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Gene expression analysis of bovine embryonic disc, trophoblast and parietal hypoblast at the start of gastrulation

Published online by Cambridge University Press:  23 May 2017

Peter L. Pfeffer*
Affiliation:
School of Biological Science, Victoria University of Wellington, Wellington, New Zealand. Agresearch, Ruakura Campus, 1 Bisley Street, Hamilton, New Zealand.
Craig S. Smith
Affiliation:
Agresearch, Ruakura Campus, 1 Bisley Street, Hamilton, New Zealand. School of Medicine, University of Notre Dame Australia, Sydney, Australia.
Paul Maclean
Affiliation:
Agresearch, Ruakura Campus, 1 Bisley Street, Hamilton, New Zealand.
Debra K. Berg
Affiliation:
Agresearch, Ruakura Campus, 1 Bisley Street, Hamilton, New Zealand.
*
All correspondence to: P.L. Pfeffer. School of Biological Science, Victoria University of Wellington, Wellington, New Zealand. Tel: +64 4 4637462. Fax: +64 4 4635331. E-mail: [email protected]

Summary

In cattle early gastrulation-stage embryos (Stage 5), four tissues can be discerned: (i) the top layer of the embryonic disc consisting of embryonic ectoderm (EmE); (ii) the bottom layer of the disc consisting of mesoderm, endoderm and visceral hypoblast (MEH); (iii) the trophoblast (TB); and (iv) the parietal hypoblast. We performed microsurgery followed by RNA-seq to analyse the transcriptome of these four tissues as well as a developmentally earlier pre-gastrulation embryonic disc. The cattle EmE transcriptome was similar at Stages 4 and 5, characterised by the OCT4/SOX2/NANOG pluripotency network. Expression of genes associated with primordial germ cells suggest their presence in the EmE tissue at these stages. Anterior visceral hypoblast genes were transcribed in the Stage 4 disc, but no longer by Stage 5. The Stage 5 MEH layer was equally similar to mouse embryonic and extraembryonic visceral endoderm. Our data suggest that the first mesoderm to invaginate in cattle embryos is fated to become extraembryonic. TGFβ, FGF, VEGF, PDGFA, IGF2, IHH and WNT signals and receptors were expressed, however the representative members of the FGF families differed from that seen in equivalent tissues of mouse embryos. The TB transcriptome was unique and differed significantly from that of mice. FGF signalling in the TB may be autocrine with both FGFR2 and FGF2 expressed. Our data revealed a range of potential inter-tissue interactions, highlighted significant differences in early development between mice and cattle and yielded insight into the developmental events occurring at the start of gastrulation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

Acampora, D., Di Giovannantonio, L.G. & Simeone, A. (2013). Otx2 is an intrinsic determinant of the embryonic stem cell state and is required for transition to a stable epiblast stem cell condition. Development 140, 4355.Google Scholar
Andersson, O., Bertolino, P. & Ibanez, C.F. (2007). Distinct and cooperative roles of mammalian Vg1 homologs GDF1 and GDF3 during early embryonic development. Dev. Biol. 311, 500–11.CrossRefGoogle ScholarPubMed
Andre, P., Song, H., Kim, W., Kispert, A. & Yang, Y. (2015). Wnt5a and Wnt11 regulate mammalian anterior-posterior axis elongation. Development 142, 1516–27.Google Scholar
Arnold, S.J. & Robertson, E.J. (2009). Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat. Rev. Mol. Cell Biol. 10, 91103.Google Scholar
Arnold, S.J., Stappert, J., Bauer, A., Kispert, A., Herrmann, B.G. & Kemler, R. (2000). Brachyury is a target gene of the Wnt/beta-catenin signalling pathway. Mech. Dev. 91, 249–58.Google Scholar
Artus, J., Panthier, J.J. & Hadjantonakis, A.K. (2010). A role for PDGF signalling in expansion of the extraembryonic endoderm lineage of the mouse blastocyst. Development 137, 3361–72.CrossRefGoogle ScholarPubMed
Ayalon, N. (1978). A review of embryonic mortality in cattle. J. Reprod. Fertil. 54, 483–93.Google Scholar
Berg, D.K., Smith, C.S., Pearton, D.J., Wells, D.N., Broadhurst, R., Donnison, M. & Pfeffer, P.L. (2011). Trophectoderm lineage determination in cattle. Dev. Cell. 20, 244–55.Google Scholar
Berg, D.K., van Leeuwen, J., Beaumont, S., Berg, M. & Pfeffer, P.L. (2010). Embryo loss in cattle between days 7 and 16 of pregnancy. Theriogenology 73, 250–60.Google Scholar
Betteridge, K.J. & Flechon, J.E. (1988). The anatomy and physiology of pre-attachment bovine embryos. Theriogenology 29, 155–87.Google Scholar
Boyer, L.A., Lee, T.I., Cole, M.F., Johnstone, S.E., Levine, S.S., Zucker, J.P., Guenther, M.G., Kumar, R.M., Murray, H.L., Jenner, R.G., Gifford, D.K., Melton, D.A., Jaenisch, R. & Young, R.A. (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947–56.Google Scholar
Brewer, J.R., Molotkov, A., Mazot, P., Hoch, R.V. & Soriano, P. (2015). Fgfr1 regulates development through the combinatorial use of signalling proteins. Genes Dev. 29, 1863–74.Google Scholar
Brown, K., Legros, S., Artus, J., Doss, M.X., Khanin, R., Hadjantonakis, A.K. & Foley, A. (2010). A comparative analysis of extraembryonic endoderm cell lines. PLoS One 5, e12016.Google Scholar
Crossley, P.H. & Martin, G.R. (1995). The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439–51.Google Scholar
Diskin, M.G., Parr, M.H. & Morris, D.G. (2011). Embryo death in cattle: an update. Reprod. Fertil. Dev. 24, 244–51.Google Scholar
Dodt, M., Roehr, J.T., Ahmed, R. & Dieterich, C. (2012). FLEXBAR − flexible barcode and adapter processing for next-generation sequencing platforms. Biology (Basel) 1, 895905.Google Scholar
Dunn, S.J., Martello, G., Yordanov, B., Emmott, S. & Smith, A.G. (2014). Defining an essential transcription factor program for naive pluripotency. Science 344, 1156–60.Google Scholar
Ewen, K.A. & Koopman, P. (2010). Mouse germ cell development: From specification to sex determination. Mol. Cell. Endocrinol. 323, 7693.Google Scholar
Familari, M. (2006). Characteristics of the endoderm: embryonic and extraembryonic in mouse. Sci. World J. 6, 1815–27.Google Scholar
Hart, A.H., Hartley, L., Sourris, K., Stadler, E.S., Li, R., Stanley, E.G., Tam, P.P., Elefanty, A.G. & Robb, L. (2002). Mixl1 is required for axial mesendoderm morphogenesis and patterning in the murine embryo. Development 129, 3597–608.Google Scholar
Hart, A.H., Willson, T.A., Wong, M., Parker, K. & Robb, L. (2005). Transcriptional regulation of the homeobox gene Mixl1 by TGF-beta and FoxH1. Biochem. Biophys. Res. Commun. 333, 1361–9.CrossRefGoogle ScholarPubMed
Kaufman, M.H. (1995). The Atlas of Mouse Development, Academic Press, London.Google Scholar
Li, H. & Durbin, R. (2009). Fast and accurate short read alignment with Burrows−Wheeler transform. Bioinformatics 25, 1754–60.CrossRefGoogle ScholarPubMed
Liu, P., Wakamiya, M., Shea, M.J., Albrecht, U., Behringer, R.R. & Bradley, A. (1999). Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22, 361–5.Google Scholar
Lu, C.C., Brennan, J. & Robertson, E.J. (2001). From fertilization to gastrulation: axis formation in the mouse embryo. Curr Opin Genet Dev. 11, 384–92.Google Scholar
Maddox-Hyttel, P., Alexopoulos, N.I., Vajta, G., Lewis, I., Rogers, P., Cann, L., Callesen, H., Tveden-Nyborg, P. & Trounson, A. (2003). Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction 125, 607–23.Google Scholar
Magnúsdóttir, E., Dietmann, S., Murakami, K., Günesdogan, U., Tang, F., Bao, S., Diamanti, E., Lao, K., Gottgens, B. & Azim Surani, M. (2013). A tripartite transcription factor network regulates primordial germ cell specification in mice. Nat. Cell Biol. 15, 905–15.CrossRefGoogle ScholarPubMed
Magnúsdóttir, E., Gillich, A., Grabole, N. & Surani, M.A. (2012). Combinatorial control of cell fate and reprogramming in the mammalian germline. Curr. Opin. Genet. Dev. 22, 466–74.Google Scholar
Mamo, S., Mehta, J.P., McGettigan, P., Fair, T., Spencer, T.E., Bazer, F.W. & Lonergan, P. (2011). RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation. Biol. Reprod. 85, 1143–51.Google Scholar
Maye, P., Becker, S., Siemen, H., Thorne, J., Byrd, N., Carpentino, J. & Grabel, L. (2004). Hedgehog signalling is required for the differentiation of ES cells into neurectoderm. Dev. Biol. 265, 276–90.Google Scholar
Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. & Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat. Method. 5, 621–8.Google Scholar
Moustakas, A. & Heldin, C.H. (2009). The regulation of TGFbeta signal transduction. Development 136, 3699– 714.Google Scholar
Nagatomo, H., Kagawa, S., Kishi, Y., Takuma, T., Sada, A., Yamanaka, K., Abe, Y., Wada, Y., Takahashi, M., Kono, T. & Kawahara, M. (2013). Transcriptional wiring for establishing cell lineage specification at the blastocyst stage in cattle. Biol. Reprod. 88, 158.Google Scholar
Niswander, L. & Martin, G.R. (1992). Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114, 755–68.Google Scholar
Ogura, Y., Takakura, N., Yoshida, H. & Nishikawa, S.I. (1998). Essential role of platelet-derived growth factor receptor alpha in the development of the intraplacental yolk sac/sinus of Duval in mouse placenta. Biol. Reprod. 58, 6572.Google Scholar
Ornitz, D.M., Xu, J., Colvin, J.S., McEwen, D.G., MacArthur, C.A., Coulier, F., Gao, G. & Goldfarb, M. (1996). Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271, 15292–7.Google Scholar
Ozawa, M., Sakatani, M., Yao, J., Shanker, S., Yu, F., Yamashita, R., Wakabayashi, S., Nakai, K., Dobbs, K.B., Sudano, M.J., Farmerie, W.G. & Hansen, P.J. (2012). Global gene expression of the inner cell mass and trophectoderm of the bovine blastocyst. BMC Dev. Biol. 12, 33.Google Scholar
Pearton, D.J., Smith, C.S., Redgate, E., van Leeuwen, J., Donnison, M. & Pfeffer, P.L. (2014). Elf5 counteracts precocious trophoblast differentiation by maintaining Sox2 and 3 and inhibiting Hand1 expression. Dev. Biol. 392, 344–57.Google Scholar
Pfeffer, P.L. (2014). Lineage commitment in the mammalian preimplantation embryo. In Reproduction in Domestic Ruminants vol. 8 (eds Juengel, J., Miyamoto, A., & Webb, R.) pp. 89103. Context, Obihiro, Japan.Google Scholar
Pfeffer, P.L. & Pearton, D.J. (2012). Trophoblast development. Reproduction 143, 231–46.Google Scholar
Phillips, N.E., Manning, C.S., Pettini, T., Biga, V., Marinopoulou, E., Stanley, P., Boyd, J., Bagnall, J., Paszek, P., Spiller, D.G., White, M.R.H., Goodfellow, M., Galla, T., Rattray, M. & Papalopulu, N. (2016). Stochasticity in the miR-9/Hes1 oscillatory network can account for clonal heterogeneity in the timing of differentiation. eLife 5, e16118.Google Scholar
R Core Team (2014). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Richardson, L., Venkataraman, S., Stevenson, P., Yang, Y., Moss, J., Graham, L., Burton, N., Hill, B., Rao, J., Baldock, R.A. & Armit, C. (2014). EMAGE mouse embryo spatial gene expression database: 2014 update. Nucl. Acid Res. 42, D835–44.Google Scholar
Rielland, M., Hue, I., Renard, J.P. & Alice, J. (2008). Trophoblast stem cell derivation, cross-species comparison and use of nuclear transfer: new tools to study trophoblast growth and differentiation. Dev. Biol. 322, 110.Google Scholar
Roberts, R.M. & Fisher, S.J. (2011). Trophoblast stem cells. Biol. Reprod. 84, 412–21.Google Scholar
Robertson, E.J. (2014). Dose-dependent Nodal/Smad signals pattern the early mouse embryo. Semin. Cell. Dev. Biol. 32, 73–9.Google Scholar
Robinson, M.D., McCarthy, D.J. & Smyth, G.K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–40.CrossRefGoogle ScholarPubMed
Sartori, R., Bastos, M.R. & Wiltbank, M.C. (2010). Factors affecting fertilization and early embryo quality in single- and superovulated dairy cattle. Reprod. Fertil. Dev. 22, 151–8.Google Scholar
Smith, C., Berg, D., Beaumont, S., Standley, N.T., Wells, D.N. & Pfeffer, P.L. (2007). Simultaneous gene quantitation of multiple genes in individual bovine nuclear transfer blastocysts. Reproduction 133, 231–42.Google Scholar
Smith, C.S., Berg, D.K., Berg, M. & Pfeffer, P.L. (2010). Nuclear transfer-specific defects are not apparent during the second week of embryogenesis in cattle. Cell Reprogram. 12, 699707.CrossRefGoogle Scholar
Sun, X., Meyers, E.N., Lewandoski, M. & Martin, G.R. (1999). Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 13, 1834–46.Google Scholar
Tagashira, S., Harada, H., Katsumata, T., Itoh, N. & Nakatsuka, M. (1997). Cloning of mouse FGF10 and up-regulation of its gene expression during wound healing. Gene 197, 399404.Google Scholar
Tanaka, S., Kunath, T., Hadjantonakis, A.K., Nagy, A. & Rossant, J. (1998). Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072–5.Google Scholar
Taniguchi, F., Harada, T., Yoshida, S., Iwabe, T., Onohara, Y., Tanikawa, M. & Terakawa, N. (1998). Paracrine effects of bFGF and KGF on the process of mouse blastocyst implantation. Mol. Reprod. Dev. 50, 5462.Google Scholar
Trapnell, C., Pachter, L. & Salzberg, S.L. (2009). TopHat: discovering splice junctions with RNA-seq. Bioinformatics 25, 1105–11.Google Scholar
Tsubooka, N., Ichisaka, T., Okita, K., Takahashi, K., Nakagawa, M. & Yamanaka, S. (2009). Roles of Sall4 in the generation of pluripotent stem cells from blastocysts and fibroblasts. Genes Cells 14, 683–94.Google Scholar
van Leeuwen, J., Berg, D.K. & Pfeffer, P.L. (2015). Morphological and gene expression changes in cattle embryos from hatched blastocyst to early gastrulation stages after transfer of in vitro produced embryos. PLoS One 10, e0129787.Google Scholar
Vejlsted, M., Du, Y., Vajta, G. & Maddox-Hyttel, P. (2006). Post-hatching development of the porcine and bovine embryo—defining criteria for expected development in vivo and in vitro . Theriogenology 65, 153–65.Google Scholar
Voiculescu, O., Bertocchini, F., Wolpert, L., Keller, R.E. & Stern, C.D. (2007). The amniote primitive streak is defined by epithelial cell intercalation before gastrulation. Nature 449, 1049–52.Google Scholar
Wang, Z., Oron, E., Nelson, B., Razis, S. & Ivanova, N. (2012). Distinct lineage specification roles for NANOG, OCT 4, and SOX2 in human embryonic stem cells. Cell. Stem Cell 10, 440–54.CrossRefGoogle Scholar
Wooding, F.B. (1992). Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta 13, 101–13.Google Scholar
Wordinger, R.J., Smith, K.J., Bell, C. & Chang, I.F. (1994). The immunolocalization of basic fibroblast growth factor in the mouse uterus during the initial stages of embryo implantation. Growth Factors 11, 175–86.Google Scholar
Yamaji, M., Seki, Y., Kurimoto, K., Yabuta, Y., Yuasa, M., Shigeta, M., Yamanaka, K., Ohinata, Y. & Saitou, M. (2008). Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 40, 1016–22.Google Scholar
Yanai, I., Benjamin, H., Shmoish, M., Chalifa-Caspi, V., Shklar, M., Ophir, R., Bar-Even, A., Horn-Saban, S., Safran, M., Domany, E., Lancet, D. & Shmueli, O. (2005). Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21, 650–9.Google Scholar
Youngren, K.K., Coveney, D., Peng, X., Bhattacharya, C., Schmidt, L.S., Nickerson, M.L., Lamb, B.T., Deng, J.M., Behringer, R.R., Capel, B., Rubin, E.M., Nadeau, J.H. & Matin, A. (2005). The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 435, 360–4.Google Scholar
Zhang, H. & Bradley, A. (1996). Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122, 2977–86.Google Scholar
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