Nodal signal is required for morphogenetic movements of epiblast layer in the pre-streak chick blastoderm

Development Growth and Differentiation

Volumn 53, Issue 3, 2011, Pages 366-377

  Yanagawa, Nariaki ^a   Sakabe, Masahide ^b   Sakata, Hirokazu ^a   Yamagishi, Toshiyuki ^a   Nakajima, Yuji ^a  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NARA MEDICAL UNIVERSITY   (Japan)

Author keywords

Gastrulation; Multicellular rosette; Nodal signal; Polonaise movements; Prestreak chick epiblast

Indexed keywords

3 [4 METHYL 2 (2 OXO 3 INDOLINYLMETHYLIDENYL) 3 PYRROLYL]PROPIONIC ACID; LEFT RIGHT DETERMINATION FACTOR; NODAL SIGNALING PROTEIN;

ARTICLE; BLASTODERM; CELL CULTURE; CELL MOTION; CHICK; ECTODERM; EMBRYO; ENZYME INHIBITION; IN VIVO STUDY; NODAL SIGNAL; NONHUMAN; PRIMITIVE STREAK; SIGNAL TRANSDUCTION;

ANIMALS; BLASTODERM; CELL MOVEMENT; CHICK EMBRYO; CHICKENS; EPITHELIUM; FETAL PROTEINS; LEFT-RIGHT DETERMINATION FACTORS; MORPHOGENESIS; NODAL PROTEIN; PYRROLES; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS;

AMNIOTA;

EID: 79954621627     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2010.01244.x     Document Type: Article

References (54)

1. Bancroft, M. & Bellairs, R. 1974. The onset of differentiation in the epiblast of the chick blastoderm (SEM and TEM). Cell Tissue Res. 155, 399-418.
2. Bertocchini, F. & Stern, C. D. 2002. The hypoblast of the chick embryo positions the primitive streak by antagonizing nodal signaling. Dev. Cell 3, 735-744.
3. Blankenship, J. T., Backovic, S. T., Sanny, J. S. P., Weitz, O. & Zallen, J. A. 2006. Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev. Cell 11, 459-470.
4. Böttcher, R. T. & Niehrs, C. 2005. Fibroblast growth factor signaling during early vertebrate development. Endocr. Rev. 26, 63-77.
5. Chapman, S. C., Collignon, J., Schoenwolf, G. C. & Lumsden, A. 2001. Improved method for chick whole-embryo culture using a filter paper carrier. Dev. Dyn. 220, 284-289.
6. Chung, H. A., Hyodo-Miura, J., Nagamune, T. & Ueno, N. 2005. FGF signal regulates gastrulation cell movements and morphology through its target NRH. Dev. Biol. 282, 95-110.
7. Ciruna, B. G., Schwartz, L., Harpal, K., Yamaguchi, T. P. & Rossant, J. 1997. Chimeric analysis of fibroblast growth factor receptor-1 (Fgfr1) function: a role for FGFR1 in morphogenetic movement through the primitive streak. Development 124, 2829-2841.
8. Ciruna, B. & Rossant, J. 2001. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev. Cell 1, 37-49.
9. Cui, C., Yang, X., Chuai, M., Glazier, J. A. & Weijer, C. J. 2005. Analysis of tissue flow patterns during primitive streak formation in the chick embryo. Dev. Biol. 284, 37-47.
10. Chuai, M., Zeng, W., Yang, X., Boychenko, V., Glazier, J. A. & Weijer, C. J. 2006. Cell movement during chick primitive streak formation. Dev. Biol. 296, 137-149.
11. Chuai, M. & Weijer, C. J. 2008. The mechanisms underlying primitive streak formation in the chick embryo. Curr. Top. Dev. Biol. 81, 135-156.
12. Conlon, F. L., Lyons, K. M., Takaesu, N., Barth, K. S., Kispert, A., Herrmann, B. & Robertson, E. J. 1994. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120, 1919-1928.
13. Darnell, D. K., Garcia-Martinez, V., Lopez-Sanchez, C., Yuan, S. & Schoenwolf, G. C. 2000. Dynamic labeling techniques for fate mapping, testing cell commitment, and following living cells in avian embryos. In Methods in Molecular Biology, Vol. 135: Developmental Biology Protocols, Vol. 1 (Eds R. S. Tuan & C. W. Lo), pp. 305-321. Humana Press Inc, Totowa, NJ.
14. Deng, C. X., Wynshaw-Boris, A., Shen, M. M., Daugherty, C., Ornitz, D. M. & Leder, P. 1994. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 8, 3045-3075.
15. Ding, J., Yang, L., Yan, Y. T., Chen, A., Desai, N., Wynshaw-Boris, A. & Shen, M. M. 1998. Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo. Nature 395, 702-706.
16. Eyal-Giladi, H. & Kochav, S. 1976. From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick: I. General morphology. Dev. Biol. 49, 321-337.
17. Foley, A. C., Skromne, I. & Stern, C. D. 2000. Reconciling different models of forebrain induction and patterning: a dual role for the hypoblast. Development 127, 3839-3854.
18. Gu, Z., Nomura, M., Simpson, B. B., Lei, H., Feijen, A., van den Eijnden-van Raaij, J., Donahoe, P. K. & Li, E. 1998. The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse. Genes Dev. 12, 844-857.
19. Gräper, L. 1929. Die Primitiventwicklung des Hünchens nach stereokinematographischen Untersuchungen kontrolliert durch vitale Farbmarkierung und verglichen mit der Entwicklung anderer Wierbeltiere. Wilhelm Roux Arch. Entwickl. Mech. Org. 116, 382-429.
20. Hamburger, V. & Hamilton, H. L. 1951. A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
21. Hatada, Y. & Stern, C. D. 1994. A fate map of the epiblast of the early chick embryo. Development 120, 2879-2889.
22. Heisenberg, C. P. & Solnica-Krezel, L. 2008. Back and forth between cell fate specification and movement during vertebrate gastrulation. Curr. Opin. Genet. Dev. 18, 311-316.
23. Khaner, O. 1995. The rotated hypoblast of the chicken embryo does not initiate an ectopic axis in the epiblast. Proc. Natl Acad. Sci. USA 92, 10733-10737.
24. Kochav, S., Ginsburg, M. & Eyal-Giladi, H. 1980. From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick: II. Microscopic anatomy and cell population dynamics. Dev. Biol. 79, 296-308.
25. Krieg, M., Arboleda-Estudillo, Y., Puech, P. H., Käfer, J., Graner, F., Müller, D. J. & Heisenberg, C. P. 2008. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 10, 429-436.
26. Lawson, A. & Schoenwolf, G. C. 2001a. New insights into critical events of avian gastrulation. Anat. Rec. 262, 238-252.
27. Lawson, A. & Schoenwolf, G. C. 2001b. Cell populations and morphogenetic movements underlying formation of the avian primitive streak and organizer. Genesis 29, 188-195.
28. Lawson, A., Colas, J. F. & Schoenwolf, G. C. 2001c. Classification scheme for genes expressed during formation and progression of the avian primitive streak. Anat. Rec. 262, 221-226.
29. Lu, C. C. & Robertson, E. J. 2004. Multiple roles for Nodal in the epiblast of the mouse embryo in the establishment of anterior-posterior patterning. Dev. Biol. 273, 149-159.
30. Matsui, H., Sakabe, M., Sakata, H., Yanagawa, N., Ikeda, K., Yamagishi, T. & Nakajima, Y. 2008. Induction of initial heart α-actin, smooth muscle α-actin, in chick pregastrula epiblast: the role of hypoblast and fibroblast growth factor-8. Dev. Growth Differ. 50, 143-157.
31. Mohammadi, M., McMahon, G., Sun, L., Tang, C., Hirth, P., Yeh, B. K., Hubbard, S. R. & Schlessinger, J. 1997. Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276, 955-960.
32. Muhr, J., Graziano, E., Wilson, S., Jessell, T. M. & Edlund, T. 1999. Convergent inductive signals specify midbrain, hindbrain, and spinal cord identity in gastrula stage chick embryos. Neuron 23, 689-702.
33. Nishimura, T. & Takeichi, M. 2008. Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 135, 1493-1502.
34. Nieto, M. A., Patel, K. & Wilkinson, D. G. 1996. In situ hybridization analysis of chick embryos in whole mount and tissue sections. In Methods in Cell Biology (Ed. M. Bronner-Fraser), pp. 220-235. Academic Press, San Diego.
35. Perea-Gomez, A., Vella, F. D. J., Shawlot, W., Oulad-Abdelghani, M., Chazaud, C., Meno, C., Pfister, V., Chen, L., Robertson, E., Hamada, H., Behringer, R. R. & Ang, S. L. 2002. Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev. Cell 3, 745-756.
36. Piccolo, S., Agius, E., Leyns, L., Bhattacharyya, S., Grunz, H., Bouwmeester, T. & De Robertis, E. M. 1999. The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397, 707-710.
37. Redkar, A., Montgomery, M. & Litvin, J. 2001. Fate map of early avian cardiac progenitor cells. Development 128, 2269-2279.
38. Sakabe, M., Sakata, H., Matsui, H., Ikeda, K., Yamagishi, T. & Nakajima, Y. 2008. ROCK1 expression is regulated by TGFβ3 and ALK2 during valvuloseptal endocardial cushion formation. Anat. Rec. 291, 845-857.
39. Sakata, H., Sakabe, M., Matsui, H., Kawada, N., Nakatani, K., Ikeda, K., Yamagishi, T. & Nakajima, Y. 2007. Rho kinase inhibitor Y27632 affects initial heart myofibrillogenesis in cultured chick blastoderm. Dev. Dyn. 236, 461-472.
40. Shen, M. M. 2007. Nodal signaling: developmental roles and regulation. Development 134, 1023-1034.
41. Skromne, I. & Stern, C. D. 2002. A hierarchy of gene expression accompanying induction of the primitive streak by Vg1 in the chick embryo. Mech. Dev. 114, 115-118.
42. Spratt Jr, N. T. 1946. Formation of the primitive streak in the explanted chick blastoderm marked with carbon particles. J. Exp. Zool. 103, 259-304.
43. Stern, C. D. 2004. Gastrulation in the chick. In Gastrulation Form Cells to Embryos (Ed. C. D. Stern), pp. 219-232. CSHL Press, New York.
44. Streit, A., Lee, K. J., Woo, I., Roberts, C., Jessell, T. M. & Stern, C. D. 1998. Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development 125, 507-519.
45. 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, 1834-1846.
46. Vakaet, L. 1970. Cinephotomicrographic investigations of gastrulation in the chick blastoderm. Arch. Biol. 81, 387-426.
47. 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, 1049-1052.
48. Waddington, C. H. 1933. Induction by the primitive streak and its derivatives in the chick. J. Exp. Biol. 10, 38-48.
49. Wagstaff, L. J., Bellett, G., Mogensen, M. M. & Münsterberg, A. 2008. Multicellular rosette formation during cell ingression in the avian primitive streak. Dev. Dyn. 237, 91-96.
50. Waldrip, W. R., Bikoff, E. K., Hoodless, P. A., Wrana, J. L. & Robertson, E. J. 1998. Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell 92, 797-808.
51. Wei, Y. & Mikawa, T. 2000. Formation of the avian primitive streak from spatially restricted blastoderm: evidence for polarized cell division in the elongating streak. Development 127, 87-96.
52. Yang, X., Dormann, D., Münsterberg, A. E. & Weijer, C. J. 2002. Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev. Cell 3, 425-437.
53. Yamaguchi, T. P., Harpal, K., Henkemeyer, M. & Rossant, J. 1994. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 8, 3032-3044.
54. Ziv, T., Shimoni, Y. & Mitrani, E. 1992. Activin can generate ectopic axial structures in chick blastoderm explants. Development 115, 689-694.