TGFβ signaling pathways and human diseases

Cancer and Metastasis Reviews

Volumn 18, Issue 2, 1999, Pages 247-259

  Padgett, Richard W ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Cancer; Development; Growth factors; Smads; TGF

Indexed keywords

SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA; DNA BINDING PROTEIN; LIGAND;

CARCINOGENESIS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; GENE ACTIVATION; GENE EXPRESSION; GENE MUTATION; GENETIC DISORDER; HUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CAENORHABDITIS ELEGANS; DROSOPHILA; METABOLISM; NEOPLASM; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS ELEGANS; DNA-BINDING PROTEINS; DROSOPHILA; HUMANS; LIGANDS; NEOPLASMS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 0033237402     PISSN: 01677659     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006325408261     Document Type: Review

References (115)

1. Kingsley DM: The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 8: 133-146, 1994
2. Massagué J: TGFβ signal transduction. Annu Rev Biochem 67: 753-791, 1998
3. Padgett RW, St. Johnston RD, Gelbart WM: A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family. Nature 325: 81-84, 1987
4. Brummel T, Abdollah S, Haerry TE, Shimell MJ, Merriam J, Raftery L, Wrana JL, O'Connor MB: The Drosophila activin receptor baboon signals through dSmad2 and controls cell proliferation but not patterning during larval development. Genes Dev 13: 98-111, 1999
5. Das P, Inoue H, Baker JC, Beppu H, Kawabata M, Harland RM, Miyazono K, Padgett RW: Drosophila dSmad2 and Atr-I transmit Activin/TGFβ Signals. Genes to Cells 4 (in press), 1999
6. Estevez M, Attisano L, Wrana JL, Albert PS, Massagué J, Riddle DL: The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development. Nature 365: 644-649, 1993
7. Savage C, Das P, Finelli AL, Townend SR, Sun C-Y, Baird SE, Padgett RW: Caenorhabditis elegans genes sma-2, sma-3, and sma-4 define a conserved family of transforming growth factorβ pathway components. Proc Natl Acad Sci USA 93: 790-794, 1996
8. Ren P, Lim CS, Johnsen R, Albert PS, Pilgrim D, Riddle DL: Control of C. elegans larval development by neuronal expression of a TGF-β homolog. Science 274: 1389-1391, 1996
9. Patterson GI, Koweek A, Wong A, Liu Y, Ruvkun C: The DAF-3 Smad protein antagonizes TGF-β-related receptor signaling in the Caenorhabditis elegans dauer pathway. Genes Dev 11: 2679-2690, 1997
10. Krishna S, Maduzia LL, Padgett RW: Specificity of TGFβ signaling is conferred by distinct type I receptors and their associated SMAD proteins in Caenorhabditis elegans. Development 126: 251-260, 1999
11. Morita K, Chow KL, Ueno N: Regulation of body length and male tail ray pattern formation of Caenorhabditis elegans by a member of TGF-β family. Development 126: 1337-1347, 1999
12. Suzuki Y, Yandell MD, Roy PJ, Krishna S, Savage-Dunn C, Ross RM, Padgett RW, Wood WB: A BMP homolog acts as a dose-dependent regulator of body size and male tail patterning in Caeiwrhabditis elegans. Development 126: 241-250, 1999
13. Cheifetz S, Weatherbee JA, Tsang ML, Anderson JK, Mole JE, Lucas R, Massague J: The transforming growth factor-beta system, a complex pattern of cross-reactive ligands and receptors. Cell 48: 409-415, 1987
14. Ebner R, Chen RH, Shum L, Lawler S, Zioncheck TF, Lee A, Lopez AR, Derynck R: Cloning of a type I TGF-β receptor and its effect on TGF-beta binding to the type II receptor. Science 260: 1344-1348, 1993
15. Mathews LS, Vale WW: Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65: 973-982, 1991
16. Ruberte E, Marty T, Nellen D, Affolter M, Basler K: 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, 1995
17. Letsou A, Arora K, Wrana JL, Simm K, Twombly V, Jamal J, Staehung-Hampton K, Hoffmann FM, Gelbari WM, Massagué J, et al.: 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, 1995
18. Yamashita H, ten Dijke P, Franzen P, Miyazono K, Heldin CH: Formation of hetero-oligomeric complexes of type I and type II receptors for transforming growth factor-beta. J Biol Chem 269: 20172-20178, 1994
19. Koenig BB, Cook JS, Wolsing DH, Ting J, Tiesman JP, Correa PE, Olson CA, Pecquet AL, Ventura F, Grant RA, et al.: Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol Cell Biol 14: 5961-5974, 1994
20. Franzen P, ten Dijke P, Ichijo H, Yamashita H, Schultz P, Heldin C-H, Miyazono K: Cloning of a TGF-β type I receptor that forms a heteromeric complex with the TFG-β type II receptor. Cell 75: 681-692, 1993
21. ten Dijke P, Ichijo H, Franzen P, Schulz P, Saras J, Toyoshima H, Heldin CH, Miyazono K: Activin receptor-like kinases: a novel subclass of cell-surface receptors with predicted serine/threonine kinase activity. Oncogene 8: 2879-2887, 1993
22. Attisano L, Cárcamo J, Ventura F, Weis FM, Massagué J, Wrana JL: Identification of human activin and TGFβ type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75: 671-680, 1993
23. ten Dijke P, Yamashita H, Sampath TK, Reddi AH, Estevez M, Riddle DL, Ichijo H, Heldin CH, Miyazono K: Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J Biol Chem 269: 16985-16988, 1994
24. Liu F, Ventura F, Doody J, Massagué J: Human type II receptor for bone morphogenic proteins (BMPs): extension of the two-kinase receptor model to the BMPs. Mol Cell Biol 15: 3479-3486, 1995
25. Armes NA, Neal KA, Smith JC: A short loop on the ALK-2 and ALK-4 activin receptors regulates signaling specificity but cannot account for all their effects on early Xenopus development. J Biol Chem 274: 7929-7935, 1999
26. Watanabe R, et al.: The MH1 domains of Smad2 and Smad3 are involved in the regulation of the ALK7 signals. Biochem Biophys Res Commun 254: 707-712, 1999
27. Yelick PC, Abduljabbar TS, Stashenko P: zALK-8, a novel type I serine/threonine kinase receptor, is expressed throughout early zebrafish development. Dev Dyn 211: 352-361, 1998
28. Xie T, Finelli AL, Padgett RW: The Drosophila saxophone Gene: A serine-threonine kinase receptor of the TGF-β superfamily. Science 263: 1756-1759, 1994
29. Brummel TJ, Twombly V, Marques G, Wrana JL, Newfeld SJ, Attisano L, Massagué J, O'Connor MB, Gelbart WM: Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 78: 251-261, 1994
30. Nellen D, Affolter M, Basler K: Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78: 225-237, 1994
31. Penton A, Chen Y, Staehling-Hampton K, Wrana JL, Attisano L, Szidonya J, Cassill JA, Massagué J, Hoffmann FM: Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk2SD is a decapenlaplegic receptor. Cell 78: 239-250, 1994
32. Wrana JL, Tran H, Attisano L, Arora K, Childs SR, Massagué J, O'Connor MB: Two distinct transmembrane serine/threonine kinases from Drosophila melanogaster form an activin receptor complex. Mol Cell Biol 14: 944-950, 1994
33. Georgi LL, Albert PS, Riddle DL: daf-I, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell 61: 635-645, 1990
34. Bassing CH, Yingling JM, Howe DJ, Wang T, He WW, Gustafson ML, Shah P, Donahoe PK, Wang XF: A transforming growth factor beta type I receptor that signals to activate gene expression. Science 263: 87-89, 1994
35. Chen RH, Ebner R, Derynck R: Inactivation of the type II receptor reveals two receptor pathways for the diverse TGF-β activities. Science 260: 1335-1338, 1993
36. Rosenzweig BL, Imamura T, Okadome T, Cox GN, Yamashita H, ten Dijke P, Heldin CH, Miyazono K: Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc Natl Acad Sci USA 92: 7632-7636, 1995
37. Nohno T, Ishikawa T, Saito T, Hosokawa K, Noji S, Wolsing DH, Rosenbaum JS: Identification of a human type II receptor for bone morphogenetic protein-4 that forms differential heteromeric complexes with bone morphogenetic protein type I receptors. J Biol Chem 270: 22522-22526, 1995
38. Nishitoh H, Ichijo H, Kimura M, Matsumoto T, Makishima F, Yamaguchi A, Yamashita H, Enomoto S, Miyazono K: Identification of type I and type II serine/threonine kinase receptors for growth/differentiation factor-5. J Biol Chem 271: 21345-21352, 1996
39. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J: Mechanism of activation of the TGF-β receptor. Nature 370: 341-347, 1994
40. Sekelsky JJ, Newfeld SJ, Raftery LA, Chartoff EH, Gelbart WM: Genetic characterization and cloning of Mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139: 1347-1358, 1995
41. Derynck R, Gelbart WM, Harland RM, Heldin CH, Kern SE, Massagué J, Melton DA, Mlodzik M, Padgett RW, Roberts AB, Smith J, Thomsen GH, Vogeistein B, Wang XF: Nomenclature: vertebrate mediators of TGFβ family signals. Cell 87: 173, 1996
42. Hoodless PA, Haerry T, Abdollah S, Stapleton M, O'Connor MB, Attisano L, Wrana JL: MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85: 489-500, 1996
43. Wiersdorff V, Lecuit T, Cohen SM, Mlodzik M: 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, 1996
44. Zhang Y, Feng X, We R, Derynck R: Receptor-associated Mad homologues synergize as effectors of the TGF-β response. Nature 383: 168-172, 1996
45. Yingling JM, Das P, Savage C, Zhang M, Padgett RW, Wang XF: Mammalian dwarfins are phosphorylated in response to transforming growth factor β and are implicated in control of cell growth. Proc Nat Acad Sci USA 93: 8940-8944, 1996
46. 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: MADR2 maps to 18q21 and encodes a TGFβ-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86: 543-552, 1996
47. Lechleider RJ, de Caestecker MP, Dehejia A, Polymeropoulos MH, Roberts AB: Serine phosphorylation, chromosomal localization, and transforming growth factor-β signal transduction by human bsp-1. J Biol Chem 271: 17617-17620, 1996
48. Lagna G, Hata A, Hemmati-Brivanlou A, Massagué J: Partnership between DPC4 and SMAD proteins in TGF-β signalling pathways. Nature 383: 832-836, 1996
49. Tsukazaki T, Chiang TA, Davison AF, Attisano L, Wrana JL: SARA, a FYVE domain protein that recruits Smad2 to the TGFβ receptor. Cell 95: 779-791, 1998
50. Liu F, Hata A, Baker JC, Doody J, Cárcamo J, Harland RM, Massagué J: A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381: 620-623, 1996
51. Baker JC, Harland RM: A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes Dev 10: 1880-1889, 1996
52. Das P, Maduzia LL, Wang H, Finelli AL, Cho SH, Smith MM, Padgett RW: The Drosophila gene Medea demonstrates the requirement for different classes of Smads in dpp signaling. Development 125: 1519-1528, 1998
53. Wisotzkey RG, Mehra A, Sutherland DJ, Dobens LL, Liu X, Dohrmann C, Attisano L, Raftery LA: Medea is a Drosophila Smad4 homolog that is differentially required to potentiate DPP responses. Development 125: 1433-1445, 1998
54. Hudson JB, Podos SD, Keith K, Simpson SL, Ferguson EL: The Drosophila Medea gene is required downstream of dpp and encodes a functional homolog of human Smad4. Development 125: 1407-1420, 1998
55. Tsuneizumi K, Nakayama T, Kamoshida Y, Kornberg TB, Christian JL, Tabata T: Daughters against dpp modulates dpp organizing activity in Drosophila wing development [see comments]. Nature 389: 627-631, 1997
56. Graff JM, Bansal A, Melton DA: Xenopus Mad proteins transduce distinct subsets of signals for the TGFβ superfamily. Cell 85: 479-487, 1996
57. Waldrip WR, Bikoff EK, Hoodless PA, Wrana JL, Robertson EJ: Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell 92: 797-808, 1998
58. Weinstein M, Yang X, Li C, Xu X, Gotay J, Deng CX: Failure of egg cylinder elongation and mesoderm induction in mouse embryos lacking the tumor suppressor Smad2. Proc Natl Acad Sci USA 95: 9378-9383, 1998
59. Yang X, Letterio JJ, Lechleider RJ, Chen L, Hayman R, Gu H, Roberts AB, Deng C: Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-β. Embo J 18: 1280-1291, 1999
60. Liu F, Pouponnot C, Massague J: Dual role of the Smad4/DPC4 tumor suppressor in TGFbeta-inducible transcriptional complexes. Genes Dev 11: 3157-3167, 1997
61. Chen X, Rubock MJ, Whitman M: A transcriptional partner for MAD proteins in TGF-β signalling. Nature 383: 691-696, 1996
62. Sirard C, de la Pompa JL, Elia A, Itie A, Mirtsos C, Cheung A, Hahn S, Wakeham A, Schwanz L, Kern SE, Rossant J, Mak TW: The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev 12: 107-119, 1998
63. Yang X, Li C, Xu X, Deng C: The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc Natl Acad Sci USA 95: 3667-3672, 1998
64. Takaku K, Oshima M, Miyoshi H, Matsui M, Seidin MF, Taketo MM: Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell 92: 645-656, 1998
65. Nomura M, Li E: Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature 393: 786-790, 1998
66. Datto MB, Frederick JP, Pan L, Borton AJ, Zhuang Y, Wang XF: Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction. Mol Cell Biol 19: 2495-2504, 1999
67. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, ten Dijke P: TGF-β receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J. 16: 5353-5362, 1997
68. Lo RS, Chen YG, Shi Y, Pavletich NP, Massague J: The L3 loop: a structural motif determining specific interactions between SMAD proteins and TGF-beta receptors. Embo J 17: 996-1005, 1998
69. Yingling JM, Datto MB, Wong C, Frederick JP, Liberati NT, Wang XF: Tumor suppressor Smad4 is a transforming growth factor beta-inducible DNA binding protein. Mol Cell Biol 17: 7019-7028, 1997
70. Chen X, Weisberg E, Fridmacher V, Watanabe M, Naco C, Whitman M: Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature 389: 85-89, 1997
71. Suzuki A, Chang C, Yingling JM, Wang XF, Hemmati-Brivanlou A: Smad5 induces ventral fates in Xenopus embryo. Dev Biol 184: 402-405, 1997
72. Hild M, Dick A, Rauch GJ, Meier A, Bouwmeester T, Haffter P, Hammerschmidt M: The smad5 mutation somitabun blocks bmp2b signaling during early dorsoventral patterning of the zebrafish embryo [In Process Citation]. Development 126: 2149-2159, 1999
73. Roelen BA, van Rooijen MA, Mummery CL: Expression of ALK-1, a type 1 serine/threonine kinase receptor, coincides with sites of vasculogenesis and angiogenesis in early mouse development. Dev Dyn 209: 418-430, 1997
74. McAllister KA, Grogg KM, Johnson DW, Gallione CJ, Baldwin MA, Jackson CE, Helmbold EA, Markel DS, McKinnon WC, Murrell J, et al.: Endoglin, a TGF-β binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet 8: 345-351, 1994
75. Nusslein-Volhard C, Wieschaus E: Mutations affecting segment number and polarity in Drosophila. Nature 287: 795-801, 1980
76. Spencer FA, Hoffmann FM, Gelbart WM: Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28: 451-461, 1982
77. Derynck R, Jarrett JA, Chen EY, Eaton DH, Bell JR, Assoian RK, Roberts AB, Sporn MB, Goeddel DV: Human transforming growth factor-β complementary DNA sequence and expression in normal and transformed cells. Nature 316: 701-706, 1985
78. Mason AJ, Hayflick JS, Ling N, Esch F, Ueno N, Ying SY, Guillemin R, Niall H, Seeburg PH: Complementary DNA sequences of ovarian follicular fluid inhibin show precursor structure and homology with transforming growth factor-beta. Nature 318: 659-663, 1985
79. Padgett RW, Wozney JM, Gelbart WM: Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc Nat Acad Sci USA 90: 2905-2909, 1993
80. Sampath TK, Rashka KE, Doctor JS, Tucker RF, Hoffmann FM: Drosophila transforming growth factor beta superfamily proteins induce endochondral bone formation in mammals. Proc Natl Acad Sci USA 90: 6004-6008, 1993
81. Irish VF, Gelbart WM: The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev 1: 868-879, 1987
82. Arora K, Levine MS, O'Connor MB: 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, 1994
83. Chen Y, Riese MJ, Killinger MA, Hoffmann FM: A genetic screen for modifiers of Drosophila decapentaplegic signaling identifies mutations in punt, Mothers against dpp and the BMP-7 homologue, 60A. Development 125: 1759-1768, 1998
84. Khalsa O, Yoon JW, Torres-Schumann S, Wharton KA: 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, 1998
85. Riddle DL, Swanson MM, Albert PS: Interacting genes in nematode dauer larva formation. Nature 290: 668-671, 1981
86. Brenner S: The genetics of Caenorhabditis elegans. Genetics 77: 71-94, 1974
87. Colavita A, Culotti JG: Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans. Dev Biol 194: 72-85, 1998
88. Sulston JE, Albertson DG, Thomson JN: The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev Biol 78: 542-576, 1980
89. Liu KS and Sternberg PW: Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14: 79-89, 1995
90. Baird SE, Fitch DH, Kassem IA, Emmons SW: Pattern formation in the nematode epidermis: determination of the arrangement of peripheral sense organs in the C. elegans male tail. Development 113: 515-526, 1991
91. Chow KL, Emmons SW: HOM-C/Hox genes and four interacting loci determine the morphogenetic properties of single cells in the nematode male tail. Development 120: 2579-2592, 1994
92. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G: The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389: 994-999, 1997
93. Ferguson EL, Horvitz HR: Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics 110: 17-72, 1985
94. Kim SK, Horvitz HR: The Caenorhabditix elegans gene lin-10 is broadly expressed while required specifically for the determination of vulval cell fates. Genes Dev 4: 357-371, 1990
95. Miller LM, Gallegos ME, Morisseau BA, Kim SK: lin-31, a Caenorhabditis elegans HNF-3/fork head transcription factor homolog, specifies three alternative cell fates in vulval development. Genes Dev 7: 933-947, 1993
96. Baird SE, Ellazar SA: TGFβ-like signaling and spicule development in Caenorhabditis elegans. Dev Biol (in press) 1999
97. Markowitz S, Wang J, Myeroff L, Parsons R, Sun L, Lutterbaugh J, Fan RS, Zborowska E, Kinzler KW, Vogelstein B, Brittain M, Willson JKV: Inactivation of the Type II TGF-β receptor in colon cancer cells with microsatellite instability. Science 268: 1336-1338, 1995
98. Markowitz SD, Roberts AB: Tumor suppressor activity of the TGF-beta pathway in human cancers. Cytokine Growth Factor Rev 7: 93-102, 1996
99. Strom EE, Huynh TV, Copeland NG, Jenkins NA, Kingsley DM, Lee SJ: Limb alternations in brachypodism mice due to mutations in a new member of the TGFβ superfamily. Nature 368: 639-643, 1994
100. Storm EE, Kingsley DM: Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 122: 3969-3979, 1996
101. Thomas JT, Lin K, Nandedkar M, Camargo M, Cervenka J, Luyten FP: A human chondrodysplasia due to a mutation in a TGF-β superfamily member. Nat Genet 12: 315-317, 1996
102. Guerrier D, Tran D, Vanderwinden JM, Hideux S, Van Outryve L, Legeai L, Bouchard M, Van Vliet G, De Laet MH, Picard JY, et al.: The persistent Müllerian duct syndrome: a molecular approach. J Clin Endocrinol Metab 68: 46-52, 1989
103. Knebelmann B, Boussin L, Guerrier D, Legeai L, Kahn A, Josso N, Picard JY: Anti-Müllerian hormone Bruxelles: a nonsense mutation associated with the persistent Müllerian duct syndrome. Proc Natl Acad Sci USA 88: 3767-3771,
104. Carré-Eusèbe D, Imbeaud S, Harbison M, New MI, Josso N, Picard JY: Variants of the anti-Müllerian hormone gene in a compound heterozygote with the persistent Müllerian duct syndrome and his family. Hum Genet 90: 389-394,
105. Imbeaud S, Carré-Eusèbe D, Rey R, Belville C, Josso N, Picard JY: Molecular genetics of the persistent Müllerian duct syndrome: a study of 19 families. Hum Mol Genet 3: 125-131, 1994
106. Imbeaud S, Faure E, Lamarre I, Mattei MG, di Clemente N, Tizard R, Carré-Eusèbe D, Belville C, Tragethon L, Tonkin C, et al.: Insensitivity to anti-Müllerian hormone due to a mutation in the human anti-Müllerian hormone receptor. Nat Genet 11: 382-388, 1995
107. Faure E, Gouedard L, Imbeaud S, Cate R, Picard JY, Josso N, di Clemente N: Mutant isoforms of the anti-Müllerian hormone type II receptor are not expressed at the cell membrane. J Biol Chem 271: 30571-30575, 1996
108. Mishina Y, Rey R, Finegold MJ, Matzuk MM, Josso N, Cate RL, Behringer RR: Genetic analysis of the Müllerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev 10: 2577-2587, 1996
109. Hahn SA, Schutte M, Hoque ATMS, Moskaluk CA, Costa LTD, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH, Kern SE: DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271: 350-353, 1996
110. Takagi Y, Kohmura H, Futamura M, Kida H, Tanemura H, Shimokawa K, Saji S: Somatic alterations of the DPC4 gene in human colorectal cancers in vivo. Gastroenterology 111: 1369-1372, 1996
111. MacGrogan D, Pegram M, Slamon D, Bookstein R: Comparative mutational analysis of DPC4 (Smad4) in prostatic and colorectal carcinomas. Oncogene 15: 1111-1114, 1997
112. Lei J, Zou TT, Shi YQ, Zhou X, Smolinski KN, Yin J, Souza RF, Appel R, Wang S, Cymes K, Chan O, Abraham JM, Harpaz N, Meltzer SJ: Infrequent DPC4 gene mutation in esophageal cancer, gastric cancer and ulcerative colitis-associated neoplasms. Oncogene 13: 2459-2462, 1996
113. Kim SK, Fan Y, Papadimitrakopoulou V, Clayman G, Hittelman WN, Hong WK, Lotan R, Mao L: DPC4, a candidate tumor suppressor gene, is altered infrequently in head and neck squamous cell carcinoma. Cancer Res 56: 2519-2521, 1996
114. Schutte M, et al.: DPC4 gene in various tumor types. Cancer Res 56: 2527-2530, 1996
115. Riggins GJ, Thiagalingam S, Rozenblum E, Weinstein CL,Kern SE, Hamilton SR, Wilson JK, Markowitz SD, Kinzler KW, Vogelstein B: Mad-related genes in the human. Nat Genet 13: 347-349, 1996