Specificity of TGFβ signaling is conferred by distinct type I receptors and their associated SMAD proteins in Caenorhabditis elegans

Development

Volumn 126, Issue 2, 1999, Pages 251-260

  Krishna, Srikant ^a   Maduzia, Lisa L ^a   Padgett, Richard W ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Caenorhabditis elegans; Sma 6; SMAD; TGF ; Type I receptor

Indexed keywords

PROTEIN; PROTEIN TYROSINE KINASE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; ACTIVIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; CAENORHABDITIS ELEGANS PROTEIN; CELL SURFACE RECEPTOR; DAF 4 PROTEIN, C ELEGANS; DAF-4 PROTEIN, C ELEGANS; GROWTH FACTOR RECEPTOR; HELMINTH PROTEIN; PROTEIN SERINE THREONINE KINASE; SMA 6 PROTEIN, C ELEGANS; SMA-6 PROTEIN, C ELEGANS; TGF BETA TYPE I RECEPTOR; TGF-BETA TYPE I RECEPTOR;

ANIMAL TISSUE; ARTICLE; BODY SIZE; CAENORHABDITIS ELEGANS; EMBRYO; EMBRYO PATTERN FORMATION; GENE MUTATION; MOLECULAR CLONING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TAIL; ALLELE; AMINO ACID SEQUENCE; ANIMAL; BODY CONSTITUTION; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MOLECULAR GENETICS; MORPHOGENESIS; SEQUENCE ALIGNMENT; TRANSGENIC ANIMAL;

ACTIVIN RECEPTORS, TYPE I; ALLELES; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY CONSTITUTION; BODY PATTERNING; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HELMINTH PROTEINS; MALE; MOLECULAR SEQUENCE DATA; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RECEPTORS, GROWTH FACTOR; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; TAIL; TRANSFORMING GROWTH FACTOR BETA;

EID: 0032589736     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. 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.
2. Attisano, L. and Wrana, J. L. (1998). Mads and Smads in TGFβ signalling. Curr. Opin. Cell Biol. 10, 188-194.
3. Baird, S. E., Fitch, D. H., Kassem, I. A. and Emmons, S. W. (1991). Pattern formation in the nematode epidermis: determination of the arrangement of peripheral sense organs in the C. elegans male tail. Development 113, 515-526.
4. 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.
5. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
6. Brunner, D., Oellers, N., Szabad, J., Biggs, W. H., 3rd, Zipursky, S. L. and Hafen, E. (1994). A gain-of-function mutation in Drosophila MAP kinase activates multiple receptor tyrosine kinase signaling pathways. Cell 76, 875-888.
7. Chen, X., Rubock, M. J. and Whitman, M. (1996). A transcriptional partner for MAD proteins in TGF-β signalling, Nature 383, 691-696.
8. 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.
9. Chen, Y., Riese, M. J., Killinger, M. A. and Hoffmann, F. M. (1998). A genetic screen for modifiers of Drosophila decapentaplegic signaling identities mutations in punt. Mothers against dpp and the BMP-7 homologue, 60A. Development 125, 1759-1768.
10. Childs, S. R. and O'Connor, M. B. (1994). Two domains of the tolloid protein contribute to its unusual genetic interaction with decapentaplegic. Developmental Biology 162, 209-220.
11. Chisholm, A. (1991). Control of cell fate in the tail region of C. elegans by the gene egl-5. Development 111, 921-932.
12. Chow, K. L. and Emmons, S. W. (1994). HOM-C/Hox genes and four interacting loci determine the morphogenetic properties of single cells in the nematode male tail. Development 120, 2579-2592.
13. Colavita, A., Krishna, S., Zheng, H., Padgett, R. W. and Culotti, J. G. (1998). Pioneer axon guidance by UNC-129, a C. elegans TGF-β. Science 281, 706-709.
14. 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., Smith, J., Thomsen, G. H., Vogelstein, B. and Wang, X. F. (1996). Nomenclature: verlebrate mediators of TGFβ family signals. Cell 87, 173.
15. Eppert, K., Scherer, S. W., Ozcelik, H., Pirone, R., Hoodless, P., Kim, H., Tsui, L. C., Bapat, B., Gallinger, S., Andrulis, I. L., Thomsen, G. H., Wrana, J. L. and Attisano, L. (1996). MADR2 maps to 18q21 and encodes a TGFβ-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86, 543-552.
16. Estevez, M., Atlisano, L., Wrana, J. L., Albert, P. S., Massagué, J. and Riddle, D. L. (1993). The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development. Nature 365, 644-649.
17. Feng, X. H., Zhang, Y., Wu, R. Y. and Derynck, R. (1998). The tumor suppressor Smad4/DPC4 and transcriptional adaptor CBP/p300 are coactivators for Smad3 in TGF-β-induced transcriptional activation. Genes Dev. 12, 2153-2163.
18. Finelli, A. L., Bossie, C. A., Xie, T. and Padgett, R. W. (1994). Mutational analysis of the Drosophila tolloid gene, a human BMP-1 homolog. Development 120, 861-870.
19. Fire, A. (1992). Histochemical techniques for locating Escherichia coli betagalactosidase activity in transgenic organisms. Genet. Anal. Tech. Appl. 9, 151-158.
20. Fire, A., Harrison, S. W. and Dixon, D. (1990). A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 93, 189-198.
21. Georgi, L. L., Albert, P. S. and Riddle, D. L. (1990). daf-1, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell 61, 635-645.
22. 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, 350-351.
23. Hata, A., Lagna, G., Massagué, J. and Hemmati-Brivanlou, A. (1998). Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev. 12, 186-197.
24. 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. and Falb, D. (1997). The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell 89, 1165-1173.
25. Heldin, C. H., Miyazono, K. and ten Dijke, P. (1997). TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471.
26. Hoodless, P. A., Haerry, T., Abdollah, S., Staplelon, 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.
27. Imamura, T., Takase, M., Nishihara, A., Oeda, E., Hanai, J., Kawabata, M. and Miyazono, K. (1997). Smad6 inhibits signalling by the TGF-β superfamily. Nature 389, 622-626.
28. Irish, V. F. and Gelbart, W. M. (1987). The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev. 1, 868-879.
29. Janknecht, R., Wells, N. J. and Hunter, T. (1998). TGF-β-stimulated cooperation of Smad proteins with the coactivators CBP/p300. Genes Dev. 12, 2114-2119.
30. Khalsa, O., Yoon, J. W., Torres-Schumann, S. and Wharton, K. A. (1998). TGF-β/BMP superfamily members. Gbb-60A and Dpp, cooperate to provide pattern information and establish cell identity in the Drosophila wing. Development 125, 2723-2734.
31. 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.
32. Kipreos, E. T., Lander, L. E., Wing, J. P., He, W. W. and Hedgecock, E. M. (1996). cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85, 829-839.
33. 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.
34. Lagna, G., Hata, A., Hemmati-Brivanlou, A. and Massagué, J. (1996). Partnership between DPC4 and SMAD proteins in TGF-beta signalling pathways. Nature 383, 832-836.
35. 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.
36. 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, 3479-386.
37. Macías-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.
38. Madhani, H. D. and Fink, G. R. (1998). The riddle of MAP kinase signaling specificity. Trends Genet. 14, 151-155.
39. Massagué, J. (1998). TGFβ Signal Transduction. Annu. Rev. Biochem. 67, 753-791.
40. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-70.
41. Miyazono, K., Ten Dijke, P., Ichijo, H. and Heldin, C. H. (1994) Receptors for transforming growth factor-beta. Adv. Immunol. 55, 181-220.
42. Nakao, A., Afrakhta, M., Moren, A., Nakayama, T., Christian, J. L., Heuchel, R., Itoh, S., Kawabata, M., Heldin, N.-E., Heldin, C.-H. and Dijke, P. t. (1997). Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 289, 631-635.
43. 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.
44. Padgett, R. W., Finelli, A. L., Savage, C., Xie, T. and Cho, S.-H. (1997). The tolloid-like Genes in Invertebrates. In The Astacins - Structure and Function of a New Protein Family (ed. R. Zwilling and W. Stöcker). Hamburg: Verlag DR Kovac.
45. Padgett, R. W., Das, P. and Krishna, S. (1998). TGFβ signaling, Smads, and tumor suppressors. BioEssays 20, 382-390.
46. Panganiban, G. E., Reuter, R., Scott, M. P. and Hoffmann, F. M. (1990). A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. Development 110, 1041-1050.
47. 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.
48. Ren, P., Lim, C. S., Johnsen, R., Albert, P. S., Pilgrim, D. and Riddle, D. L. (1996). Control of C. elegans larval development by neuronal expression of a TGF-β homolog. Science 274, 1389-1391.
49. Riddle, D. L., Swanson, M. M. and Albert, P. S. (1981). Interacting genes in nematode dauer larva formation. Nature 290, 668-671.
50. 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.
51. 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.
52. Shimell, M. J., Ferguson, E. L., Childs, S. R. and O'Connor, M. B. (1991). The Drosophila dorsal-ventral patterning gene tolloid is related to human bone morphogenetic protein I. Cell 67, 469-481.
53. Suzuki, Y., Yandell, M. D., Roy, P. J., Krishna, S., Savage-Dunn, C., Ross, R. M., Padgett, R. W. and Wood, W. B. (1999). A BMP homolog acts as a dose-dependent regulator of body size and male tail patterning in Caenorhabditis elegans. Development 126, 241-250.
54. Szüts, D., Eresh, S. and Bienz, M. (1998). Functional intertwining of Dpp and EGFR signaling during Drosophila endoderm induction. Genes Dev. 12, 2022-2035.
55. 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.
56. Ventura, F., Doody, J., Liu, F., Wrana, J. L. and Massagué, J. (1994). Reconstitution and transphosphorylation of TGF-β receptor complexes. EMBO J. 13, 5581-5589.
57. Weis-Garcia, F. and Massagué, J. (1996). Complementation between kinase-defective and activation-defective TGF-β receptors reveals a novel form of receptor cooperativity essential for signaling. EMBO J. 15, 276-289.
58. Wieser, R., Wrana, J. L. and Massagué, J. (1995). GS domain mutations that constitutively activate TβR-1, the downstream signaling component in the TGF-β receptor complex. EMBO J. 14, 2199-2208.
59. Wittmann, C., Bossinger, O., Goldstein, B., Fleischmann, M., Kohler, R., Brunschwig, K., Tobler, H. and Muller, F. (1997). The expression of the C. elegans labial-like Hox gene ceh-13 during early embryogenesis relies on cell fate and on anteroposterior cell polarity. Development 124, 4193-4200.
60. 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.
61. 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.
62. Wu, R. Y., Zhang, Y., Feng, X. H. and Derynck, R. (1997). Heteromeric and homomeric interactions correlate with signaling activity and functional cooperativity of Smad3 and Smad4/DPC4. Mol. Cell Biol. 17, 2521-2528.
63. 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.
64. Yamashita, H., ten Dijke, P., Franzen, P., Miyazono, K. and Heldin, C. H. (1994). Formation of hetero-oligomeric complexes of type I and type II receptors for transforming growth factor-beta. J. Biol. Chem. 269, 20172-20178.
65. 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.
66. Zou, H., Wieser, R., Massagué, J. and Niswander, L. (1997). Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11, 2191-2203.