The type I serine/threonine kinase receptor ActRIA (ALK2) is required for gastrulation of the mouse embryo

Development

Volumn 126, Issue 11, 1999, Pages 2551-2561

  Gu, Zhenyu ^a,b   Reynolds, Ellen M ^a   Song, Jihwan ^a,b   Lei, Hong ^a   Feijen, Alie ^c   Yu, Lian ^a   He, Weiwu ^a   MacLaughlin, David T ^a   Van Den Eijnden Van Raaij, Janny ^c   Donahoe, Patricia K ^a   Li, En ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HUBRECHT INSTITUTE   (Netherlands)

Author keywords

Activin; BMP; Gastrulation; Gene targeting; Mesoderm formation; Mouse; Serine threonine kinase receptor

Indexed keywords

CELL RECEPTOR; PROTEIN SERINE THREONINE KINASE; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL TISSUE; ARTICLE; BLASTOCYST; CHIMERA; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; GASTRULATION; GENE MUTATION; GENE TARGETING; GERM LAYER; HOMOZYGOTE; MESODERM; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR GENE; SOMITE;

ACTIVIN RECEPTORS, TYPE I; ANIMALS; CELL DIFFERENTIATION; CHIMERA; DNA-BINDING PROTEINS; EMBRYO; ENDODERM; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; GENES, LETHAL; HEPATOCYTE NUCLEAR FACTOR 4; MESODERM; MICE; MICROINJECTIONS; MUTATION; PHENOTYPE; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, GROWTH FACTOR; SIGNAL TRANSDUCTION; STEM CELLS; TRANSCRIPTION FACTORS;

ANIMALIA; MAMMALIA;

EID: 0032992759     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Albano, R. M., Arkell, R., Beddington, R. S. P. and Smith, J. C. (1994). Expression of inhibin subunits and follistatin during postimplantation mouse development: decidual expression of activin and expression of follistatin in primitive streak, somites and hindbrain. Development 120, 803-813.
2. Armes, N. A. and Smith, J. C. (1997). The ALK-2 and ALK-4 activin receptors transduce distinct mesoderm-inducing signals during early Xenopus development but do not co-operate to establish thresholds. Development 124, 3797-3804.
3. Attisano, L., Carcamo, J., Ventura, F., Weis, F. M., Massagué, J. and Wrana, J. L. (1993). Identification of human activin and TGF beta type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75, 671-680.
4. Beddington, R. S. and Robertson, E. J. (1989). An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 105, 733-737.
5. Chang, C., Wilson, P. A., Mathews, L. S. and Hemmati-Brivanlou, A. (1997). A Xenopus type I activin receptor mediates mesodermal but not neural specification during embryogenesis. Development 124, 827-837.
6. Chen, W. S., Manova, K., Weinstein, D. C., Duncan, S. A., Plump, A. S., Prezioso, V. R., Bachvarova, R. F. and Darnell, J. E., Jr. (1994). Disruption of the HNF-4 gene, expressed in visceral endoderm, leads to cell death in embryonic ectoderm and impaired gastrulation of mouse embryos. Genes Dev. 8, 2466-2477.
7. Conlon, F. L., Lyons, K. M., Takaesu, N., Barth, K. S., Kispert, A., Herrmann, B. and 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.
8. Coucouvanis, E. and Martin, G. R. (1995). Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83, 279-287.
9. Duncan, S. A., Manova, K., Chen, W. S., Hoodless, P., Weinstein, D. C., Bachvarova, R. F. and Darnell, J. E., Jr. (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 primary endoderm in the implanting blastocyst. Proc. Natl. Acad. Sci. USA 91, 7598-7602.
10. Duncan, S. A., Nagy, A. and Chan, W. (1997). Murine gastrulation requires HNF-4 regulated gene expression in the visceral endoderm: tetraploid rescue of Hnf-4(-/-) embryos. Development 124, 279-287.
11. Feijen, A., Goumans, M. J. and van den Eijnden-van Raaij, A. J. M. (1994). Expression of activin subunits, activin receptors and follistalin in postimplantation mouse embryos suggests specific developmental functions for different activins. Development 120, 3621-3637.
12. Friedrich, G. and Soriano, P. (1991). Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mouse. Genes Dev. 5, 1513-1523.
13. Green, J. B. and Smith, J. C. (1990). Graded changes in dose of a Xenopus activin A homologue elicit slepwise transitions in embryonic cell fate. Nature 347, 391-394.
14. Green, J. B., New, H. V. and Smith, J. C. (1992). Responses of embryonic Xenopus cells to activin and FGF are separated by multiple dose thresholds and correspond to distinct axes of the mesoderm. Cell 71, 731-739.
15. Gu, Z., Nomura, M., Simpson, B. B., Lei, H., Feijen, A., van den Eijndenvan Raaij, J. E., Donahoe, P. K. and 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.
16. Harland, R. M. (1994). The transforming growth factor beta family and induction of the vertebrate mesoderm: bone morphogenetic proteins are ventral inducers. Proc. Natl. Acad. Sci. USA 91, 10243-10246.
17. He, W. W., Gustafson, M. L., Hirobe, S. and Donahoe, P. K. (1993). Developmental expression of four novel serine/threonine kinase receptors homologous to the activin/transforming growth factor-beta type II receptor family. Dev. Dyn. 196, 133-142.
18. Hogan, B., Beddington, R., Costantini, F. and Lacy, E. (1994). Summary of mouse development. In Manipulating the Mouse Embryo, pp. 19-113. Cold Spring Harbor Laboratory Press.
19. Jones, C. M., Kuehn, M. R., Hogan, B. L., Smith, J. C. and Wright, C. V. (1995). Nodal-related signals induce axial mesoderm and dorsalize mesoderm during gastrulation. Development 121, 3651-3662.
20. Jones, C.M., Lyons, K. M. and Hogan, B. L. M. (1991). Involvement of bone morphogenetic protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111, 531-542.
21. Kaufman, M. H. (1992). The Atlas of Mouse Development. San Diego: Academic Press.
22. Kessler, D. S. and Melton, D. A. (1995). Induction of dorsal mesoderm by soluble, mature Vg1 protein. Development 121, 2155-2164.
23. Lawson, K. A., Meneses, J. J. and Pedersen, R. A. (1991). Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113, 891-911.
24. Li, E., Bestor, T. H. and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926.
25. Massagué, J. (1998). TGF-beta signal transduction. Annu. Rev. Biochem. 67, 753-91
26. Matzuk, M. M., Kumar, T. R., Vassalli, A., Bickenbach, J. R., Roop, D. R., Jaenisch, R. and Bradley, A. (1995). Functional analysis of activins during mammalian development. Nature 374, 354-356.
27. Mishina, V., 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.
28. Nagy, A. and Rossant, J. (1993). Production of completely ES cell-derived fetuses. In Gene Targeting, (ed. A. L. Joyner). pp. 147-180. Oxford: IRL Press.
29. Nomura, M. and Li, E. (1998). Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature 393, 786-790.
30. Robertson, E. J. (1987). Embryo-derived stem cell lines. In Terotocarcinomas and Embryonic Stem Cells: A Practical Approach, (ed. E. J. Robertson). pp. 71-112. Oxford: IRL Press.
31. Roelen, B. A. J., Lin, H. Y., Knezevic, V., Freund, E. and Mummery, C. (1994). Expression of TGF-βs and their receptors during implantation and oganogenesis of the mouse embryo. Dev. Biol. 166, 716-728.
32. Schmitt, J., Mielke, R. and Schrewe, H. (1995). Genomic organization of a mouse type I activin receptor. Biochem. Biophys. Res. Commun. 213, 211-217.
33. Sirard, C., de la Pompa, J. L., Elia, A., Itie, A., Mirtsos, C., Cheung, A., Hahn, S., Wakeham, A., Schwartz, L., Kern, S. E., Rossant, J. and Mak, T. W. (1998). The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev. 12, 107-119.
34. Slack, J. M. (1994). Inducing factors in Xenopus early embryos. Curr. Biol. 4, 116-126.
35. Smith, J. C. (1993). Mesoderm-induction factors in early vertebrate development. EMBO J. 12, 4463-4470.
36. Tam, P. P. and Behringer, R. R. (1997). Mouse gastrulation: the formation of a mammalian body plan. Mech. Dev. 68, 3-25.
37. ten Dijke, P., Ichijo, H., Franzen, P., Schulz, P., Saras, J., Toyoshima, H., Heldin, C. H. and Miyazono, K. (1993). Activin receptor-like kinases: a novel subclass of cell-surface receptors with predicted serine/threonine kinase activity. Oncogene 8, 2879-2887.
38. ten Dijke, P., Yamashita, H., Ichijo, H., Franzen, P., Laiho, M., Miyazono, K. and Heldin, C. H. (1994). Characterization of type I receptors for transforming growth factor-beta and activin. Science 264, 101-104.
39. Teixeira, J., He, W. W., Shah, P. C., Morikawa, N., Lee, M. M., Catlin, E. A., Hudson, P. L., Wing, J., Maclaughlin, D. T. and Donahoe, P. K. (1996). Developmental expression of a candidate mullerian inhibiting substance type II receptor. Endocrinology 137, 160-165.
40. Thomas, P. and Beddington, R. S. P. (1996). Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Current Biol. 6, 1487-1496.
41. Verschueren, K., Dewulf, N., Goumans, M., Lonnoy, O., Feijen, A., Grimsby, S., Spiegle, K. V., Dijke, P. t., Moren, A., Vanscheeuwijck, P., Heldin, C., Miyazono, K., Mummery, C., Raaij, J. V. D. E.-V. and Huylebroeck, D. (1995). Expression of type I and type IB receptors for activin in midgestation mouse embryos suggests distinct functions in organogenesis. Mech. Dev. 52, 109-123.
42. Waldrip, W. R., Bikoff, E. K., Hoodless, P. A., Wrana, J. L. and Robertson, E. J. (1998). Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell 92, 797-808.
43. Weinstein, M., Yang, X., Li, C., Xu, X., Gotay, J. and Deng, C. X. (1998). Failure of egg cylinder elongation and mesoderm induction in mouse embryos lacking the tumor suppressor smad2. Proc. Natl. Acad. Sci. USA 95, 9378-9383.
44. Wilkinson, D. G. (1992). Whole Mount In Situ Hybridization of Vertebrate Embryos. Oxford, UK: IRL Press at Oxford University Press.
45. Wilkinson, D. G., Bhatt, S. and Herrmann, B. G. (1990). Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343, 657-659.
46. 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.
47. Yang, X., Li, C., Xu, X. and Deng, C. (1998). The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc. Natl. Acad. Sci. USA 95, 3667-3672.
48. Zhou, X., Sasaki, H., Lowe, L., Hogan, B. L. and Kuehn, M. R. (1993). Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature 361, 543-547.