DNA-binding domain mutations in SMAD genes yield dominant-negative proteins or a neomorphic protein that can activate WG target genes in Drosophila

Development

Volumn 132, Issue 21, 2005, Pages 4883-4894

  Takaesu, Norma T ^a   Herbig, Eric ^a,c   Zhitomersky, David ^b   O'Connor, Michael B ^b   Newfeld, Stuart J ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Colon cancer; Drosophila; Pancreatic cancer; SMAD genes; TGF ; Tumorigenesis

Indexed keywords

PROTEIN WG; SMAD PROTEIN; SMAD4 PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ALLELE; ARTICLE; CARCINOGENESIS; COLON POLYPOSIS; CONTROLLED STUDY; DNA BINDING; DROSOPHILA; EMBRYO; GENE EXPRESSION; HETEROZYGOSITY; HUMAN; MISSENSE MUTATION; MUTANT; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN DOMAIN; WILD TYPE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; HUMANS; MUTATION; NEOPLASMS; PROTO-ONCOGENE PROTEINS; SMAD PROTEINS; SMAD4 PROTEIN; WING;

EID: 28044455428     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02048     Document Type: Article

References (68)

1. Adamson, A. and Shearn, A. (1996). Molecular genetic analysis of ash2, a member of the Trithorax group required for imaginal disc pattern formation. Genetics 144, 621-633.
2. Aigouy, B., Van de Bor, V., Boeglin, M. and Giangrande, A. (2004). Time-lapse and cell ablation reveal the role of cell interactions in fly glia migration and proliferation. Development 131, 5127-5138.
3. Akong, K., Grevengoed, E., Price, M., McCartney, B., Hayden, M., DeNofrio, J. and Peifer M. (2002). Drosophila APC2 and APC1 play overlapping roles in Wingless signaling in the embryo and imaginal discs. Dev. Biol. 250, 91-100.
4. Alexandre, C., Lecourtois, M. and Vincent, J.-P. (1999). Wingless and Hedgehog pattern Drosophila denticle belts by regulating the production of short-range signals. Development 126, 5689-5698.
5. Barnard, J., Lyons, R. and Moses, H. (1990). The cell biology of TGF-β. Biochem. Biophys. Acta 1032, 79-87.
6. Biehs, B., Sturtevant, M. and Bier, E. (1998). Boundaries in the Drosophila wing imaginal disc organize vain-specific genetic programs. Development 125, 4245-4257.
7. Blair, S. (1992). Shaggy (zeste-white 3) and the formation of supernumerary bristle precursors in the developing wing blade of Drosophila. Dev. Biol. 152, 263-278.
8. Brand, A. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
9. Chai, J., Wu, J., Yan, N., Massagué, J., Pavletich, N. and Shi, Y. (2003). Features of Smad3 MH1-DNA complex: role of water and zinc in DNA binding. J. Biol. Chem. 278, 20327-20331.
10. Chen, Y., Riese, M., Killinger, M. and Hoffmann, F. (1998). A genetic screen for modifiers of Drosophila dpp signaling identifies mutations in punt, Mad and the BMP-7 homologue, 60A. Development 125, 1759-1768.
11. Couso, J., Bishop, S. and Martinez-Arias, A. (1994). The wingless signaling pathway and the patterning of the wing margin in Drosophila. Development 120, 621-636.
12. Dai, J., Turnacioglu, K., Schutte, M., Sugar, A. and Kern, S. (1998). DPC4 transcriptional activation and dysfunction in cancer cells. Cancer Res. 58, 4592-4597.
13. 1 cell cycle arrest and apoptosis induction by nuclear Smad4/DPC4: phenotypes reversed by a tumorigenic mutation. Proc. Natl. Acad. Sci. USA 96, 1427-1432.
14. Das, P., Maduzia, L., Wang, H., Finelli, A., Cho, S., Smith, M. and Padgett, R. (1998). The Drosophila gene Medea demonstrates the requirement for different classes of Smads in Dpp signaling. Development 125, 1519-1528.
15. de Celis, J., Barrio, R. and Kafatos, F. (1996). A gene complex acting downstream of dpp in Drosophila wing morphogenesis. Nature 381, 421-424.
16. Diaz-Benjumea, F. and Cohen, S. (1993). Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75, 741-752.
17. Drysdale, R. A. and Crosby, M. A. (2005). FlyBase: genes and gene models. Nucl. Acids Res. 33, D390-D395.
18. Eppert, K., Scherer, S., Ozcelik, S., Pirone, R., Hoodless, P., Kim, H., Tsui, L., Bapat, B., Gallinger, S., Andrulis, I. et al. (1996). MADR2 maps to 18q21 and encodes a TGF-β regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86, 543-552.
19. Fynan, T. and Reiss, M. (1993). Resistance to inhibition of cell growth by TGF-β and its role in oncogenesis. Crit. Rev. Oncog. 4, 493-540.
20. Gritzan, U., Hatini, V. and DiNardo, S. (1999). Mutual antagonism between signals secreted by adjacent Wg and En cells leads to specification of complementary regions of the Drosophila parasegment. Development 126, 4107-4115.
21. Hahn, S., Schutte, M., Hoque, A., Moskaluk, C., Da Costa, L., Rozenblum, E., Weinstein, C., Fischer, A., Yeo, C., Hruban, R. et al. (1996). DPC-4: a candidate tumor suppressor gene at human chromosome 18q21. Science 271, 350-353.
22. Hamada, F., Tomoyasu, Y., Takatsu, Y., Nakamura, M., Nagai, S., Suzuki, A., Fujita, F., Shibuya, H., Toyoshima, K., Ueno, N. et al. (1999). Negative regulation of Wg signaling by Daxin, Drosophila homolog of axin. Science 283, 1739-1742.
23. Hayward, P., Brennan, K., Sanders, P., Balayo, T., DasGupta, R., Perrimon, N. and Martinez-Arias, A. (2005). Notch modulates Wnt signaling by associating with Armadillo/β-catenin and regulating its transcriptional activity. Development 132, 1819-1830.
24. Held, L. (2002). Imaginal Discs: The Genetic and Cellular Logic of Pattern Formation. Cambridge: Cambridge University Press.
25. Hempen, P., Zhang, L., Bansal, R., Iacobuzio-Donahue, C., Murphy, K., Maitra, A., Vogelstein, B., Whitehead, R., Markowitz, S., Willson, J. et al. (2003). Evidence of selection for clones having genetic inactivation of the activin A type II receptor gene in gastrointestinal cancers. Cancer Res. 63, 994-999.
26. Hoodless, P., Haerry, T., Abdollah, S., Stapleton, M., O'Connor, M., Attisano, L. and Wrana, J. (1996). MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500.
27. Howe, J., Roth, S., Ringold, J., Summers, R., Jarvinen, H., Sistonen, P., Tomlinson, I., Houlston, R., Bevan, S., Mitros, F. et al. (1998). Mutations in the Smad4/DPC4 gene in juvenile polyposis. Science 280, 1086-1088.
28. Hu, M. and Rosenblum, N. (2004). Smad1, β-catenin and Tcf4 associate in a molecular complex with the myc promoter in dysplastic renal tissue and cooperate to control myc transcription. Development 132, 215-225.
29. Hu, M., Piscione, T. and Rosenblum, N. (2003). Elevated Smad1/β-catenin complexes and renal medullary dysplasia in ALK3 transgenic mice. Development 130, 2753-2766.
30. Hudson, J., Podos, S., Keith, K., Simpson, S. and Ferguson, E. (1998). The Drosophila Medea gene is required downstream of Dpp and encodes a functional homolog of human Smad4. Development 125, 1407-1420.
31. Iacobuzio-Donahue, C., Song, J., Parmiagiani, G., Yeo, C., Hruban, R. and Kern, S. (2004). Missense mutations of MADH4: characterization of the mutational hot spot and functional consequences in human tumors. Clin. Cancer Res. 10, 1597-1604.
32. Inoue, T. and Thomas, J. (2000). Targets of TGF-β signaling in C. elegans dauer formation. Dev. Biol. 217, 192-204.
33. Janody, F., Lee, J., Jahren, N., Hazelett, D., Benlali, A., Miura, G., Draskovic, I. and Treisman, J. (2004). A mosaic genetic screen reveals distinct roles for Trithorax and Polycomb group genes in Drosophila eye development. Genetics 166, 187-200.
34. Kinzler, K. and Vogelstein, B. (1996). Lessons from hereditary colon cancer. Cell 87, 159-170.
35. Lagna, G., Hata, A., Hemmati-Brivanlou, A. and Massagué, J. (1996). Partnership between DPC4 and Smads in TGF-β signaling pathways. Nature 383, 832-836.
36. Lorson, C., Hahnen, E., Androphy, E. and Wirth, B. (1999). A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc. Natl. Acad. Sci. USA 96, 6307-6311.
37. Marenda, D., Zraly, C. and Dingwall, A. (2004). The Drosophila Brahma (SWI/SNF) chromatin remodeling complex exhibits cell-type specific activation and repression functions. Dev. Biol. 267, 279-293.
38. Marquez, R., Singer, M., Takaesu, N., Waldrip, W., Kraytsberg, Y. and Newfeld, S. (2001). Transgenic analysis of the Smad family of TGF-β signal transducers in Drosophila suggests new roles and interactions between family members. Genetics 157, 1639-1648.
39. Massagué, J., Blain, S. and Lo, R. (2000). TGF-β signaling in growth control, cancer & heritable disorders. Cell 103, 295-309.
40. Newfeld, S., Chartoff, E., Graff, J., Melton, D. and Gelbart, W. (1996). Mad encodes a conserved cytoplasmic protein required in DPP/TGF-β responsive cells. Development 122, 2099-2108.
41. Newfeld, S., Wisotzkey, R. and Kumar, S. (1999). Molecular evolution of a developmental pathway: Phylogenetic analyses of TGF-β family ligands, receptors and Smad signal transducers. Genetics 152, 783-795.
42. Nicholls, R. and Gelbart, W. (1998). Identification of chromosomal regions involved in dpp function in Drosophila. Genetics 149, 203-215.
43. Nishita, M., Hashimoto, M., Ogata, S., Laurent, M., Ueno, N., Shibuya, H. and Cho, K. (2000). Interaction between Wnt and TGF-β signaling pathways during formation of Spemann's organizer. Nature 403, 781-785.
44. Padgett, R., Wozney, J. and Gelbart, W. (1993). Human BMP sequences confer normal dorsal-ventral patterning in Drosophila embryos. Proc. Natl. Acad. Sci. USA 90, 2905-2909.
45. Peltomaki, P. (2001). Deficient DNA mismatch repair: a common etiologic factor for colon cancer. Hum. Mol. Gen. 10, 735-740.
46. Pouliot, F. and LaBrie, C. (1999). Expression profile of agonistic Smads in human breast cancer cells: absence of regulation by estrogens. Int. J. Cancer 81, 98-103.
47. Raftery, L., Twombly, V., Wharton, K. and Gelbart, W. (1995). Genetic screens to identify elements of the dpp signaling pathway in Drosophila. Genetics 139, 241-254.
48. Ray, R. and Wharton, K. (2001). Context-dependent relationship between the BMPs gbb and dpp during development of the Drosophila wing disk. Development 128, 3913-3925.
49. Riggins, G., Thiagalingam, S., Rozenblum, E., Weinstein, C., Kern, S., Hamilton, S., Willson, J., Markowitz, S., Kinzler, K. and Vogelstein, B. (1996). Mad-related genes in the human. Nat. Genet. 13, 347-349.
50. Riggins, G., Kinzler, K., Vogelstein, B. and Thiagalingam, S. (1997). Frequency of Smad gene mutations in human cancers. Cancer Res. 57, 2578-2580.
51. Sampath, T., Rashka, K., Doctor, J., Tucker, R. and Hoffmann, F. (1993). Drosophila TGF-β superfamily proteins induce endochondrial bone formation in mammals. Proc. Natl. Acad. Sci. USA 90, 6004-6008.
52. Sansom, O., Reed, K., Hayes, A., Ireland, H., Brinkmann, H., Newton, I., Bathe, E., Simon-Assmann, P., Clevers, H., Nathke, I. et al. (2004). Loss of APC in vivo immediately perturbs Wnt signaling, differentiation and migration. Genes Dev. 18, 1385-1390.
53. Schutte, M., Hruban, R., Hedrick, L., Cho, K., Nadasdy, G., Weinstein, C., Bova, G., Isaacs, W., Cairns, P., Nawroz, H. et al. (1996). DPC4 gene in various tumor types. Cancer Res. 56, 2527-2530.
54. Sekelsky, J., Newfeld, S., Raftery, L., Chartoff, E. and Gelbart, W. (1995). Genetic characterization and cloning of Mad, a gene required for dpp function in Drosophila. Genetics 139, 1347-1358.
55. Shi, Y., Wang, Y., Jayaraman, L., Yang, H., Massagué, J. and Pavelitch, N. (1998). Crystal structure of a Smad MH1 domain bound to DNA: insights on DNA binding. Cell 94, 585-594.
56. Siegfried, E., Chou, T. and Perrimon, N. (1992). wg signaling acts through zeste-white3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell 71, 1167-1179.
57. Skeath, J. and Carroll, S. (1991). Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev. 5, 984-995.
58. Souza, R. (2001). A molecular rationale for the how, when and why of colorectal cancer screening. Aliment. Pharmacol. Ther. 15, 451-462.
59. St Johnston, R., Hoffmann, F., Blackman, R., Segal, D., Grimaila, R., Padgett, R., Irick, H. and Gelbart, W. (1990). Molecular organization of the dpp gene in Drosophila. Genes Dev. 4, 1114-1127.
60. Su, M., Wisotzkey, R. and Newfeld, S. (2001). A screen for modifiers of dpp mutant phenotypes identifies lilliputian, the only member of the Fragile-X/Burkitt's Lymphoma family of transcription factors in Drosophila. Genetics 157, 717-725.
61. Thatcher, J., Haun, C. and Okkema, P. (1999). The DAF-3 Smad binds DNA and represses gene expression in the Caenorhabditis elegans pharynx. Development 126, 97-107.
62. Thiagalingam, S., Lengauer, D., Leach, F., Schutte, M., Hahn, S., Overhauser, J., Willson, J., Markowitz, S., Hamilton, S., Kern, S. et al. (1996). Evaluation of candidate tumor suppressor genes on chromosome 18 in colorectal cancer. Nat. Genet. 13, 343-346.
63. Wisotzkey, R., Mehra, A., Sutherland, D., Dobens, L., Liu, X., Dohrmann, C., Attisano, L. and Raftery, L. (1998). Medea is a Drosophila Smad4 homolog that is differentially required to potentiate Dpp responses. Development 125, 1433-1445.
64. Wolff, T. (2000). Histological techniques for the Drosophila eye. Part I: Larva and Pupa. In Drosophila Protocols (ed. W. Sullivan, M. Ashburner and R. Hawley), pp. 201-227. New York: Cold Spring Harbor Laboratory Press.
65. Xu, J. and Attisano, L. (2000). Mutations in the tumor suppressors Smad2 and Smad4 inactivate TGF-β signaling by targeting Smads to the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 97, 4820-4825.
66. Xu, X., Yin, Z., Hudson, J., Ferguson, E. and Frasch, M. (1998). Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev. 12, 2354-2370.
67. Yu, K., Sturtevant, M., Biehs, B., Francois, V., Padgett, R., Blackman, R. and Bier, E. (1996). The Drosophila dpp and sog genes function antagonistically during wing vein development. Development 122, 4033-4044.
68. Zhang, H., Chen, X., Wang, M., Wang, J., Qi, Q., Zhang, R., Xu, W., Fei, Q., Wang, F., Cheng, Q., et al. (2004). Defective expression of TGF-β receptor type II is associated with CpG methylated promoter in primary non-small cell lung cancer. Clin. Cancer Res. 10, 2359-2367.