Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-23T13:41:10.164Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological changes and germ layer formation in the porcine embryos from days 7–13 of development

Published online by Cambridge University Press:  15 November 2013

Ruizhen Sun ,
Lei Lei ,
Shichao Liu ,
Binghua Xue ,
Jianyu Wang ,
Jiaqiang Wang ,
Jingling Shen ,
Lian Duan ,
Xinghui Shen  and
Yimei Cong
...Show all authors
Ruizhen Sun
Affiliation:
Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China.
Lei Lei
Affiliation:
Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China.
Shichao Liu
Affiliation:
College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China.
Binghua Xue
Affiliation:
College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China.
Jianyu Wang
Affiliation:
College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China.
Jiaqiang Wang
Affiliation:
College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China.
Jingling Shen
Affiliation:
Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China.
Lian Duan
Affiliation:
Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China.
Xinghui Shen
Affiliation:
Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China.
Yimei Cong
Affiliation:
College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China.
Yanli Gu
Affiliation:
Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China.
Kui Hu
Affiliation:
College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China.
Lianhong Jin*
Affiliation:
Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China or College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China. Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China.
Zhong-hua Liu*
Affiliation:
Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China or College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China. College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China.
*
All correspondence to: Lianhong Jin or Zhong-Hua Liu. Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China. Tel: +86 0451 86674518. e-mail: wstjlh@126.com; or College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China. Tel: +86 0451 55191747. e-mail: liu086@yahoo.com
All correspondence to: Lianhong Jin or Zhong-Hua Liu. Department of Histology and Embryology, Harbin Medical University, 194 Xuefu Road, Nangang District, Harbin, Heilongjiang Province, 150081, China. Tel: +86 0451 86674518. e-mail: wstjlh@126.com; or College of Life Sciences, Northeast Agricultural University, Xiangfang District, Harbin 150030, Heilongjiang Province, China. Tel: +86 0451 55191747. e-mail: liu086@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Summary

Morphogenesis and identification of embryonic differentiation in porcine embryos are crucial issues for developmental biology and laboratory animal science. The current paper presents a study on the asynchronous development of hatched porcine embryos from days 7 to 13 post-insemination. Examination of semi-thin sections of the hypoblast showed that it had characteristics similar to those of the mouse anterior visceral endoderm during embryonic disc formation. Also, a cavity appeared in the epiblast, which was similar to a mouse proamniotic cavity. With the gradual disappearance of Rauber's layer, the cavity opened and contacted the external environment directly, all of which formed the embryonic disc. To confirm the differentiation characteristics, we performed immunohistochemical analyses and showed that GATA6 was detected clearly in parietal endoderm cells during embryonic disc establishment. OCT4 was expressed in the inner cell mass (ICM) and trophoblast of hatched blastocysts and in the epiblast during formation of the embryonic disc. However, OCT4 showed comparatively decreased expression in the posterior embryonic disc, primitive streak and migrating cells. SOX2 was present in the ICM and epiblast. Therefore, both SOX2 and OCT4 can be used as markers of pluripotent cells in the porcine embryonic disc. At the start of gastrulation, staining revealed VIMENTIN in the posterior of the embryonic disc, primitive streak and in migrating cells that underlay the embryonic disc and was also expressed in epiblast cells located in the anterior primitive streak. Together with serial sections of embryos stained by whole mount immunohistochemistry, the mesoderm differentiation pattern was shown as an ingression movement that took place at the posterior of the embryonic disc and with bilateral migration along the embryonic disc borders.

Keywords

DifferentiationGATA6Hatched embryosMorphologySOX2
Type
Research Article
Information
Zygote , Volume 23 , Issue 2 , April 2015 , pp. 266 - 276
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, L.L. (1978). Growth, protein content and distribution of early pig embryos. Anat. Rec. 190, 143–53.Google Scholar
Avilion, A.A., Nicolis, S.K., Pevny, L.H., Perez, L., Vivian, N. & Lovell-Badge, R. (2003). Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17, 126–40.CrossRefGoogle ScholarPubMed
Barends, P.M., Stroband, H.W., Taverne, N., te Kronnie, G., Leën, M.P. & Blommers, P.C. (1989). Integrity of the preimplantation pig blastocyst during expansion and loss of polar trophectoderm (Rauber cells) and the morphology of the embryoblast as an indicator for developmental stage. J. Reprod. Fertil. 87, 715–26.CrossRefGoogle ScholarPubMed
Cai, K.Q., Capo-Chichi, C.D., Rula, M.E., Yang, D.H. & Xu, X.X. (2008). Dynamic GATA6 expression in primitive endoderm formation and maturation in early mouse embryogenesis. Dev. Dynam. 237, 2820–9.CrossRefGoogle ScholarPubMed
du Puy, L., Lopes, S.M., Haagsman, H.P. & Roelen, B.A. (2011). Analysis of co-expression of OCT4, NANOG and SOX2 in pluripotent cells of the porcine embryo, in vivo and in vitro. Theriogenology 75, 513–26.Google Scholar
Evans, M. J., Notarianni, E., Laurie, S. & Moor, R.M. (1990). Derivation and preliminary characterization of pluripotent cell-lines from porcine and bovine blastocysts. Theriogenology 33, 125–8.CrossRefGoogle Scholar
Fléchon, J.E., Degrouard, J. & Fléchon, B. (2004). Gastrulation events in the pre-streak pig embryo: ultrastructure and cell markers. Genesis 38, 13–25.CrossRefGoogle Scholar
Gao, Y., Hyttel, P. & Hall, V.J. (2011). Dynamic changes in epigenetic marks and gene expression during porcine epiblast specification. Cell Reprogram. 13, 345–60.CrossRefGoogle ScholarPubMed
Ginis, I., Luo, Y., Miura, T., Thies, S., Brandenberger, R., Gerecht-Nir, S., Amit, M., Hoke, A., Carpenter, M.K., Itskovitz-Eldor, J. & Rao, M.S. (2004). Differences between human and mouse embryonic stem cells. Dev. Biol. 269, 360–80.CrossRefGoogle ScholarPubMed
Hall, V.J., Jacobsen, J.V., Rasmussen, M.A. & Hyttel, P. (2010). Ultrastructural and molecular distinctions between the porcine inner cell mass and epiblast reveal unique pluripotent cell states. Dev. Dynam. 239, 2911–20.Google Scholar
Hassoun, R., Schwartz, P., Feistel, K., Blum, M. & Viebahn, C. (2009). Axial differentiation and early gastrulation stages of the pig embryo. Differentiation 78, 301–11.CrossRefGoogle ScholarPubMed
Joyce, B. & Srinivas, S. (2012). Cell movements in the egg cylinder stage mouse embryo. In Mouse Development: From Oocyte to Stem Cells. Results and Problems in Cell Differentiation (ed. Kubiak, J.Z.), pp. 219–29. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Kirchhof, N., Carnwath, J.W., Lemme, E., Anastassiadis, K., Schöler, H. & Niemann, H. (2000). Expression pattern of Oct-4 in preimplantation embryos of different species. Biol. Reprod. 63, 1698–705.CrossRefGoogle ScholarPubMed
Koutsourakis, M., Langeveld, A., Patient, R., Beddington, R. & Grosveld, F. (1999). The transcription factor GATA6 is essential for early extra-embryonic development. Development 126, 723–32.CrossRefGoogle Scholar
Kuijk, E.W., Du Puy, L., Van Tol, H.T., Oei, C.H., Haagsman, H.P., Colenbrander, B. & Roelen, B.A. (2008). Differences in early lineage segregation between mammals. Dev. Dynam. 237, 918–27.Google Scholar
Kumar, B.M., Maeng, G.H., Jeon, R.H., Lee, Y.M., Lee, W.J., Jeon, B.G., Ock, S.A. & Rho, G.J. (2012). Developmental expression of lineage specific genes in porcine embryos of different origins. J. Assist. Reprod. Genet. 29, 723–33.CrossRefGoogle ScholarPubMed
Nagy, A., Gertsenstein, M., Vintersten, K. & Behringer, R. (2002). Manipulating the Mouse Embryo: A Laboratory Manual 3rd edn.Cold Spring Harbor, USA: Cold Spring Harbor Laboratory Press.Google Scholar
Patten, B.M. (1948). Embryology of the Pig 3rd edn. Philadelphia: The Blakiston Company.Google Scholar
Perry, J.S. & Rowlands, I.W. (1962). Early pregnancy in the pig. J. Reprod. Fertil. 4, 175–88.CrossRefGoogle Scholar
Rodríguez, A., Allegrucci, C. & Alberio, R. (2012). Modulation of pluripotency in the porcine embryo and iPS cells. PLoS One 7, e49079. doi:10.1371/journal.pone.0049079CrossRefGoogle ScholarPubMed
van de Pavert, S.A., Schipper, H., de Wit, A.A., Soede, N.M., van den Hurk, R., Taverne, M.A., Boerjan, M.L. & Stroband, H.W. (2001). Comparison of anterior–posterior development in the porcine versus chicken embryo, using goosecoid expression as a marker. Reprod. Fertil. Dev. 13, 177–85.Google Scholar
Vejlsted, M., Du, Y., Vajta, G. & Maddox-Hyttel, P. (2006a). Post-hatching development of the porcine and bovine embryo-defining criteria for expected development in vivo and in vitro. Theriogenology 65, 153–65.CrossRefGoogle ScholarPubMed
Vejlsted, M., Offenberg, H., Thorup, F. & Maddox-Hyttel, P. (2006b). Confinement and clearance of OCT4 in the porcine embryo at stereomicroscopically defined stages around gastrulation. Mol. Reprod. Dev. 73, 709–18.CrossRefGoogle ScholarPubMed
Wolf, X.A., Rasmussen, M.A., Schauser, K., Jensen, A.T., Schmidt, M. & Hyttel, P. (2011a). OCT4 expression in outgrowth colonies derived from porcine inner cell masses and epiblasts. Reprod. Domest. Anim. 46, 385–92.CrossRefGoogle ScholarPubMed
Wolf, X.A., Serup, P. & Hyttel, P. (2011b). Three-dimensional localisation of NANOG, OCT4, and E-CADHERIN in porcine pre- and peri-implantation embryos. Dev. Dynam. 240, 204–10.CrossRefGoogle ScholarPubMed
Wolf, X.A, Serup, P. & Hyttel, P. (2011c). Three-dimensional immunohistochemical characterization of lineage commitment by localization of T and FOXA2 in porcine peri-implantation embryos. Dev. Dynam. 240, 890–7.Google Scholar
Yamada, T., Kawamata, T., Walker, D.G. & McGeer, P.L. (1992). Vimentin immunoreactivity in normal and pathological human brain tissue. Acta Neuropathol. 84, 157–62.CrossRefGoogle ScholarPubMed