BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo

Genes and Development

Volumn 18, Issue 15, 2004, Pages 1838-1849

  Chuva De Sousa Lopes, Susana M ^a   Roelen, Bernard A J ^b,c,d   Monteiro, Rui M ^a   Emmens, Roul ^a   Lin, Herbert Y ^b,c   Li, En ^b,c,e   Lawson, Kirstie A ^a   Mummery, Christine L ^a  

^a HUBRECHT INSTITUTE   (Netherlands)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UTRECHT UNIVERSITY   (Netherlands)

^e NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

ALK2; BMP signaling; Embryo; Mouse; Primordial germ cells; Visceral endoderm

Indexed keywords

ADENOVIRUS VECTOR; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR; FIBRONECTIN; PROTEIN ALK2; SMAD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EMBRYO CULTURE; ENDODERM; ENZYME PHOSPHORYLATION; EXPLANT; GENE DELETION; HETEROZYGOTE; IMMUNOHISTOCHEMISTRY; MOUSE; NIDATION; NONHUMAN; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ACTIVIN RECEPTORS, TYPE I; ADENOVIRIDAE; ANIMALS; BONE MORPHOGENETIC PROTEINS; EMBRYO; ENDODERM; FIBRONECTINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; HETEROZYGOTE; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

ADENOVIRIDAE; ANIMALIA;

EID: 3543127068     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.294004     Document Type: Article

References (57)

1. Anderson, R., Fässler, R., Georges-Labouesse, E., Hynes, R.O., Bader, B.L., Kreidberg, J.A., Schaible, K., Heasman, J., and Wylie, C. 1999. Mouse primordial germ cells lacking β1 integrins enter the germline but fail to migrate normally to the gonads. Development 126: 1655-1664.
2. Beppu, H., Kawabata, M., Hamamoto, T., Chytil, A., Minowa, O., Noda, T., and Miyazono, K. 2000. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev. Biol. 221: 249-258.
3. Chang, H. and Matzuk, M.M. 2001. Smad5 is required for mouse primordial germ cell development. Mech. Dev. 104: 61-67.
4. Chang, H., Huylebroeck, D., Verschueren, K., Guo, Q., Matzuk, M.M., and Zwijsen, A. 1999. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 126: 1631-1642.
5. Chiquoine, A.D. 1954. The identification, origin and migration of primordial germ cells in the mouse embryo. Anat. Rec. 118: 135-146.
6. Chuva de Sousa Lopes, S.M., Carvalho, R.L., van den Driesche S., Goumans, M.J., ten Dijke, P., and Mummery, C.L. 2003. Distribution of phosphorylated Smad2 identifies target tissues of TGFβ ligands in mouse development. Gene Expr. Patterns 3: 355-360.
7. Coucouvanis, E. and Martin, G.R. 1999. BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 126: 535-546.
8. Dolci, S., Williams, D.E., Ernst, M.K., Resnick, J.L., Brannan, C.I., Lock, L.F., Lyman, S.D., Boswell, H.S., and Donovan, P.J. 1991. Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature 352: 809-811.
9. Duncan, S.A., Manova, K., Chen, W.S., Hoodless, P., Weinstein, D.C., Bachvarova, R.F., and Damell, J.E. 1994. Expression of transcription factor HNF-4 in the extraembryonic endoderm, gut, and nephrogenic tissue of the developing mouse embryo: HNF-4 is a marker for the primary endoderm in the implanting blastocyst. Proc. Natl. Acad. Sci. 91: 7598-7602.
10. Dziadek, M. and Adamson, E. 1978. Localization and synthesis of αfoetoprotein in post-implantation mouse embryos. J. Embryol. Exp. Morph. 43: 289-313.
11. Faure, S., Lee, M.A., Keller, T., ten Dijke, P., and Whitman, M. 2000. Endogenous patterns of TGFβ superfamily signaling during early Xenopus development. Development 127: 2917-2931.
12. Fujii, M., Takeda, K., Imamura, T., Aoki, H., Sampath, T.K., Enomoto, S., Kawabata, M., Kato, M., Ichijo, H., and Miyazono, K. 1999. Roles of bone morphogenetic protein type I receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol. Biol. Cell 10: 3801-3813.
13. Fujikura, J., Yamato, E., Yonemura, S., Hosoda, K., Masui, S., Nakao, K., Miyazaki, J., and Niwa, H. 2002. Differentiation of embryonic stem cells is induced by GATA factors. Genes & Dev. 16: 784-789.
14. Ginsburg, M., Snow, M.H., and McLaren, A. 1990. Primordial germ cells in the mouse embryo during gastrulation. Development 110: 521-528.
15. Godin, I., Deed, R., Cooke, J., Zsebo, K., Dexter, M., and Wylie, C.C. 1991. Effects of the steel gene product on mouse primordial germ cells in culture. Nature 352: 807-809.
16. Goumans, M.J., Zwijsen, A., van Rooijen, M.A., Huylebroeck, D., Roelen, B.A., and Mummery, C.L. 1999. Transforming growth factor-β signalling in extraembryonic mesoderm is required for yolk sac vasculogenesis in mice. Development 126: 3473-3483.
17. Gu, Z., Reynolds, E.M., Song, J., Lei, H., Feijen, A., Yu, L., He, W., MacLaughlin, D.T., van den Eijnden-van Raaij, J., Donahoe, P.K., et al. 1999. The type I serine/threonine kinase receptor ActRIA (ALK2) is required for gastrulation of the mouse embryo. Development 126: 2551-2561.
18. Gualdi, R., Bossard, P., Zheng, M., Hamada, Y., Coleman, J.R., and Zaret, K.S. 1996. Hepatic specification of the gut endoderm in vitro: Cell signaling and transcriptional control. Genes & Dev. 10: 1670-1682.
19. Hayashi, K., Kobayashi, T., Umino, T., Goitsuka, R., Matsui, Y., and Kitamura, D. 2002. SMAD1 signaling is critical for initial commitment of germ cell lineage from mouse epiblast. Mech. Dev. 118: 99-109.
20. Inoue, K., Kohda, T., Lee, J., Ogonuki, N., Mochida, K., Noguchi, Y., Tanemura, K., Kaneko-Ishino, T., Ishino, F., and Ogura, A. 2002. Faithful expression of imprinted genes in cloned mice. Science 295: 297.
21. Korschynskyi, O. and ten Dijke, P. 2002. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 277: 4883-4891.
22. Kumar, A., Novoselov, V., Celeste, A.J., Wolfman, N.M., ten Dijke, P., and Kuehn, M.R. 2001. Nodal signaling uses activin and transforming growth factor-Β receptor-regulated Smads. J. Biol. Chem. 276: 656-661.
23. Kuo, C.T., Morrisey, E.E., Anandappa, R., Sigrist, K., Lu, M.M., Parmacek, M.S., Soudais, C., and Leiden, J.M. 1997. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes & Dev. 11: 1048-1060.
24. Lawson, K.A. and Hage, W.J. 1994. Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found. Symp. 182: 68-91.
25. Lawson, K.A., Dunn, N.R., Roelen, B.A., Zeinstra, L.M., Davis, A.M., Wright, C.V., Korving, J.P., and Hogan, B.L. 1999. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes & Dev. 13: 424-436.
26. Levenberg, S., Golub, J.S., Amit, M., Itskovitz-Eldor, J., and Langer, R. 2002. Endothelial cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. 99: 4391-4396.
27. Li, Y., Lemaire, P., and Behringer, R.R. 1997. Esxl, a novel X chromosome-linked homeobox gene expressed in mouse extraembryonic tissues and male germ cells. Dev. Biol. 188: 85-95.
28. Liu, F., Ventura, F., Doody, J., and Massagué, J. 1995. Human type II receptor for bone morphogenic proteins (BMPs): Extension of the two-kinase receptor model to the BMPs. Mol. Cell Biol. 15: 3479-3486.
29. Matzuk, M.M., Kumar, T.R., and Bradley, A. 1995. Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 374: 356-360.
30. McLaren, A. 2003. Primordial germ cells in the mouse. Dev. Biol. 262: 1-15.
31. Mishina, Y., Suzuki, A., Ueno, N., and Behringer, R.R. 1995. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes & Dev. 9: 3027-3037.
32. Mishina, Y., Crombie, R., Bradley, A., and Behringer, R.R. 1999. Multiple roles for activin-like kinase-2 signaling during mouse embryogenesis. Dev. Biol. 213: 314-326.
33. Monteiro, R.M., Chuva de Sousa Lopes, S.M., Korchynskyi, O., ten Dijke, P., and Mummery, C.L. 2004. Spatio-temporal activation of Smadl and Smad5 in vivo: Monitoring transcriptional activity of Smad proteins. J. Cell. Sci. (in press).
34. Oh, S.P. and Li, E. 1997. The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes & Dev. 11: 1812-1826.
35. Oh, S.P., Seki, T., Goss, K.A., Imamura, T., Yi, Y., Donahoe, P.K., Li, L., Miyazono, K., ten Dijke, P., Kim, S., et al. 2000. Activin receptor-like kinase 1 modulates transforming growth factor-Β1 signaling in the regulation of angiogenesis. Proc. Natl. Acad. Sci. 97: 2626-2631.
36. Persson, U., Izumi, H., Souchelnytskyi, S., Itoh, S., Grimsby, S., Engström, U., Heldin, C.H., Funa, K., and ten Dijke, P. 1998. The L45 loop in type I receptors for TGFβ family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434: 83-87.
37. Pesce, M., Gioia Klinger, F., and De Felici, M. 2002. Derivation in culture of primordial germ cells from cells of the mouse epiblast: Phenotypic induction and growth control by BMP4 signalling. Mech. Dev. 112: 15-24.
38. Qi, X., Li, T.G., Hao, J., Hu, J., Wang, J., Simmons, H., Miura, S., Mishina, Y., and Zhao, G.Q. 2004. BMP4 supports self-renewal of embryonic stem cells by inhibiting mitogen-activated protein kinase pathways. Proc. Natl. Acad. Sci. 101: 6027-6032.
39. Roelen, B.A., Lin, H.Y., Knežević, V., Freund, E., and Mummery, C.L. 1994. Expression of TGFβs and their receptors during implantation and organogenesis of the mouse embryo. Dev. Biol. 166: 716-728.
40. Roelen, B.A., Goumans, M.J., van Rooijen, M.A., and Mummery, C.L. 1997a. Differential expression of BMP receptors in early mouse development. Int. J. Dev. Biol. 41: 541-549.
41. Roelen, B.A., van Rooijen, M.A., and Mummery, C.L. 1997b. Expression of ALK-1, a type 1 serine/threonine kinase receptor, coincides with sites of vasculogenesis and angiogenesis in early mouse development. Dev. Dyn. 209: 418-430.
42. Saitou, M., Barton, S.C., and Surani, M.A. 2002. A molecular programme for the specification of germ cell fate in mice. Nature 418: 293-300.
43. Sato, M., Kimura, T., Kurokawa, K., Fujita, Y., Abe, K., Masuhara, M., Yasunaga, T., Ryo, A., Yamamoto, M., and Nakano, T. 2002. Identification of PGC7, a new gene expressed specifically in preimplantation embryos and germ cells. Mech. Dev. 113: 91-94.
44. Shi, Y. and Massagué, J. 2003. Mechanisms of TGFβ signaling from cell membrane to the nucleus. Cell 113: 685-700.
45. Song, J., Oh, S.P., Schrewe, H., Nomura, M., Lei, H., Okano, M., Gridley, T., and Li, E. 1999. The type II activin receptors are essential for egg cylinder growth, gastrulation and rostral head development in mice. Dev. Biol. 213: 157-169.
46. Tam, P.P. and Zhou, S.X. 1996. The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev. Biol. 178: 124-132.
47. Tanaka, S.S. and Matsui, Y. 2002. Developmentally regulated expression of mil-1 and mil-2, mouse interferon-induced transmembrane protein like genes, during formation and differentiation of primordial germ cells. Mech. Dev. 119 Suppl. 1: S261-S267.
48. Toyooka, Y., Tsunekawa, N., Akasu, R., and Noce, T. 2003. Embryonic stem cells can form germ cells in vitro. Proc. Natl. Acad. Sci. 100: 11457-11462.
49. Tremblay, K.D., Dunn, N.R., and Robertson, E.J. 2001. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 128: 3609-3621.
50. Watt, A.J., Jones, E.A., Ure, J.M., Peddie, D., Wilson, D.I., and Forrester, L.M. 2001. A gene trap integration provides an early in situ marker for hepatic specification of the foregut endoderm. Mech. Dev. 100: 205-215.
51. Winnier, G., Blessing, M., Labosky, P.A., and Hogan, B.L. 1995. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes & Dev. 9: 2105-2116.
52. Yeom, Y.I., Fuhrmann, G., Ovitt, C.E., Brehm, A., Ohbo, K., Gross, M., Hubner, K., and Schöler, H.R. 1996. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122: 881-894.
53. Yi, S.E., Daluiski, A., Pederson, R., Rosen, V., and Lyons, K.M. 2000. The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 127: 621-630.
54. Ying, Y. and Zhao, G.Q. 2001. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev. Biol. 232: 484-492.
55. Ying, Y., Liu, X.M., Marble, A., Lawson, K.A., and Zhao, G.Q. 2000. Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol. Endocrinol. 14: 1053-1063.
56. Ying, Y., Qi, X., and Zhao, G.Q. 2001. Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8b signaling pathways. Proc. Natl. Acad. Sci. 98: 7858-7862.
57. Yoshimizu, T., Obinata, M., and Matsui, Y. 2001. Stage-specific tissue and cell interactions play key roles in mouse germ cell specification. Development 128: 481-490.