ortega MS & Hansen PJ 2014 The WNT signaling antagonist Dickkopf-1 directs lineage commitment and promotes survival of the preimplantation embryo. ASEB Journal 28 39753986. (https://doi.org/10.1096/fj.14-253112)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Edeling M, Ragi G, Huang S, Pavenstädt H & Susztak K 2016 Developmental signalling pathways in renal fibrosis: the roles of Notch, Wnt and Hedgehog. Nature Reviews: Nephrology 12 426439. (https://doi.org/10.1038/nrneph.2016.54)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Faunes F, Hayward P, Descalzo SM, Chatterjee SS, Balayo T, Trott J, Christoforou A, Ferrer-Vaquer A, Hadjantonakis AK & Dasgupta R et al.2013 A membrane-associated β-catenin/Oct4 complex correlates with ground-state pluripotency in mouse embryonic stem cells. Development 140 11711183. (https://doi.org/10.1242/dev.085654)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Feng Z, Xu W, Zhang C, Liu M & Wen H 2017 Inhibition of gamma-secretase in Notch1 signaling pathway as a novel treatment for ovarian cancer. Oncotarget 8 82158225. (https://doi.org/10.18632/oncotarget.14152)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fox V, Gokhale PJ, Walsh JR, Matin M, Jones M & Andrews PW 2008 Cell-cell signaling through NOTCH regulates human embryonic stem cell proliferation. Stem Cells 26 715723. (https://doi.org/10.1634/stemcells.2007-0368)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gao C, Xiao G & Hu J 2014 Regulation of Wnt/β-catenin signaling by posttranslational modifications. Cell and Bioscience 4 13. (https://doi.org/10.1186/2045-3701-4-13)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hayward P, Kalmar T & Arias AM 2008 Wnt/Notch signalling and information processing during development. Development 135 411424. (https://doi.org/10.1242/dev.000505)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hirata H, Yoshiura S, Ohtsuka T, Bessho Y, Harada T, Yoshikawa K & Kageyama R 2002 Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science 298 840843. (https://doi.org/10.1126/science.1074560)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hu S, Chen Q, Lin T, Hong W, Wu W, Wu M, Du X & Jin R 2018 The function of Notch1 intracellular domain in the differentiation of gastric cancer. Oncology Letters 15 61716178. (https://doi.org/10.3892/ol.2018.8118)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Huang G, Ye S, Zhou X, Liu D & Ying QL 2015 Molecular basis of embryonic stem cell self-renewal: from signaling pathways to pluripotency network. Cellular and Molecular Life Sciences 72 17411757. (https://doi.org/10.1007/s00018-015-1833-2)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kaemmerer E, Jeon MK, Berndt A, Liedtke C & Gassler N 2019 Targeting Wnt signaling via notch in intestinal carcinogenesis. Cancers 11 555. (https://doi.org/10.3390/cancers11040555)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kao LC, Tulac S, Lobo S, Imani B, Yang JP, Germeyer A, Osteen K, Taylor RN, Lessey BA & Giudice LC 2002 Global gene profiling in human endometrium during the window of implantation. Endocrinology 143 21192138. (https://doi.org/10.1210/endo.143.6.8885)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kelly KF, Ng DY, Jayakumaran G, Wood GA, Koide H & Doble BW 2011 β-Catenin enhances Oct-4 activity and reinforces pluripotency through a TCF-independent mechanism. Cell Stem Cell 8 214227. (https://doi.org/10.1016/j.stem.2010.12.010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kemp C, Willems E, Abdo S, Lambiv L & Leyns L 2005 Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development. Developmental Dynamics 233 10641075. (https://doi.org/10.1002/dvdy.20408)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Keramari M, Razavi J, Ingman KA, Patsch C, Edenhofer F, Ward CM & Kimber SJ 2010 Sox2 is essential for formation of trophectoderm in the preimplantation embryo. PLoS ONE 5 e13952. (https://doi.org/10.1371/journal.pone.0013952)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Khan Z, Vijayakumar S, de la Torre TV, Rotolo S & Bafico A 2007 Analysis of endogenous LRP6 function reveals a novel feedback mechanism by which Wnt negatively regulates its receptor. Molecular and Cellular Biology 27 72917301. (https://doi.org/10.1128/MCB.00773-07)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kim W, Kim M & Jho EH 2013 Wnt/β-catenin signalling: from plasma membrane to nucleus. Biochemical Journal 450 921. (https://doi.org/10.1042/BJ20121284)

  • Kwon GS, Viotti M & Hadjantonakis AK 2008 The endoderm of the mouse embryo arises by dynamic widespread intercalation of embryonic and extraembryonic lineages. Developmental Cell 15 509520. (https://doi.org/10.1016/j.devcel.2008.07.017)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Li J, Liu WM, Cao YJ, Peng S, Zhang Y & Duan EK 2008 Roles of Dickkopf-1 and its receptor Kremen1 during embryonic implantation in mice. Fertility and Sterility 90 (Supplement) 14701479. (https://doi.org/10.1016/j.fertnstert.2007.09.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Li Y, Lu W, King TD, Liu CC, Bijur GN & Bu G 2010 Dkk1 stabilizes Wnt co-receptor LRP6: implication for Wnt ligand-induced LRP6 down-regulation. PLoS ONE 5 e11014. (https://doi.org/10.1371/journal.pone.0011014)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lim KT, Gupta MK, Lee SH, Jung YH, Han DW & Lee HT 2013 Possible involvement of Wnt/β-catenin signaling pathway in hatching and trophectoderm differentiation of pig blastocysts. Theriogenology 79 28490.e1. (https://doi.org/10.1016/j.theriogenology.2012.08.018)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ma L, Wang Y, Hui Y, Du Y, Chen Z, Feng H, Zhang S, Li N, Song J & Fang Y et al.2019 WNT/NOTCH pathway is essential for the maintenance and expansion of human MGE progenitors. Stem Cell Reports 12 934949. (https://doi.org/10.1016/j.stemcr.2019.04.007)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marambaud P, Shioi J, Serban G, Georgakopoulos A, Sarner S, Nagy V, Baki L, Wen P, Efthimiopoulos S & Shao Z et al.2002 A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO Journal 21 19481956. (https://doi.org/10.1093/emboj/21.8.1948)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marikawa Y & Alarcon VB 2012 Creation of trophectoderm, the first epithelium, in mouse preimplantation development. Results and Problems in Cell Differentiation 55 165184. (https://doi.org/10.1007/978-3-642-30406-4_9)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marson A, Foreman R, Chevalier B, Bilodeau S, Kahn M, Young RA & Jaenisch R 2008 Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell 3 132135. (https://doi.org/10.1016/j.stem.2008.06.019)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Menchero S, Rollan I, Lopez-Izquierdo A, Andreu MJ, Sainz de Aja J, Kang M, Adan J, Benedito R, Rayon T & Hadjantonakis AK et al.2019 Transitions in cell potency during early mouse development are driven by Notch. eLife 8 e42930. (https://doi.org/10.7554/eLife.42930)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Merilahti JAM & Elenius K 2019 Gamma-secretase-dependent signaling of receptor tyrosine kinases. Oncogene 38 151163. (https://doi.org/10.1038/s41388-018-0465-z)

  • Mi K & Johnson GV 2007 Regulated proteolytic processing of LRP6 results in release of its intracellular domain. Journal of Neurochemistry 101 517529. (https://doi.org/10.1111/j.1471-4159.2007.04447.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Minten MA, Bilby TR, Bruno RG, Allen CC, Madsen CA, Wang Z, Sawyer JE, Tibary A, Neibergs HL & Geary TW et al.2013 Effects of fertility on gene expression and function of the bovine endometrium. PLoS ONE 8 e69444. (https://doi.org/10.1371/journal.pone.0069444)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Muñoz Descalzo S & Martinez Arias A 2012 The structure of Wntch signalling and the resolution of transition states in development. Seminars in Cell and Developmental Biology 23 443449. (https://doi.org/10.1016/j.semcdb.2012.01.012)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Murta D, Batista M, Trindade A, Silva E, Henrique D, Duarte A & Lopes-da-Costa L 2014 In vivo notch signaling blockade induces abnormal spermatogenesis in the mouse. PLoS ONE 9 e113365. (https://doi.org/10.1371/journal.pone.0113365)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nagy A, Gertsenstein M, Vintersten K & Behringer R 2003 Manipulating the Mouse Embryo: A Laboratory Manual, 3rd ed. Cold Spring Harbor Laboratory Press.

  • Neves J, Parada C, Chamizo M & Giráldez F 2011 Jagged 1 regulates the restriction of Sox2 expression in the developing chicken inner ear: a mechanism for sensory organ specification. Development 138 735744. (https://doi.org/10.1242/dev.060657)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Niwa H, Miyazaki J & Smith AG 2000 Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics 24 372376. (https://doi.org/10.1038/74199)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Noli L, Capalbo A, Ogilvie C, Khalaf Y & Ilic D 2015 Discordant growth of monozygotic twins starts at the blastocyst stage: a case study. Stem Cell Reports 5 946953. (https://doi.org/10.1016/j.stemcr.2015.10.006)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rao TP & Kühl M 2010 An updated overview on Wnt signaling pathways: a prelude for more. Circulation Research 106 17981806. (https://doi.org/10.1161/CIRCRESAHA.110.219840)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rayon T, Menchero S, Nieto A, Xenopoulos P, Crespo M, Cockburn K, Cañon S, Sasaki H, Hadjantonakis AK & de la Pompa JL et al.2014 Notch and hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Developmental Cell 30 410422. (https://doi.org/10.1016/j.devcel.2014.06.019)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Reznikova TV, Phillips MA & Rice RH 2009 Arsenite suppresses Notch1 signaling in human keratinocytes. Journal of Investigative Dermatology 129 155161. (https://doi.org/10.1038/jid.2008.207)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH & Robson P 2005 Transcriptional regulation of nanog by OCT4 and SOX2. Journal of Biological Chemistry 280 2473124737. (https://doi.org/10.1074/jbc.M502573200)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rossant J & Tam PP 2009 Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136 701713. (https://doi.org/10.1242/dev.017178)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Schrode N, Xenopoulos P, Piliszek A, Frankenberg S, Plusa B & Hadjantonakis AK 2013 Anatomy of a blastocyst: cell behaviors driving cell fate choice and morphogenesis in the early mouse embryo. Genesis 51 219233. (https://doi.org/10.1002/dvg.22368)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Shi S, Stahl M, Lu L & Stanley P 2005 Canonical Notch signaling is dispensable for early cell fate specifications in mammals. Molecular and Cellular Biology 25 95039508. (https://doi.org/10.1128/MCB.25.21.9503-9508.2005)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Siebel C & Lendahl U 2017 Notch signaling in development, tissue homeostasis, and disease. Physiological Reviews 97 12351294. (https://doi.org/10.1152/physrev.00005.2017)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Souilhol C, Cormier S, Tanigaki K, Babinet C & Cohen-Tannoudji M 2006 RBP-Jkappa-dependent notch signaling is dispensable for mouse early embryonic development. Molecular and Cellular Biology 26 47694774. (https://doi.org/10.1128/MCB.00319-06)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stephenson RO, Yamanaka Y & Rossant J 2010 Disorganized epithelial polarity and excess trophectoderm cell fate in preimplantation embryos lacking E-cadherin. Development 137 33833391. (https://doi.org/10.1242/dev.050195)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F & Rossant J 2005 Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132 20932102. (https://doi.org/10.1242/dev.01801)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Takeuchi M, Seki M, Furukawa E, Takahashi A, Saito K, Kobayashi M, Ezoe K, Fukui E, Yoshizawa M & Matsumoto H 2017 Improvement of implantation potential in mouse blastocysts derived from IVF by combined treatment with prolactin, epidermal growth factor and 4-hydroxyestradiol. Molecular Human Reproduction 23 557570. (https://doi.org/10.1093/molehr/gax035)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • van den Berg DL, Snoek T, Mullin NP, Yates A, Bezstarosti K, Demmers J, Chambers I & Poot RA 2010 An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6 369381. (https://doi.org/10.1016/j.stem.2010.02.014)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP, Davis RW & Zernicka-Goetz M 2004 A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Developmental Cell 6 133144. (https://doi.org/10.1016/s1534-5807(0300404-0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Watanabe Y, Miyasaka KY, Kubo A, Kida YS, Nakagawa O, Hirate Y, Sasaki H & Ogura T 2017 Notch and Hippo signaling converge on strawberry Notch 1 (Sbno1) to synergistically activate Cdx2 during specification of the trophectoderm. Scientific Reports 7 46135. (https://doi.org/10.1038/srep46135)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wei Z, Yang Y, Zhang P, Andrianakos R, Hasegawa K, Lyu J, Chen X, Bai G, Liu C & Pera M et al.2009 Klf4 interacts directly with Oct4 and Sox2 to promote reprogramming. Stem Cells 27 29692978. (https://doi.org/10.1002/stem.231)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wu G & Schöler HR 2014 Role of Oct4 in the early embryo development. Cell Regeneration 3 7. (https://doi.org/10.1186/2045-9769-3-7)

  • Xie H, Tranguch S, Jia X, Zhang H, Das SK, Dey SK, Kuo CJ & Wang H 2008 Inactivation of nuclear Wnt-beta-catenin signaling limits blastocyst competency for implantation. Development 135 717727. (https://doi.org/10.1242/dev.015339)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Xie D, Chen CC, Ptaszek LM, Xiao S, Cao X, Fang F, Ng HH, Lewin HA, Cowan C & Zhong S 2010 Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Research 20 804815. (https://doi.org/10.1101/gr.100594.109)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yoshinaga K 2013 A sequence of events in the uterus prior to implantation in the mouse. Journal of Assisted Reproduction and Genetics 30 10171022. (https://doi.org/10.1007/s10815-013-0093-z)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhang Y, Yang Z & Wu J 2007 Signaling pathways and preimplantation development of mammalian embryos. FEBS Journal 274 43494359. (https://doi.org/10.1111/j.1742-4658.2007.05980.x)

    • PubMed
    • Search Google Scholar
    • Export Citation