Skip to main content

Establishment of Anterior–Posterior Axis in the Mouse Embryo

  • Chapter
  • First Online:
New Principles in Developmental Processes
  • 1118 Accesses

Abstract

The anterior–posterior (A–P) axis is the first established and morphologically discernible axis of the body during mouse development. From embryonic day (E) 4.5 to E6.5 of mouse embryos, the formation of the distal visceral endoderm (DVE) followed by that of the anterior visceral endoderm (AVE) breaks the A–P symmetry of the embryo. The DVE progenitor cells arise in primitive endoderm (PrE) cells of the late blastocyst with an asymmetrical distribution. This asymmetry may contribute to the determination of the A–P axis in later embryos. At E5.5, DVE cells mature, and migrate from the distal tip to the future anterior side. The DVE migration guides the migration of newly formed AVE and trigger the extensive movement of visceral endoderm (VE) cells in a wide area. Our observations revise the earlier model about AVE development, namely, that the AVE is directly derived from the DVE.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Beddington RS, Robertson EJ (1999) Axis development and early asymmetry in mammals. Cell 96(2):195–209. doi:10.1016/S0092-8674(00)80560-7

    Article  CAS  PubMed  Google Scholar 

  • Bloomekatz J, Grego-Bessa J, Migeotte I, Anderson KV (2012) Pten regulates collective cell migration during specification of the anterior-posterior axis of the mouse embryo. Dev Biol 364(2):192–201. doi:10.1016/j.ydbio.2012.02.005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brennan J, Lu CC, Norris DP, Rodriguez TA, Beddington RS, Robertson EJ (2001) Nodal signalling in the epiblast patterns the early mouse embryo. Nature (Lond) 411(6840):965–969. doi:10.1038/35082103

    Article  CAS  Google Scholar 

  • Camus A, Perea-Gomez A, Moreau A, Collignon J (2006) Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo. Dev Biol 295(2):743–755. doi:10.1016/j.ydbio.2006.03.047

    Article  CAS  PubMed  Google Scholar 

  • Chazaud C, Rossant J (2006) Disruption of early proximodistal patterning and AVE formation in Apc mutants. Development(Camb) 133(17):3379–3387. doi:10.1242/dev.02523

    CAS  Google Scholar 

  • Chu J, Shen MM (2010) Functional redundancy of EGF-CFC genes in epiblast and extraembryonic patterning during early mouse embryogenesis. Dev Biol 342(1):63–73. doi:10.1016/j.ydbio.2010.03.009

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • del Barco Barrantes I, Davidson G, Grone HJ, Westphal H, Niehrs C (2003) Dkk1 and noggin cooperate in mammalian head induction. Genes Dev 17(18):2239–2244. doi:10.1101/gad.269103

    Article  PubMed Central  PubMed  Google Scholar 

  • Ding J, Yang L, Yan YT, Chen A, Desai N, Wynshaw-Boris A, Shen MM (1998) Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo. Nature (Lond) 395(6703):702–707. doi:10.1038/27215

    Article  CAS  Google Scholar 

  • Granier C, Gurchenkov V, Perea-Gomez A, Camus A, Ott S, Papanayotou C, Iranzo J, Moreau A, Reid J, Koentges G, Saberan-Djoneidi D, Collignon J (2011) Nodal cis-regulatory elements reveal epiblast and primitive endoderm heterogeneity in the peri-implantation mouse embryo. Dev Biol 349(2):350–362. doi:10.1016/j.ydbio.2010.10.036

    Article  CAS  PubMed  Google Scholar 

  • Huynh JR, St. Johnston D (2004) The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr Biol 14(11):R438–449. doi:10.1016/j.cub.2004.05.040

    Article  CAS  PubMed  Google Scholar 

  • Kimura C, Yoshinaga K, Tian E, Suzuki M, Aizawa S, Matsuo I (2000) Visceral endoderm mediates forebrain development by suppressing posteriorizing signals. Dev Biol 225(2):304–321. doi:10.1006/dbio.2000.9835

    Article  CAS  PubMed  Google Scholar 

  • Kimura C, Shen MM, Takeda N, Aizawa S, Matsuo I (2001) Complementary functions of Otx2 and Cripto in initial patterning of mouse epiblast. Dev Biol 235(1):12–32. doi:10.1006/dbio.2001.0289

    Article  CAS  PubMed  Google Scholar 

  • Kimura-Yoshida C, Nakano H, Okamura D, Nakao K, Yonemura S, Belo JA, Aizawa S, Matsui Y, Matsuo I (2005) Canonical Wnt signaling and its antagonist regulate anterior-posterior axis polarization by guiding cell migration in mouse visceral endoderm. Dev Cell 9(5):639–650. doi:10.1016/j.devcel.2005.09.011

    Article  CAS  PubMed  Google Scholar 

  • Meno C, Saijoh Y, Fujii H, Ikeda M, Yokoyama T, Yokoyama M, Toyoda Y, Hamada H (1996) Left-right asymmetric expression of the TGF beta-family member lefty in mouse embryos. Nature (Lond) 381(6578):151–155. doi:10.1038/381151a0

    Article  CAS  Google Scholar 

  • Mesnard D, Guzman-Ayala M, Constam DB (2006) Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development (Camb) 133(13):2497–2505. doi:10.1242/dev.02413

    CAS  Google Scholar 

  • Migeotte I, Omelchenko T, Hall A, Anderson KV (2010) Rac1-dependent collective cell migration is required for specification of the anterior-posterior body axis of the mouse. PLoS Biol 8(8):e1000442. doi:10.1371/journal.pbio.1000442

    Article  PubMed Central  PubMed  Google Scholar 

  • Morkel M, Huelsken J, Wakamiya M, Ding J, van de Wetering M, Clevers H, Taketo MM, Behringer RR, Shen MM, Birchmeier W (2003) Beta-catenin regulates Cripto- and Wnt3-dependent gene expression programs in mouse axis and mesoderm formation. Development (Camb) 130(25):6283–6294. doi:10.1242/dev.00859

    Article  CAS  Google Scholar 

  • Morris SA, Grewal S, Barrios F, Patankar SN, Strauss B, Buttery L, Alexander M, Shakesheff KM, Zernicka-Goetz M (2012) Dynamics of anterior-posterior axis formation in the developing mouse embryo. Nat Commun 3:673. doi:10.1038/ncomms1671

    Article  PubMed Central  PubMed  Google Scholar 

  • Nakamura T, Hamada H (2012) Left-right patterning: conserved and divergent mechanisms. Development (Camb) 139(18):3257–3262. doi:10.1242/dev.061606

    Article  CAS  Google Scholar 

  • Nakamura T, Mine N, Nakaguchi E, Mochizuki A, Yamamoto M, Yashiro K, Meno C, Hamada H (2006) Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system. Dev Cell 11(4):495–504. doi:10.1016/j.devcel.2006.08.002

    Article  CAS  PubMed  Google Scholar 

  • Nomura M, Li E (1998) Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature (Lond) 393(6687):786–790. doi:10.1038/31693

    Article  CAS  Google Scholar 

  • Nowotschin S, Costello I, Pillisezek A, Kwon GS, Mao CA, Klein WH, Robertson EJ, Hadjantonakis AK (2013) The T-box transcription factor Eomesodermin is essential for AVE induction in the mouse embryos. Genens Dev 27(9):997–1002. doi:10.1101/gad.215152.113

    Google Scholar 

  • Perea-Gomez A, Vella FD, Shawlot W, Oulad-Abdelghani M, Chazaud C, Meno C, Pfister V, Chen L, Robertson E, Hamada H, Behringer RR, Ang SL (2002) Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev Cell 3(5):745–756

    Article  CAS  PubMed  Google Scholar 

  • Rakeman AS, Anderson KV (2006) Axis specification and morphogenesis in the mouse embryo require Nap1, a regulator of WAVE-mediated actin branching. Development (Camb) 133(16):3075–3083. doi:10.1242/dev.02473

    Article  CAS  Google Scholar 

  • Rivera-Perez JA, Mager J, Magnuson T (2003) Dynamic morphogenetic events characterize the mouse visceral endoderm. Dev Biol 261(2):470–487. doi:10.1016/S0012-1606(03)00302-6

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez TA, Srinivas S, Clements MP, Smith JC, Beddington RS (2005) Induction and migration of the anterior visceral endoderm is regulated by the extra-embryonic ectoderm. Development (Camb) 132(11):2513–2520. doi:10.1242/dev.01847

    Article  CAS  Google Scholar 

  • Rossant J, Tam PP (2009) Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development (Camb) 136(5):701–713. doi:10.1242/dev.017178

    Article  CAS  Google Scholar 

  • Srinivas S (2006) The anterior visceral endoderm-turning heads. Genesis 44(11):565–572. doi:10.1002/dvg.20249

    Article  CAS  PubMed  Google Scholar 

  • Sugihara K, Nakatsuji N, Nakamura K, Nakao K, Hashimoto R, Otani H, Sakagami H, Kondo H, Nozawa S, Aiba A, Katsuki M (1998) Rac1 is required for the formation of three germ layers during gastrulation. Oncogene 17(26):3427–3433. doi:10.1038/sj.onc.1202595

    Article  CAS  PubMed  Google Scholar 

  • Takaoka K, Hamada H (2012) Cell fate decisions and axis determination in the early mouse embryo. Development (Camb) 139(1):3–14. doi:10.1242/dev.060095

    Article  CAS  Google Scholar 

  • Takaoka K, Yamamoto M, Shiratori H, Meno C, Rossant J, Saijoh Y, Hamada H (2006) The mouse embryo autonomously acquires anterior-posterior polarity at implantation. Dev Cell 10(4):451–459. doi:10.1016/j.devcel.2006.02.017

    Article  CAS  PubMed  Google Scholar 

  • Takaoka K, Yamamoto M, Hamada H (2011) Origin and role of distal visceral endoderm, a group of cells that determines anterior-posterior polarity of the mouse embryo. Nat Cell Biol 13(7):743–752. doi:10.1038/ncb2251

    Article  CAS  PubMed  Google Scholar 

  • Tam PP, Loebel DA (2007) Gene function in mouse embryogenesis: get set for gastrulation. Nat Rev Genet 8(5):368–381. doi:10.1038/nrg2084

    Article  CAS  PubMed  Google Scholar 

  • Trichas G, Smith AM, White N, Wilkins V, Watanabe T, Moore A, Joyce B, Sugnaseelan J, Rodriguez TA, Kay D, Baker RE, Maini PK, Srinivas S (2012) Multi-cellular rosettes in the mouse visceral endoderm facilitate the ordered migration of anterior visceral endoderm cells. PLoS Biol 10(2):e1001256. doi:10.1371/journal.pbio.1001256

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Waldrip WR, Bikoff EK, Hoodless PA, Wrana JL, Robertson EJ (1998) Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell 92(6):797–808

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto M, Saijoh Y, Perea-Gomez A, Shawlot W, Behringer RR, Ang SL, Hamada H, Meno C (2004) Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature (Lond) 428(6981):387–392. doi:10.1038/nature02418

    Article  CAS  Google Scholar 

  • Yamamoto M, Beppu H, Takaoka K, Meno C, Li E, Miyazono K, Hamada H (2009) Antagonism between Smad1 and Smad2 signaling determines the site of distal visceral endoderm formation in the mouse embryo. J Cell Biol 184(2):323–334. doi:10.1083/jcb.200808044

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamanaka Y, Ralston A, Stephenson RO, Rossant J (2006) Cell and molecular regulation of the mouse blastocyst. Dev Dyn 235(9):2301–2314. doi:10.1002/dvdy.20844

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank members of the Hamada laboratory for discussion.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katsuyoshi Takaoka .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Japan

About this chapter

Cite this chapter

Takaoka, K. (2014). Establishment of Anterior–Posterior Axis in the Mouse Embryo. In: Kondoh, H., Kuroiwa, A. (eds) New Principles in Developmental Processes. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54634-4_2

Download citation

Publish with us

Policies and ethics