Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo

Genes and Development

Volumn 13, Issue 14, 1999, Pages 1834-1846

  Sun, Xin ^a   Meyers, Erik N ^a,b   Lewandoski, Mark ^a   Martin, Gail R ^a  

^a Dept Anat Prog in Devmtl Biol ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anterior visceral endoderm; Cell migration; Epithelial to mesenchymal transition; Fgf4; Fgf8; Gastrulation; Mouse embryo; Neuroectoderm patterning; Primitive streak

Indexed keywords

FIBROBLAST GROWTH FACTOR;

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; EMBRYO; EMBRYO PATTERN FORMATION; ENDODERM; EPITHELIUM; GASTRULATION; GENE DISRUPTION; GENE EXPRESSION; MESENCHYME; MESODERM; MOUSE; NEUROECTODERM; NONHUMAN; PHENOTYPE; PRIMITIVE STREAK; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA; MAMMALIA;

EID: 0033565746     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.14.1834     Document Type: Article

References (71)

1. Amaya, E., T.J. Musci, and M.W. Kirschner. 1991. Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66: 257-270.
2. Ang, S.-L., A. Wierda, D. Wong, K.A. Stevens, S. Cascio, J. Rossant, and K.S. Zaret. 1993. The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119: 1301-1315.
3. Ang, S.-L., R.A. Conlon, O. Jin, and J. Rossant. 1994. Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development 120: 2979-2989.
4. Arman, E., R. Haffner-Krausz, Y. Chen, J.K. Heath, and P. Lonai. 1998. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc. Natl. Acad. Sci. 95: 5082-5087.
5. Baldwin, H.S., H.M. Shen, H.C. Yan, H.M. DeLisser, A. Chung, C. Mickanin, T. Trask, N.E. Kirschbaum, P.J. Newman, S.M. Albelda, and C.A. Buck. 1994. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): Alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 120: 2539-2553.
6. Barnes, J.D., J.L. Crosby, C.M. Jones, C.V. Wright, and B.L. Hogan. 1994. Embryonic expression of Lim-1, the mouse homolog of Xenopus Xlim-1, suggests a role in lateral mesoderm differentiation and neurogenesis. Dev. Biol. 161: 168-178.
7. Basilico, C. and D. Moscatelli. 1992. The FGF family of growth factors and oncogenes. Adv. Cancer Res. 59: 115-165.
8. Beddington, R.S.P. and E.J. Robertson. 1998. Anterior patterning in mouse. Trends Genet. 14: 277-284.
9. _. 1999. Axis development and early asymmetry in mammals. Cell 96: 195-209.
10. Belo, J.A., T. Bouwmeester, L. Leyns, N. Kertesz, M. Gallo, M. Follettie, and E.M. De Robertis. 1997. Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68: 45-57.
11. Blum, M., S.J. Gaunt, K.W. Cho, H. Steinbeisser, B. Blumberg, D. Bittner, and E.M. De Robertis. 1992. Gastrulation in the mouse: The role of the homeobox gene goosecoid. Cell 69: 1097-1106.
12. Bouillet, P., C. Chazaud, M. Oulad-Abdelghani, P. Dolle, and P. Chambon. 1995. Sequence and expression pattern of the Stra7 [Gbx-2] homeobox-containing gene induced by retinoic acid in P19 embryonal carcinoma cells. Dev. Dynamics 204: 372-382.
13. Burdsal, C.A., C.H. Damsky, and R.A. Pedersen. 1993. The role of E-cadherin and integrins in mesoderm differentiation and migration at the mammalian primitive streak. Development 118: 829-844.
14. Chapman, D. and V. Papaioannou. 1998. Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature 391: 695-697.
15. Chapman, D., I. Agulnik, S. Hancock, L. Silver, and V. Papaioannou. 1996. Tbx6, a mouse T-box gene implicated in paraxial mesoderm formation at gastrulation. Dev. Biol. 180: 534-542.
16. Chen, E.B. and M.J. Stern. 1998. Understanding cell migration guidance: Lessons from sex myoblast migration in C. elegans. Trends Genet. 14: 322-327.
17. Chesley, P. 1935. Development of the short-tailed mutant in the house mouse. J. Exp. Zool. 70: 429-459.
18. Ciruna, B.G., L. Schwartz, K. Harpal, T.P. Yamaguchi, and J. Rossant. 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.
19. Collignon, J., I. Varlet, and E.J. Robertson. 1996. Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature 381: 155-158.
20. Crossley, P.H. and G.R. Martin. 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: 439-451.
21. Deng, C.-X., A. Wynshaw-Boris, M.M. Shen, C. Daugherty, D.M. Ornitz, and P. Leder. 1995. Murine FGFR-1 is required for early postimplantation growth and axial formation. Genes & Dev. 8: 3045-3057.
22. Ding, J., L. Yang, Y.T. Yan, A. Chen, N. Desai, A. Wynshaw-Boris, and M.M. Shen. 1998. Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo. Nature 395: 702-707.
23. Doniach, T. 1993. Planar and vertical induction of anteroposterior pattern during the development of the amphibian central nervous system. J. Neurobiol 24: 1256-1275.
24. Dush, M. and G.R. Martin. 1992. Analysis of mouse Evx genes: Evx-1 displays graded expression in the primitive streak. Dev. Biol. 151: 273-287.
25. Echelard, Y., D.J. Epstein, B. St-Jacques, L. Shen, R.J. Mohle, J.A. McMahon, and A.P. McMahon. 1993. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75: 1417-1430.
26. Faust, C., A. Schumacher, B. Holdener, and T. Magnuson. 1995. The eed mutation disrupts anterior mesoderm production in mice. Development 121: 273-285.
27. Faust, C., K.A. Lawson, N.J. Schork, B. Thiel, and T. Magnuson. 1998. The Polycomb-group gene eed is required for normal morphogenetic movements during gastrulation in the mouse embryo. Development 125: 4495-4506.
28. Feldman, B., W. Poueymirou, V.E. Papaioannou, T.M. DeChiara, and M. Goldfarb. 1995. Requirement of FGF-4 for postimplantation mouse development. Science 267:246-249.
29. Frohman, M.A., M. Boyle, and G.R. Martin. 1990. Isolation of the mouse Hox-2.9 gene: Analysis of embryonic expression suggests that positional information along the anterior posterior axis is specified by mesoderm. Development 110: 589-607.
30. Furuta, Y., D. Ilic, S. Kanazawa, N. Takeda, T. Yamamoto, and S. Aizawa. 1995. Mesodermal defect in late phase of gastrulation by a targeted mutation of focal adhesion kinase, FAK. Oncogene 11: 1989-1995.
31. George, E.L., E.N. Georges-Labouesse, R.S. Patel-King, H. Rayburn, and R.O. Hynes. 1993. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119: 1079-1091.
32. Ginsburg, M., M. Snow, and A. McLaren. 1990. Primordial germ cells in the mouse embryo during gastrulation. Development 110: 521-528.
33. Griffin, K., S. Amacher, C. Kimmel, and D. Kimelman, 1998. Molecular identification of spadetail: Regulation of zebrafish trunk and tail mesoderm formation by T-box genes. Development 125: 3379-3388.
34. Haub, O. and M. Goldfarb. 1991. Expression of the fibroblast growth factor-5 gene in the mouse embryo. Development 112: 397-406.
35. Hébert, J.M., M. Boyle, and G.R. Martin. 1991. mRNA localization studies suggest that murine fibroblast growth factor-5 plays a role in gastrulation. Development 112: 407-415.
36. Hébert, J., T. Rosenquist, J. Götz, and G. Martin. 1994. FGF5 as a regulator of the hair growth cycle: Evidence from targeted and spontaneous mutations. Cell 78: 1017-1025.
37. Hermesz, E., S. Mackem, and K.A. Mahon. 1996. Rpx: A novel anterior-restricted homeobox gene progressively activated in the prechordal plate, anterior neural plate and Rathke's pouch of the mouse embryo. Development 122: 41-52.
38. Kimelman, D. and M.W. Kirschner. 1987. Synergistic induction of mesoderm by FGF and TGF-β and the identification of an mRNA coding for FGF in the early Xenopus embryo. Cell 51: 869-877.
39. Lawson, K.A., J.J. Meneses, and R.A. Pedersen. 1991. Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113: 891-911.
40. Mahmood, R., J. Bresnick, A. Hornbruch, C. Mahony, N. Morton, K. Colquhoun, P. Martin, A. Lumsden, C. Dickson, and I. Mason. 1995. A role for FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol. 5: 797-806.
41. Mansour, S.L., J.M. Goddard, and M.R. Capecchi. 1993. Mice homozygous for a targeted disruption of the proto-oncogene int-2 have developmental defects in the tail and inner ear. Development 117: 13-28.
42. Maruoka, Y., N. Ohbayashi, M. Hoshikawa, N. Itoh, B. Hogan, and Y. Furuta. 1998. Comparison of the expression of three highly related genes, Fgf8, Fgf17 and Fgf18, in the mouse embryo. Mech. Dev. 74: 175-177.
43. Meyers, E.N., M. Lewandoski, and G.R. Martin. 1998. An Fgf8 mutant allelic series generated by Cre-and Flp-mediated recombination. Nat. Genet. 18: 136-141.
44. Monaghan, A.P., K.H. Kaestner, E. Grau, and G. Schutz. 1993. Postimplantation expression patterns indicate a role for the mouse forkhead/HNF-3 alpha, beta and gamma genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm. Development 119: 567-578.
45. Nakatsuji, N., M.H. Snow, and C.C. Wylie. 1986. Cinemicrographic study of the cell movement in the primitive-streak-stage mouse embryo. J. Embryol. Exp. Morphol. 96: 99-109.
46. Neubüser, A., H. Peters, R. Balling, and G.R. Martin. 1997. Antagonistic interactions between FGF and BMP signaling pathways: A mechanism for positioning the sites of tooth formation. Cell 90: 247-255.
47. Niswander, L. and G.R. Martin. 1992. Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114: 755-768.
48. Ohbayashi, N., M. Hoshikawa, S. Kimura, M. Yamasaki, S. Fukui, and N. Itoh. 1998. Structure and expression of the mRNA encoding a novel fibroblast growth factor, FGF-18. J. Biol. Chem. 273: 18161-18164.
49. Oliver, G., A. Mailhos, R. Wehr, N.G. Copeland, N.A. Jenkins, and P. Gruss. 1995. Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121: 4045-4055.
50. Quinlan, G., E. Williams, S. Tan, and P. Tam. 1995. Neuroectodermal fate of epiblast cells in the distal region of the mouse egg cylinder: Implication for body plan organization during early embryogenesis. Development 121: 87-98.
51. Ruiz I Altaba, A. 1993. Induction and axial patterning of the neural plate: Planar and vertical signals. J. Neurobiol. 24: 1276-1304.
52. Sasaki, H. and B.L. Hogan. 1993. Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118: 47-59.
53. Schumacher, A., C. Faust, and T. Magnuson. 1996. Positional cloning of a global regulator of anterior-posterior patterning in mice. Nature 384: 19-26.
54. Shawlot, W. and R.R. Behringer. 1995. Requirement for Lim1 in head-organizer function. Nature 374: 425-430.
55. Simeone, A., D. Acampora, A. Mallamaci, A. Stornaiuolo, M.R. D'Apice, V. Nigro, and E. Boncinelli. 1993. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 12: 2735-2747.
56. Skaer, H. 1997. Morphogenesis: FGF branches out. Curr. Biol. 7: 238-241.
57. Slack, J.M.W., B.G. Darlington, J.K. Heath, and S.F. Godsave. 1987. Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. Nature 326: 197-200.
58. Slack, J., H. Issacs, J. Song, L. Durbin, and M. Pownall. 1996. The role of fibroblast growth factors in early Xenopus development. Biochem. Soc. Symp. 62: 1-12.
59. Smith, J.C., N.A. Armes, F.L. Conlon, M. Tada, M. Umbhauer, and K.M. Weston. 1997. Upstream and downstream from Brachyury, a gene required for vertebrate mesoderm formation. Cold Spring Harb. Symp. Quant. Biol. 62: 337-346.
60. Tam, P.P.L. and R.R. Behringer. 1997. Mouse gastrulation: The formation of a mammalian body plan. Mech. Dev. 68: 3-25.
61. Thomas, P. and R. Beddington. 1996. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6: 1487-1496.
62. Thomas, P.Q., A. Brown, and R.S. Beddington. 1998. Hex: A homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors. Development 125: 85-94.
63. Tsang, A., J. Visvader, C. Turner, Y. Fujiwara, C. Yu, M. Weiss, M. Crossley, and S. Orkin. 1997. FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation. Cell 90: 109-119.
64. Varlet, I., J. Collignon, and E.J. Robertson. 1997. nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 124: 1033-1044.
65. Wassarman, K., M. Lewandoski, K. Campbell, A.L. Joyner, J.L.R. Rubenstein, S. Martinez, and G.R. Martin. 1997. Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development 124: 2923-2934.
66. Wilkinson, D., G. Peters, C. Dickson, and A. McMahon. 1988. Expression of the FGF-related proto-oncogene int-2 during gastrulation and neurulation in the mouse. EMBO J. 7: 691-695.
67. Wilkinson, D.G., S. Bhatt, and B.G. Herrmann. 1990. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343: 657-659.
68. Wilson, V., L. Manson, W.C. Skarnes, and R.S. Beddington. 1995. The T gene is necessary for normal mesodermal morphogenetic cell movements during gastrulation. Development 121: 877-886.
69. Winnier, G., M. Blessing, P.A. Labosky, and B.L. Hogan. 1995. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes & Dev. 9: 2105-2116.
70. Yamaguchi, T.P., K. Harpal, M. Henkemeyer, and J. Rossant. 1995. fgfr1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes & Dev. 8: 3032-3044.
71. Yang, J.T., H. Rayburn, and R.O. Hynes. 1993. Embryonic mesodermal defects in alpha 5 integrin-deficient mice. Development 119: 1093-1105.