The Drosophila gene Medea demonstrates the requirement for different classes of Smads in dpp signaling

Development

Volumn 125, Issue 8, 1998, Pages 1519-1528

  Das, Pradeep ^a   Maduzia, Lisa L ^a   Wang, Huang ^a   Finelli, Alyce L ^a,b   Cho, Seo Hee ^a   Smith, Marsha M ^a   Padgettt, Richard W ^a  

^a RUTGERS UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BMP; Drosophila; Mad; Medea; Pattern formation; Smad; TGF

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL NUCLEUS; DEVELOPMENTAL GENETICS; DROSOPHILA; EMBRYO; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

AMINO ACID SEQUENCE; ANIMALS; BODY PATTERNING; CELL LINE; CROSSES, GENETIC; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EVOLUTION, MOLECULAR; EYE; FEMALE; GENES, INSECT; GENES, TUMOR SUPPRESSOR; HUMANS; INSECT PROTEINS; MALE; MICROSCOPY, ELECTRON, SCANNING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA; WING;

ANIMALIA; ARACHNIDA; CAENORHABDITIS ELEGANS; HEXAPODA;

EID: 0031812292     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Affolter, M., Nellen, D., Nussbaumer, U. and Basler, K. (1994). Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF-β homologs during Drosophila embryogenesis. Development 120, 3105-3117.
2. Arora, K., Levine, M. S. and O'Connor, M. B. (1994). The screw gene encodes a ubiquitously expressed member of the TGF-β family required for specification of dorsal cell fates in the Drosophila embryo. Genes Dev. 8, 2588-2601.
3. Baker, J. C. and Harland, R. M. (1996). A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes Dev. 10, 1880-1889.
4. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
5. Brown, N. H. and Kafatos, F. C. (1988). Functional cDNA libraries from Drosophila embryos. J. Mol. Biol. 203, 425-437.
6. Brummel, T. J., Twombly, V., Marques, G., Wrana, J. L., Newfeld, S. J., Attisano, L., Massagué, J., O'Connor, M. B. and Gelbart, W. M. (1994). Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 78, 251-261.
7. Chanut, F. and Heberlein, U. (1997). Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124, 559-567.
8. Chen, X., Rubock, M. J. and Whitman, M. (1996). A transcriptional partner for MAD proteins in TGF-β signalling. Nature 383, 691-696.
9. Chen, X., Weisberg, E., Fridmacher, V., Watanabe, M., Naco, G. and Whitman, M. (1997). Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature 389, 85-89.
10. D1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras. Development 119, 1359-1369.
11. Derynck, R., Gelbart, W. M., Harland, R. M., Heldin, C. H., Kern, S. E., Massagué, J., Melton, D. A., Mlodzik, M., Padgett, R. W., Roberts, A. B., et al. (1996). Nomenclature: vertebrate mediators of TGFβ family signals. Cell 87, 173.
12. Doctor, J. S., Jackson, P. D., Rashka, K. E., Visalli, M. and Hoffmann, F. M. (1992). Sequence, biochemical characterization, and developmental expression of a new member of the TGF-beta superfamily in Drosophila melanogaster. Dev. Biol. 151, 491-505.
13. Hahn, S. A., Schutte, M., Hoque, A. T., Moskaluk, C. A., da Costa, L. T., Rozenblum, E., Weinstein, C. L., Fischer, A., Yeo, C. J., Hruban, R. H. and Kern, S. E. (1996). DPC4, A Candidate Tumor Suppressor Gene at Human Chromosome 18q21.1. Science 271, 350-353.
14. Hata, A., Lo, R. S., Wotton, D., Lagna, G. and Massagué, J. (1997). Mutations increasing autoinhibition inactivate tumour suppressors Smad2 and Smad4. Nature 388, 82-87.
15. Hayashi, H., Abdollah, S., Qiu, Y., Cai, J., Xu, Y. Y., Grinnell, B. W., Richardson, M. A., Topper, J. N., Gimbrone, M. A., Jr., Wrana, J. L. et al. (1997). The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell 89, 1165-1173.
16. Hogan, B. L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
17. Hoodless, P. A., Haerry, T., Abdollah, S., Stapteton, M., O'Connor, M. B., Attisano, L. and Wrana, J. L. (1996). MAORI, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500.
18. Inamura, T., Takase, M., Nishihara, A., Oeda, E., Hanai, J.-i., Kawabata, M. and Miyazano, K. (1997). Smad6 inhibits signalling by the TGF-β superfamily. Nature 389, 622-626.
19. Irish, V. F. and Gelbart, W. M. (1987). The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev. 1, 868-79.
20. Kim, J., Johnson, K., Chen, H. J., Carroll, S. and Laughon, A. (1997). Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature 388, 304-308.
21. Kingsley, D. M. (1994). The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8, 133-146.
22. Kretzschmar, M., Liu, F., Hata, A., Doody, J. and Massagué J. (1997). The TGF-β family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11, 984-995.
23. Lagna, G., Hata, A., Hemmati-Brivanlou, A. and Massagué J. (1996). Partnership between DPC4 and SMAD proteins in TGF-β signalling pathways. Nature 383, 832-836.
24. Letsou, A. et al. (1995). Drosophila Dpp signaling is mediated by the punt gene product: a dual ligand-binding type II receptor of the TGFβ receptor family. Cell 80, 899-908.
25. Liu, F., Hata, A., Baker, J. C., Doody, J., Cárcamo, J., Harland, R. M. and Massagué, J. (1996). A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381, 620-623.
26. Macias-Silva, M., Abdollah, S., Hoodless, P. A., Pirone, R., Attisano, L. and Wrana, J. L. (1996). MADR2 is a substrate of the TGFβ receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 87, 1215-1224.
27. Maduzia, L. L. and Padgett, R. W. (1997). Drosophila Mad, a Member of the Smad Family, Translocates to the Nucleus upon Stimulation of the dpp pathway. Biochem. Biophys. Res. Acta 238, 595-598.
28. Massagué, J. (1996). TGFβ signaling: receptors, transducers, and Mad proteins. Cell 85, 947-950.
29. Massagué, J., Cheifetz, S., Laiho, M., Ralph, D. A., Weis, F. M. and Zentella, A. (1992). Transforming growth factor-β. Cancer Surveys 12, 81103.
30. Nakao, A., Afrakhta, M., Moren, A., Nakayama, T., Christian, J. L., Heuchel, R., Itoh, S., Kawabata, M., Heldin, N.-E., Heldin, C.-H. et al. (1997). Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 289, 631-635.
31. Nellen, D., Affolter, M. and Basler, K. (1994). Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78, 225-237.
32. Newfeld, S. J., Mehra, A., Singer, M. A., Wrana, J. L., Attisano, L. and Gelbart, W. M. (1997). Mothers against dpp participates in a DPP/TGF-β rsponsive serine-threonine kinase signal transduction cascade. Development 124, 3167-3176.
33. Padgett, R. W., Das, P. and Krishna, S. (1998). TGFβ Signaling, Smads, and Tumor Suppressors. BioEssays (In press)
34. Padgett, R. W., St. Johnston, R. D. and Gelbart, W. M. (1987). A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family. Nature 325, 81-84.
35. Padgett, R. W. Wozney, J. M. and Gelbart, W. M. (1993). Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 90, 2905-2909.
36. Patterson, G. I., Koweek, A., Wong, A., Liu, Y. and Ruvkun, G. (1997). The DAF-3 Smad protein antagonizes TGF-β-related receptor signaling in the Caenorhabditis elegans dauer pathway. Genes Dev. 11, 2679-2690.
37. Penton, A. and Hoffmann, F. M. (1996). Decapentaplegic restricts the domain of wingless during Drosophila limb patterning. Nature 382, 162-164.
38. Poole, S. J., Kauvar, L. M., Drees, B. and Kornberg, T. (1985). The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell 40, 37-43.
39. Raftery, L. A., Twombly, V., Wharton, K. and Gelbart, W. M. (1995). Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics 139, 241-254.
40. Roberts, A. B., Anzano, M. A., Lamb, L. C., Smith, J. M. and Sporn, M. B. (1981). New class of transforming growth factors potentiated by epidermal growth factor: isolation from non-neoplastic tissues. Proc. Natl. Acad. Sci. USA 78, 339-43.
41. Ruberte, E., Marty, T., Nellen, D., Affolter, M. and Basler, K. (1995). An absolute requirement or both the type II and type I receptors, punt and thick veins, for dpp signaling in vivo. Cell 80, 889-897.
42. Savage, C., Das, P., Finelli, A. L., Townsend, S. R., Sun, C. Y., Baird, S. E. and Padgett, R. W. (1996). Caenorhabditis elegans genes sma-2, sma-3, and sma-4 define a conserved family of transforming growth factor β pathway components. Proc. Natl. Acad. Sci. USA 93, 790-794.
43. Segal, D. and Gelbart, W. M. (1985). Shortvein, a new component of the decapentaplegic gene complex in Drosophila melanogaster. Genetics 109, 119-143.
44. Sekelsky, J. J., Newfeld, S. J., Raftery, L. A., Chartoff, E. H. and Gelbart, W. M. ( 1995). Genetic characterization and cloning of Mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139, 1347-1358.
45. Shearn, A. and Garen, A. (1974). Genetic control of imaginal disc development in Drosophila. Proc. Natl. Acad. Sci. USA 71, 1393-7.
46. Shi, Y., Hata, A., Lo, R. S., Massagué, J. and Pavletich, N. P. (1997). A structural basis for mutational inactivation of the tumour suppressor Smad4. Nature 388, 87-93.
47. Spencer, F. A., Hoffmann, F. M. and Gelbart, W. M. (1982). Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28, 451-461.
48. Treisman, J. E. and Rubin, G. M. ( 1995). wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121, 3519-3527.
49. Tsuneizumi, K., Nakayama, T., Kamoshida, Y., Kornberg, T., Christian, J. and Tabata, T. (1997). Daughters against dpp modulates organizing activity in Drosophila wing development. Nature 389, 627-631.
50. Wharton, K. A., Thomsen, G. H. and Gelbart, W. M. (1991). Drosophila 60A gene, another transforming growth factor β family member, is closely related to human bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA 88, 9214-9218.
51. Wiersdorff, V., Lecuit, T., Cohen, S. M. and Mlodzik, M. (1996). Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development 122, 2153-2162.
52. Wieser, R., Wrana, J. L. and Massagué, J. (1995). GS domain mutations that constitutively activate TβR-I, the downstream signaling component in the TGF-β receptor complex. EMBO J. 14, 2199-2208.
53. Wozney, J. M., Rosen, V., Celeste, A. J., Mitsock, L. M. and Whitters, M. J. (1988). Novel regulators of bone formation: molecular clones and activities. Science 242, 1528-1531.
54. Wrana, J. L., Attisano, L., Wieser, R., Ventura, F. and Massagué, J. (1994). Mechanism of activation of the TGF-β receptor. Nature 370, 341-347.
55. Wu, R.-Y., Zhang, Y., Feng, X.-H. and Derynck, R. (1996). Heteromeric and Homomeric Interactions Correlate with Signaling Activity and Functional Cooperativity of Smad3 and Smad4/DPC4. Molec. Cell. Biol. 17, 2521-2528.
56. Xie, T., Finelli, A. L. and Padgett, R. W. (1994). The Drosophila saxophone Gene: A Serine-Threonine Kinase Receptor of the TGF-β Superfamily. Science 263, 1756-1759.
57. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
58. Yingling, J. M., Das, P., Savage, C., Zhang, M., Padgett, R. W. and Wang, X. F. (1996). Mammalian dwarfins are phosphorylated in response to transforming growth factor β and are implicated in control of cell growth. Proc. Natl. Acad. Sci. USA 93, 8940-8944.
59. Zhang, Y., Feng, X., We, R. and Derynck, R. (1996). Receptor-associated Mad homologues synergize as effectors of the TGF-β response. Nature 383, 168-172.