Differential requirements for Smad4 in TGFβ-dependent patterning of the early mouse embryo

Development

Volumn 131, Issue 15, 2004, Pages 3501-3512

  Chu, Gerald C ^a,b   Dunn, N Ray ^a   Anderson, Dorian C ^a   Oxburgh, Leif ^a   Robertson, Elizabeth J ^a  

^a HARVARD UNIVERSITY   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Anterior primitive streak; Mesoderm patterning; Mouse; Smad4; TGF

Indexed keywords

BONE MORPHOGENETIC PROTEIN; LIGAND; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; ENDODERM; FETUS MEMBRANE; GASTRULATION; GENE INACTIVATION; GENETIC ANALYSIS; IN SITU HYBRIDIZATION; MESODERM; MOUSE; NONHUMAN; NOTOCHORD; PHENOTYPE; PRIMITIVE STREAK; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOMITE;

ALLANTOIS; ALLELES; ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; CELL LINEAGE; DNA-BINDING PROTEINS; EMBRYO; EMBRYONIC AND FETAL DEVELOPMENT; ENDODERM; GERM CELLS; HEART; IN SITU HYBRIDIZATION; MESODERM; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MORPHOGENESIS; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; MAMMALIA;

EID: 4444249320     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01248     Document Type: Article

References (63)

1. Attisano, L. and Wrana, J. L. (2000). Smads as transcriptional co-modulators. Curr. Opin. Cell Biol. 12, 235-243.
2. Barnes, J. D., Crosby, J. L., Jones, C. M., Wright, C. V. and Hogan, B. L. (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.
3. Brennan, J., Lu, C. C., Norris, D. P., Rodriguez, T. A., Beddington, R. S. and Robertson, E. J. (2001). Nodal signalling in the epiblast patterns the early mouse embryo. Nature 411, 965-969.
4. Das, P., Maduzia, L. L., Wang, H., Finelli, A. L., Cho, S. H., Smith, M. M. and Padgett, R. W. (1998). The Drosophila gene Medea demonstrates the requirement for different classes of Smads in dpp signaling. Development 125, 1519-1528.
5. de Caestecker, M. P., Hemmati, P., Larisch-Bloch, S., Ajmera, R., Roberts, A. B. and Lechleider, R. J. (1997). Characterization of functional domains within Smad4/DPC4. J. Biol. Chem. 272, 13690-13696.
6. Derynck, R. and Zhang, Y. E. (2003). Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425, 577-584.
7. Dufort, D., Schwartz, L., Harpal, K. and Rossant, J. (1998). The transcription factor HNF3beta is required in visceral endoderm for normal primitive streak morphogenesis. Development 125, 3015-3025.
8. Dunn, N. R., Vincent, S. D., Oxburgh, L., Robertson, E. J. and Bikoff, E. K. (2004). Combinatorial activities of Smad2 and Smad3 regulate mesoderm formation and patterning in the mouse embryo. Development 131, 1717-1728.
9. Gu, Z., Nomura, M., Simpson, B. B., Lei, H., Feijen, A., van den Eijnden-van Raaij, J., 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.
10. Hallonet, M., Kaestner, K. H., Martin-Parras, L., Sasaki, H., Betz, U. A. and Ang, S. L. (2002). Maintenance of the specification of the anterior definitive endoderm and forebrain depends on the axial mesendoderm: a study using HNF3beta/Foxa2 conditional mutants. Dev. Biol. 243, 20-33.
11. Hayashi, S. and McMahon, A. P. (2002). Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244, 305-318.
12. Hayashi, K., Kobayashi, T., Umino, T., Goitsuka, R., Matsui, Y. and Kitamura, D. (2002a). SMAD1 signaling is critical for initial commitment of germ cell lineage from mouse epiblast. Mech. Dev. 118, 99-109.
13. Hayashi, S., Lewis, P., Pevny, L. and McMahon, A. P. (2002b). Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Gene Expr. Patterns 2, 93-97.
14. Hoodless, P. A., Haerry, T., Abdollah, S., Stapleton, M., O'Connor, M. B., Attisano, L. and Wrana, J. L. (1996). MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500.
15. Hoodless, P. A., Pye, M., Chazaud, C., Labbe, E., Attisano, L., Rossant, J. and Wrana, J. L. (2001). FoxH1 (Fast) functions to specify the anterior primitive streak in the mouse. Genes Dev. 15, 1257-1271.
16. Hudson, J. B., Podos, S. D., Keith, K., Simpson, S. L. and Ferguson, E. L. (1998). The Drosophila Medea gene is required downstream of dpp and encodes a functional homolog of human Smad4. Development 125, 1407-1420.
17. Labbé, E., Silvestri, C., Hoodless, P. A., Wrana, J. L. and Attisano, L. (1998). Smad2 and Smad3 positively and negatively regulate TGF beta-dependent transcription through the forkhead DNA-binding protein FAST2. Mol. Cell 2, 109-120.
18. Lagna, G., Hata, A., Hemmati-Brivaniou, A. and Massague, J. (1996). Partnership between DPC4 and SMAD proteins in TGF-beta signalling pathways. Nature 383, 832-836.
19. Lawson, K. A. and Hage, W. J. (1994). Clonal analysis of the origin of primordial germ cells in the mouse. CIBA Found. Symp. 182, 68-84.
20. 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.
21. Lawson, K. A., Dunn, N. R., Roelen, B. A., Zeinstra, L. M., Davis, A. M., Wright, C. V. E., Korving, J. P. and Hogan, B. L. M. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424-436.
22. Li, W., Qiao, W., Chen, L., Xu, X., Yang, X., Li, D., Li, C., Brodie, S. G., Meguid, M. M., Hennighausen, L. et al. (2003). Squamous cell carcinoma and mammary abscess formation through squamous metaplasia in Smad4/Dpc4 conditional knockout mice. Development 130, 6143-6153.
23. Lien, C. L., McAnally, J., Richardson, J. A. and Olson, E. N. (2002). Cardiac-specific activity of an Nkx2-5 enhancer requires an evolutionarily conserved Smad binding site. Dev. Biol. 244, 257-266.
24. Loebel, D. A., Watson, C. M., De Young, R. A. and Tam, P. P. (2003). Lineage choice and differentiation in mouse embryos and embryonic stem cells. Dev. Biol. 264, 1-14.
25. Lowe, L. A., Yamada, S. and Kuehn, M. R. (2001). Genetic dissection of nodal function in patterning the mouse embryo. Development 128, 1831-1843.
26. Lu, C. C., Brennan, J. and Robertson, E. J. (2001). From fertilization to gastrulation: axis formation in the mouse embryo. Curr. Opin. Genet. Dev. 11, 384-392.
27. Macías-Silva, M., Abdollah, S., Hoodless, P. A., Pirone, R., Attisano, L. and Wrana, J. L. (1996). MADR2 is a substrate of the TGFbeta receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 87, 1215-1224.
28. Martinez Barbera, J. P., Clements, M., Thomas, P., Rodriguez, T., Meloy, D., Kioussis, D. and Beddington, R. S. P. (2000). The homeobox gene Hex is required in definitive endodermal tissues for normal forebrain, liver and thyroid formation. Development 127, 2433-2445.
29. Massagué, J. (1998). TGF-beta signal transduction. Annu. Rev. Biochem. 67, 753-791.
30. Massagué, J., Blain, S. W. and Lo, R. S. (2000). TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103, 295-309.
31. McLaren, A. (2003). Primordial germ cells in the mouse. Dev. Biol. 262, 1-15.
32. Moustakas, A., Souchelnytskyi, S. and Heldin, C. H. (2001). Smad regulation in TGF-beta signal transduction. J. Cell Sci. 114, 4359-4369.
33. Nagy, A., Gertsenstein, M., Vintersten, K. and Behringer, R. (2003). Manipulating the Mouse Embryo: A Laboratory Manual. New York, NY: Cold Spring Harbor Laboratory Press.
34. Nishizaki, Y., Shimazu, K., Kondoh, H. and Sasaki, H. (2001). Identification of essential sequence motifs in the node/notochord enhancer of Foxa2 (Hnf3beta) gene that are conserved across vertebrate species. Mech. Dev. 102, 57-66.
35. Norris, D. P., Brennan, J., Bikoff, E. K. and Robertson, E. J. (2002). The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development 129, 3455-3468.
36. O'Gorman, S., Dagenais, N. A., Qian, M. and Marchuk, Y. (1997). Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc. Natl. Acad. Sci. USA 94, 14602-14607.
37. Pearce, J. J. and Evans, M. J. (1999). Mml, a mouse Mix-like gene expressed in the primitive streak. Mech. Dev. 87, 189-192.
38. Pierreux, C. E., Nicolas, F. J. and Hill, C. S. (2000). Transforming growth factor beta-independent shuttling of Smad4 between the cytoplasm and nucleus. Mol. Cell. Biol. 20, 9041-9054.
39. Robertson, E. J. (1987). Embryo-derived stem cell lines. In Teratocarcinoma and Embryonic Stem Cells: A Practical Approach (ed. E. J. Robertson), pp. 71-112. Oxford, UK: IRL Press.
40. Rodriguez, T. A., Casey, E. S., Harland, R. M., Smith, J. C. and Beddington, R. S. (2001). Distinct enhancer elements control Hex expression during gastrulation and early organogenesis. Dev. Biol. 234, 304-316.
41. Schier, A. F. (2003). Nodal signaling in vertebrate development. Annu. Rev. Cell Dev. Biol. 19, 589-621.
42. Schlange, T., Andree, B., Arnold, H. H. and Brand, T. (2000). BMP2 is required for early heart development during a distinct time period. Mech. Dev. 91, 259-270.
43. Schultheiss, T. M., Burch, J. B. and Lassar, A. B. (1997). A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 11, 451-462.
44. Sirard, C., de la Pompa, J. L., Elia, A., Itie, A., Mirtsos, C., Cheung, A., Hahn, S., Wakeham, A., Schwartz, L., Kern, S. E. et al. (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.
45. Sirard, C., Kim, S., Mirtsos, C., Tadich, P., Hoodless, P. A., Itie, A., Maxson, R., Wrana, J. L. and Mak, T. W. (2000). Targeted disruption in murine cells reveals variable requirement for Smad4 in transforming growth factor beta-related signaling. J. Biol. Chem. 275, 2063-2070.
46. 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.
47. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
48. Takaku, K., Miyoshi, H., Matsunaga, A., Oshima, M., Sasaki, N. and Taketo, M. M. (1999). Gastric and duodenal polyps in Smad4 (Dpc4) knockout mice. Cancer Res. 59, 6113-6117.
49. Thomas, P. Q., Brown, A. and Beddington, R. S. P. (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.
50. Tremblay, K. D., Hoodless, P. A., Bikoff, E. K. and Robertson, E. J. (2000). Formation of the definitive endoderm in mouse is a Smad2-dependent process. Development 127, 3079-3090.
51. Vincent, S. D., Dunn, N. R., Hayashi, S., Norris, D. P. and Robertson, E. J. (2003). Cell fate decisions within the mouse organizer are governed by graded Nodal signals. Genes Dev. 17, 1646-1662.
52. Wakefield, L. M. and Roberts, A. B. (2002). TGF-beta signaling: positive and negative effects on tumorigenesis. Curr. Opin. Genet. Dev. 12, 22-29.
53. Watanabe, M., Rebbert, M. L., Andreazzoli, M., Takahashi, N., Toyama, R., Zimmerman, S., Whitman, M. and Dawid, I. B. (2002). Regulation of the Lim-1 gene is mediated through conserved FAST-1/FoxH1 sites in the first intron. Dev. Dyn. 225, 448-456.
54. Whitman, M. (2001). Nodal signaling in early vertebrate embryos: themes and variations. Dev. Cell 1, 605-617.
55. Wisotzkey, R. G., Mehra, A., Sutherland, D. J., Dobens, L. L., Liu, X., Dohrmann, C., Attisano, L. and Raftery, L. A. (1998). Medea is a Drosophila Smad4 homolog that is differentially required to potentiate DPP responses. Development 125, 1433-1445.
56. Wrana, J. L., Attisano, L., Carcamo, J., Zentella, A., Doody, J., Laiho, M., Wang, X. F. and Massague, J. (1992). TGF beta signals through a heteromeric protein kinase receptor complex. Cell 71, 1003-1014.
57. Yamamoto, M., Meno, C., Sakai, Y., Shiratori, H., Mochida, K., Ikawa, Y., Saijoh, Y. and Hamada, H. (2001). The transcription factor FoxH1 (FAST) mediates nodal signaling during anterior-posterior patterning and node formation in the mouse. Genes Dev. 15, 1242-1256.
58. 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.
59. Yeo, C. Y., Chen, X. and Whitman, M. (1999). The role of FAST-1 and Smads in transcriptional regulation by activin during early Xenopus embryogenesis. J. Biol. Chem. 274, 26584-26590.
60. Zaffran, S., Xu, X., Lo, P. C., Lee, H. H. and Frasch, M. (2002). Cardiogenesis in the Drosophila model: control mechanisms during early induction and diversification of cardiac progenitors. Cold Spring Harb. Symp. Quant. Biol. 67, 1-12.
61. Zhang, Y., Musci, T. and Derynck, R. (1997). The tumor suppressor Smad4/DPC 4 as a central mediator of Smad function. Curr. Biol. 7, 270-276.
62. Zhao, G. Q. (2003). Consequences of knocking out BMP signaling in the mouse. Genesis 35, 43-56.
63. Zhou, Y. X., Zhao, M., Li, D., Shimazu, K., Sakata, K., Deng, C. X. and Lu, B. (2003). Cerebellar deficits and hyperactivity in mice lacking Smad4. J. Biol. Chem. 278, 42313-42320.