TGF-β signaling, Smads, and tumor suppressors

BioEssays

Volumn 20, Issue 5, 1998, Pages 382-390

  Padgett, Richard W ^a,b   Das, Pradeep ^a   Krishna, Srikant ^a  

^a RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; PHOSPHOPROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; DROSOPHILA; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; TRANSACTIVATION; VERTEBRATE;

ANIMALS; CAENORHABDITIS ELEGANS; DNA-BINDING PROTEINS; DROSOPHILA; GENE EXPRESSION REGULATION; MODELS, GENETIC; PHOSPHOPROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; VERTEBRATES;

ANIMALIA; CAENORHABDITIS ELEGANS; VERTEBRATA;

EID: 0031863899     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-1878(199805)20:5<382::AID-BIES5>3.0.CO;2-Q     Document Type: Review

References (87)

1. Roberts AB, Anzano MA, Lamb LC, Smith JM, Sporn MB (1981) New class of transforming growth factors potentiated by epidermal growth factor. Proc Natl Acad Sci USA 78:5339-5343.
2. Mathews LS, Vale WW (1991) Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65:973-982.
3. Ebner R, Chen R-H, Shum L, Lawler S, Zioncheck TF, Lee A, Lopez AR, Derynck R (1993) Cloning of a type I TGF-β receptor and its effect on TGF-β binding to the type II receptor. Science 260:1344.
4. Sekelsky JJ, Newfeld SJ, Raftery LA, Chartoff EH, Gelbart WM (1995) Genetic characterization and cloning of Mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139:1347-1358.
5. Savage C, Das P, Finelli AL, Townsend SR, Sun C-Y, Baird SE, Padgett RW (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.
6. Derynck R, Jarrett JA, Chen EY, Eaton DH, Bell JR, Assoian HK, Roberts AB, Sporn MB, Goeddel DV (1985) Human transforming growth factor-beta complementary DNA sequence and expression in normal and transformed cells. Nature 316:701-705.
7. Mason AJ, Hayflick JS, Ling N, Esch F, Ueno N, Ying SY, Guillemin H, Niall H, Seeburg PH (1986) Complementary DNA sequences of ovarian follicular fluid inhibin show precursor structure and homology with transforming growth factor-beta. Nature 318:659-663.
8. Spencer FA, Hoffman FM, Gelbart WM (1982) Decapentaplegic: A gene complex affecting development in Drosophila melanogaster. Cell 28:451-461.
9. Segal D, Gelbart WM (1985) Shortvein, a new component of the decapentaplegic gene complex in Drosophila melanogaster. Genetics 109: 119-143.
10. Irish VF, Gelbart WM (1987) The decapentaplegic gene is required for dorso-ventral patterning of the Drosophila embryo. Genes Dev 1:868-879.
11. Padgett RW, St Johnston RD, Gelbart WM (1987) A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family. Nature 325:81-84.
12. Padgett RW, Wozney JM, Gelbart WM (1993) Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc Natl Acad Sci USA 90:2905-2909.
13. Sampath TK, Rashka KE, Doctor JS, Tucker RF, Hoffmann FM (1993) Drosophila transforming growth factor beta superfamily proteins induce endochondral bone formation in mammals. Proc Natl Acad Sci USA 90:6004-6008.
14. Arora K, Levine MS, O'Connor MB (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.
15. Wharton KA, Thomsen GH, Gelbart WM (1991) Drosophila 60A gene, another transforming growth factor beta family member, is closely related to human bone morphogenetic proteins. Proc Natl Acad Sci USA 88:9214-9218.
16. Doctor JS, Jackson PD, Rashka KE, Visalli M, Hoffmann FM (1992) Sequence, biochemical characterization, and developmental expression of a new member of the TGF-β superfamily in Drosophila melanogaster. Dev Biol 151:491-505.
17. Wrana JL, Tran H, Attisano L, Arora K, Childs SR, Massagué J, O'Connor MB (1994) Two distinct transmembrane serine/threonine kinases from Drosophila melanogaster form an activin receptor complex. Mol Cell Biol 14:944-950.
18. Ruberte E, Marty T, Nellen D, Affolter M, Basler K (1995) An absolute requirement for both the type II and type I receptors, punt and thick veins, for dpp signaling in vivo. Cell 80:889-897.
19. Georgi LL, Albert PS, Riddle DL (1990) daf-1, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell 61:635-645.
20. Estevez M, Attisano L, Wrana JL, Albert PS, Massagué J, Riddle DL (1993) The daf-4 gene encodes a bone morphogenetic protein receptor controlling C elegans dauer larvae development. Nature 365:644-649.
21. Ren P, Lim CS, Johnsen R, Albert PS, Pilgrim D, Riddle DL (1996) Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science 274:1389-1391.
22. Jurgens G, Wieschaus E, Nüsslein-Volhard C, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. Wilhelm Rouxs Arch Dev Biol 193:283-295.
23. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA (1988) Novel regulators of bone formation: Molecular clones and activities. Science 242:1528-1531.
24. Shimell MJ, Ferguson EL, Childs SR, O'Connor MB (1991) The Drosophila dorsal-ventral gene tolloid is related the human bone morphogenetic protein 1. Cell 67:469-481.
25. Ferguson EL, Anderson KV (1992a) Localized enhancement and repression of the activity of the TGF-beta family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114:583-597.
26. Zwilling R, Neurath H (1987) Invertebrate proteases. Methods Enzymol 81:633-664
27. Journet A, Tosi M (1986) Cloning and sequencing of full-length cDNA encoding the precursor of human complement component Clr. Biochem J 240:783-787.
28. Mackinnon CM, Carter PE, Smith SJ, Dunbar B, Fothergill JE (1987) Molecular cloning of cDNA for human complement component Cls. Eur J Biochem 169:547-553.
29. Childs SR, O'Connor MB (1994) Two domains of the tolloid protein contribute to its unusual genetic interaction with decapentaplegic. Dev Biol 162:209-220.
30. Finelli AL, Bossie CA, Xie T, Padgett RW (1994) Mutational analysis of the Drosophila tolloid gene, a human BMP-1 homolog. Development 120:861-870
31. Stöcker W, Zwilling R (1995) Astacin. Methods Enzymol 248:305-325
32. Roebroek AJM, Creemers JWM, Pauli IGL, Kurzik-Dumke U, Rentrop M, Gateff EAF, Leunissen JAM, Van de Ven WJM (1992) Cloning and functional expression of Dfurin2, a subtilisin-like proprotein processing enzyme of Drosophila melanogaster with multiple repeats of a cysteine motif. J Biol Chem 24:17208-17215.
33. Graff JM, Thies RS, Song JJ, Celeste AJ, Melton DA (1994) Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 79:169-179.
34. Suzuki N, Labosky PA, Furuta Y, Hargett L, Dunn R, Fogo AB, Takahara K, Peters DMP, Greenspan DS, Hogan BLM (1996) Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid. Development 122:3587-3595.
35. Sasai Y, Lu B, Steinbeisser H, De Robertis EM (1995) Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus Nature 376:333-336
36. Xu RJ, Kim J, Taira M, Zhan S, Sredni D, Kung H (1995) A dominant-negative bone morphogenetic protein-4 receptor causes neuralization in Xenopus ectoderm. Biochem Biophys Res Commun 212:212-219.
37. Hawley SHB, Wünnenberg-Stapleton K, Hashimoto C, Laurent MN, Watabe T, Blumberg BW, Cho KWY (1995) Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev 9:2923-2935.
38. Steinbeisser H, Fainsod A, Niehrs C, Sasai Y, De Robertis EM (1995) The role of gscand BMP-4 in dorsal-ventral patterning of the marginal zone in Xenopus: A loss-of-function study using antisense RNA. EMBO J 14:5230-5243.
39. Piccolo S, Sasai Y, Lu B, De Robertis EM (1996) Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86:589-598.
40. Zimmerman LB, De Jesús-Escobar JM, Harland RM (1996) The Spemann organizer signal noggin binds and inactivates bone morphoqenetic protein 4. Cell 86:599-606.
41. Holley SA, Neul JL, Attisano L, Wrana JL, Sasai Y, O'Connor MB, De Robertis EM, Ferguson EL (1996) The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor. Cell 86:607-617.
42. Wieser R, Wrana JL, Massagué J (1995) GS domain mutations that constitutively activate TβR-I, the downstream signaling component in the TGF-beta receptor complex. EMBO J 14:2199-2208.
43. Xie T, Finelli AL, Padgett RW (1994) The Drosophila saxophone gene: A serine-threonine kinase receptor of the TGF-β superfamily. Science 263:1756-1759.
44. Nellen D, Affolter M, Basler K (1994) Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78:225-237.
45. Brummel T, Twombly V, Marques G, Wrana JL, Newfeld S, Attisano L, Massagué J, O'Connor MB, Gelbart WM (1994) Characterization and relationship of dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 78:251-261.
46. Penton A, Chen Y, Staehling-Hampton K, Wrana JL, Attisano L, Szidonya J, Cassill JA, Massagué J, Hoffmann FM (1994) Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that brk25D is a decapentaplegic receptor. Cell 78:239-250.
47. Singer MA, Penton A, Twombly V, Hoffmann FM, Gelbart WM (1997) Signaling through both type I DPP receptors is required for anterior-posterior patterning of the entire Drosophila wing. Development 124:79-89.
48. Letsou A, Arora K, Wrana JL, Simin K, Twombly V, Jamal J, Staehling-Hampton K, Hoffmann FM, Gelbart WM, Massagué J, O'Connor MB (1995) Drosophila dpp signaling is mediated by the punt gene product: A dual ligand-binding type II receptor for the TGF-β receptor family. Cell 80:899-908.
49. Childs SR, Wrana JL, Arora K, Attisano L, O'Connor MB, Massagué J (1993) Identification of a Drosophila activin receptor. Proc Natl Acad Sci USA 90:9475-9479.
50. ten Dijke P, Miyazono K, Heldin CH (1996) Signaling via heteroligomeric complexes of type I and type II serine/threonine kinase receptors. Curr Opin Cell Biol 8:139-145.
51. Anders RA, Leof EB (1996) Chimeric granulocyte/macrophage colony stimulating factor/transforming growth factor-β (TGF-β) receptors define a model system for investigating the role of homomeric and heteromeric receptors in TGF-β signaling. J Biol Chem 271:21758-21766.
52. Luo K, Lodish HF (1996) Signaling by chimeric erythropoietin-TGF-β receptors: Homodimerization of the cytoplasmic domain of the type I TGF-β receptor and heterodimerization with the type II receptor are both required for intracellular signal transduction. EMBO J 15:4485-4496.
53. Raftery LA, Twombly V, Wharton K, Gelbart WM (1995) Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics 139:241-254.
54. Derynck R, Gelbart WM, Harland RM, Heldin C-H, Kern SE, Massagué J, Melton DA, Mlodzik M, Padgett RW, Roberts AB, Smith J, Thomsen GH, Vogelstein B, Wang XF (1996) Nomenclature Vertebrate mediators of TGF-β family signals. Cell 87:173.
55. Hoodless PA, Haeny T, Abdollah S, Stapleton M, O'Connor MB, Attisano L, Wrana JL (1996) MADRI, a MAD-related protein that functions in BMP2 signalling pathways. Cell 85:489-500.
56. Wiersdorff V, Lecuit T, Cohen SM, Mlodzik M (1996) Mad acts downstream of receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development 122:2153-2162.
57. Newfeld SJ, Chartoff EH, Graff JM, Melton DA, Gelbart WM (1996) Mothers against dpp encodes a conserved cytoplasmic protein required in DPP/TGF-β responsive cells. Development 122:2099-2108.
58. Macias-Silva M, Abdollah S, Hoodless PA, Pirone R, Attisano L, Wrana JL (1996) MADR2 is a substrate of the TGF-β receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 87:1215-1224.
59. Kretzschmar M, Liu F, Hata A, Doody J, 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.
60. Hahn SA, Schutte M, Shamsul Hoque ATM, Moskaluk CA, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH, Kern SE (1996) DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271:350.
61. Eppert K, Scherer SW, Ozcelik H, Pirone R, Hoodless P, Kim H, Tsui LC, Bapat B, Gallinger S, Andrulis IL, Thomsen GH, Wrana JL, 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.
62. Leichleider R, de Caestecker MP, Dehejia A, Polymeropoulos MH, Roberts AB (1996) Serine phosphorylation, chromosomal localization and Transforming Growth Factor-β signal transduction by human bsp-1. J Biol Chem 271:17617-17620.
63. Liu F, Hata A, Baker JC, Doody J, Cárcamo J, Harland RM, Massagué J (1996) A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381:620.
64. Yingling JM, Das P, Savage C, Zhang M, Padgett RW, Wang X-F (1996) Mammalian Dwarfins are phosphorylated in response to TGFβ and are implicated in control of cell growth. Proc Natl Acad Sci USA 93:8940-8944.
65. Graff JM, Bansal A, Melton DA (1996) Xenopus Mad proteins transduce distinct subsets of signals for the TGF-β superfamily. Cell 85:479-487.
66. Thomsen GH (1996) Xenopus mothers against dpp is an embryonic ventralizing agent that acts downstream of the BMP-2/4 receptor. Development 122:2359-2366.
67. Baker JC, Harland RM (1996) A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes Dev 10:1880-1889.
68. Hiyashi H, Abdollah YQ, Cai J, Xu YY, Grinnell BW, Richardson MA, Topper JN, Gimbrone MA Jr, Wrana JL, Falb D (1997) The MAD-related protein Smad7 associates with the TGF-β receptor and functions as an antagonist of TGF-β signaling. Cell 89:1165-1173.
69. Chen X, Rubock MJ, Whitman M (1996) A transcriptional partner for MAD proteins in TGF-β signalling. Nature 383:691.
70. Kim J, Johnson K, Chen HJ, Carroll S, Laughon A (1997) MAD binds to DNA and directly mediates activation of vestigial by DPP. Nature (in press). Nature 388:304
71. Kim J, Johnson K, Chen HJ, Carroll S, Laughon A (1997) MAD binds to DNA and directly mediates activation of vestigial by DPP. Nature (in press). Nature 388:304
72. Markowitz SD, Roberts AB (1996) Tumor suppressor activity of the TGF-β pathway in human cancers. Cytokine Growth Factor Rev 7:93-102.
73. Riggins GJ, Thiagalingam S, Rozenblum E, Weinstein CL, Kern SE, Hamilton SR, Willson JK, Markowitz SD, Kinzler KW, Vogelstein B (1996) Mad-related genes in the human. Nature Genet 13:347.
74. Shi Y, Hata A, Lo RS, Massagué J, Pavletich NP (1997) A structural basis for mutational inactivation by the tumour suppressor Smad4. Nature 388:87.
75. Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N, Taniguchi T, Nishida E, Matsumoto K (1995) Identification of a member of the MAPKKK family as a potential mediator of TGF-β signal transduction. Science 270:2008.
76. Kretzschmar M, Doody J, Massagué J (1997) Opposing BMP and EGF signalling pathways converge on the TGF-β family mediator Smad1. Nature 389:618.
77. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, Miyazono K (1997) Smad6 inhibits signalling by the TGF-β superfamily. Nature 389:622.
78. Nakao A, Afrakhte M, Morén A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin N-E, Heldin C-H, ten Dijke P (1997) Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 389:631.
79. Tsuneizumi K, Nakayama T, Kamoshida Y, Kornberg TB, Christian JL, Tabata T (1997) Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature 389:627.
80. Marqués G, Musacchio M, Shimell MJ, Wünnenberg-Stapleton K, Cho, KWY, O'Connor MB (1997) Production of a DPP Activity Gradient in the Early Drosophila Embryo through the Opposing Actions of the SOG and TLD proteins. Cell 91:417.
81. Piccolo S, Agius E, Lu B, Goodman S, Dale L, De Robertis EM (1997) Cleavage of Chordin by Xolloid Metalloprotease Suggests a Role for Proteolytic Processing in the Regulation of Spemann Organizer Activity. Cell 91:407.
82. Patterson GI, Koweek A, Wong A, Ruvkun G (1997) The DAF-3 Smad protein antagonizes TGF-β-related receptor signaling in the Caenorhabditis elegans dauer pathway. Genes & Development 11:2679.
83. Das P, Maduzia LL, Wang H, Finelli AL, Cho S-H, Smith MM, Padgett RW (1998) The Drosophila gene Medea demonstrates the requirement for different classes of Smads in dpp signaling. Development 125 (In Press).
84. Hudson JB, Podos SD, Keith K, Simpson SL, Ferguson EL (1998) The Drosophila Medea gene is required downstream of dpp and encodes a functional homolog of human Smad4. Development 125 (In Press).
85. Wisotzkey RG, Mehra A, Sutherland DJ, Dobens LL, Liu X, Dohrmann C, Attisano L, Raftery LA (1998) Medea is a Drosophila Smad4 homolog that is differentially required to potentiate DPP responses. Development 125 (In Press).
86. Liu F, Pouponnot C, Massagué J (1997) Dual role of the Smad4/DPC4 tumor suppressor in TGFβ-inducible transcriptional complexes. Genes & Development 11:3157.
87. Hata A, Lagna G, Massagué J, Hemmati-Brivanlou (1998) Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes & Development 12:186-197.