TGFβ in Cancer

Cell

Volumn 134, Issue 2, 2008, Pages 215-230

  Massagué, Joan ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 9; MEMBRANE RECEPTOR; MITOGENIC AGENT; MUELLERIAN INHIBITING FACTOR; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

APOPTOSIS; AUTOCRINE EFFECT; CANCER CELL; CANCER INHIBITION; CARCINOGENIC ACTIVITY; CELL AGING; CELL DIFFERENTIATION; CELL INVASION; CELL LINE; CELL TRANSFORMATION; CYTOSTASIS; DNA BINDING; EPITHELIUM CELL; FIBROBLAST; HUMAN; IMMUNITY; IMMUNOREGULATION; MESENCHYME CELL; METASTASIS; MICROENVIRONMENT; MODULATION; MYOFIBROBLAST; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STROMA; STROMA CELL; ANIMAL; DISEASE COURSE; DRUG ANTAGONISM; METABOLISM; NEOPLASM;

METAZOA;

ANIMALS; DISEASE PROGRESSION; HUMANS; NEOPLASMS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 47549090432     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.07.001     Document Type: Review

References (119)

1. Allinen M., Beroukhim R., Cai L., Brennan C., Lahti-Domenici J., Huang H., Porter D., Hu M., Chin L., Richardson A., et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6 (2004) 17-32
2. Arteaga C.L. Inhibition of TGFbeta signaling in cancer therapy. Curr. Opin. Genet. Dev. 16 (2006) 30-37
3. Ashcroft G.S., Yang X., Glick A.B., Weinstein M., Letterio J.L., Mizel D.E., Anzano M., Greenwell-Wild T., Wahl S.M., Deng C., and Roberts A.B. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat. Cell Biol. 1 (1999) 260-266
4. Bardeesy N., Cheng K.H., Berger J.H., Chu G.C., Pahler J., Olson P., Hezel A.F., Horner J., Lauwers G.Y., Hanahan D., and DePinho R.A. Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer. Genes Dev. 20 (2006) 3130-3146
5. Becker C., Fantini M.C., and Neurath M.F. TGF-beta as a T cell regulator in colitis and colon cancer. Cytokine Growth Factor Rev. 17 (2006) 97-106
6. Bhowmick N.A., Chytil A., Plieth D., Gorska A.E., Dumont N., Shappell S., Washington M.K., Neilson E.G., and Moses H.L. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303 (2004) 848-851
7. Bhowmick N.A., Ghiassi M., Bakin A., Aakre M., Lundquist C.A., Engel M.E., Arteaga C.L., and Moses H.L. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell 12 (2001) 27-36
8. Bierie B., and Moses H.L. Tumour microenvironment: TGFbeta: The molecular Jekyll and Hyde of cancer. Nat. Rev. Cancer 6 (2006) 506-520
9. Biswas S., Chytil A., Washington K., Romero-Gallo J., Gorska A.E., Wirth P.S., Gautam S., Moses H.L., and Grady W.M. Transforming growth factor beta receptor type II inactivation promotes the establishment and progression of colon cancer. Cancer Res. 64 (2004) 4687-4692
10. Biswas S., Guix M., Rinehart C., Dugger T.C., Chytil A., Moses H.L., Freeman M.L., and Arteaga C.L. Inhibition of TGF-beta with neutralizing antibodies prevents radiation-induced acceleration of metastatic cancer progression. J. Clin. Invest. 117 (2007) 1305-1313
11. Bleuming S.A., He X.C., Kodach L.L., Hardwick J.C., Koopman F.A., Ten Kate F.J., van Deventer S.J., Hommes D.W., Peppelenbosch M.P., Offerhaus G.J., et al. Bone morphogenetic protein signaling suppresses tumorigenesis at gastric epithelial transition zones in mice. Cancer Res. 67 (2007) 8149-8155
12. Broderick P., Carvajal-Carmona L., Pittman A.M., Webb E., Howarth K., Rowan A., Lubbe S., Spain S., Sullivan K., Fielding S., et al. A genome-wide association study shows that common alleles of SMAD7 influence colorectal cancer risk. Nat. Genet. 39 (2007) 1315-1317
13. Bruna A., Darken R.S., Rojo F., Ocana A., Penuelas S., Arias A., Paris R., Tortosa A., Mora J., Baselga J., and Seoane J. High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer Cell 11 (2007) 147-160
14. Buck M.B., Fritz P., Dippon J., Zugmaier G., and Knabbe C. Prognostic significance of transforming growth factor beta receptor II in estrogen receptor-negative breast cancer patients. Clin. Cancer Res. 10 (2004) 491-498
15. Cerutti J.M., Ebina K.N., Matsuo S.E., Martins L., Maciel R.M., and Kimura E.T. Expression of Smad4 and Smad7 in human thyroid follicular carcinoma cell lines. J. Endocrinol. Invest. 26 (2003) 516-521
16. Chen C.R., Kang Y., Siegel P.M., and Massagué J. E2F4/5 and p107 as Smad cofactors linking the TGFbeta receptor to c-myc repression. Cell 110 (2002) 19-32
17. Dalal B.I., Keown P.A., and Greenberg A.H. Immunocytochemical localization of secreted transforming growth factor-beta 1 to the advancing edges of primary tumors and to lymph node metastases of human mammary carcinoma. Am. J. Pathol. 143 (1993) 381-389
18. Davis B.N., Hilyard A.C., Lagna G., and Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454 (2008) 56-61
19. De Robertis E.M., and Kuroda H. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20 (2004) 285-308
20. De Wever O., and Mareel M. Role of tissue stroma in cancer cell invasion. J. Pathol. 200 (2003) 429-447
21. Derynck R., and Akhurst R.J. Differentiation plasticity regulated by TGF-beta family proteins in development and disease. Nat. Cell Biol. 9 (2007) 1000-1004
22. Descargues P., Sil A.K., Sano Y., Korchynskyi O., Han G., Owens P., Wang X.J., and Karin M. IKKalpha is a critical coregulator of a Smad4-independent TGFbeta-Smad2/3 signaling pathway that controls keratinocyte differentiation. Proc. Natl. Acad. Sci. USA 105 (2008) 2487-2492
23. Dowdy S.C., Mariani A., Reinholz M.M., Keeney G.L., Spelsberg T.C., Podratz K.C., and Janknecht R. Overexpression of the TGF-beta antagonist Smad7 in endometrial cancer. Gynecol. Oncol. 96 (2005) 368-373
24. Dupont S., Zacchigna L., Cordenonsi M., Soligo S., Adorno M., Rugge M., and Piccolo S. Germ-layer specification and control of cell growth by Ectodermin, a Smad4 ubiquitin ligase. Cell 121 (2005) 87-99
25. Engle S.J., Ormsby I., Pawlowski S., Boivin G.P., Croft J., Balish E., and Doetschman T. Elimination of colon cancer in germ-free transforming growth factor beta 1-deficient mice. Cancer Res. 62 (2002) 6362-6366
26. Feng X.H., and Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 21 (2005) 659-693
27. Fidler I.J. The pathogenesis of cancer metastasis: The 'seed and soil' hypothesis revisited. Nat. Rev. Cancer 3 (2003) 453-458
28. Foletta V.C., Lim M.A., Soosairajah J., Kelly A.P., Stanley E.G., Shannon M., He W., Das S., Massagué J., and Bernard O. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J. Cell Biol. 162 (2003) 1089-1098
29. Forrester E., Chytil A., Bierie B., Aakre M., Gorska A.E., Sharif-Afshar A.R., Muller W.J., and Moses H.L. Effect of conditional knockout of the type II TGF-beta receptor gene in mammary epithelia on mammary gland development and polyomavirus middle T antigen induced tumor formation and metastasis. Cancer Res. 65 (2005) 2296-2302
30. Friese M.A., Wischhusen J., Wick W., Weiler M., Eisele G., Steinle A., and Weller M. RNA interference targeting transforming growth factor-beta enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumorigenicity in vivo. Cancer Res. 64 (2004) 7596-7603
31. Gomis R.R., Alarcon C., He W., Wang Q., Seoane J., Lash A., and Massagué J. A FoxO-Smad synexpression group in human keratinocytes. Proc. Natl. Acad. Sci. USA 103 (2006) 12747-12752
32. Gomis R.R., Alarcon C., Nadal C., Van Poznak C., and Massagué J. C/EBPbeta at the core of the TGFbeta cytostatic response and its evasion in metastatic breast cancer cells. Cancer Cell 10 (2006) 203-214
33. Gorelik L., and Flavell R.A. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12 (2000) 171-181
34. Groppe J., Hinck C.S., Samavarchi-Tehrani P., Zubieta C., Schuermann J.P., Taylor A.B., Schwarz P.M., Wrana J.L., and Hinck A.P. Cooperative assembly of TGF-beta superfamily signaling complexes is mediated by two disparate mechanisms and distinct modes of receptor binding. Mol. Cell 29 (2008) 157-168
35. Guasch G., Schober M., Pasolli H.A., Conn E.B., Polak L., and Fuchs E. Loss of TGFbeta signaling destabilizes homeostasis and promotes squamous cell carcinomas in stratified epithelia. Cancer Cell 12 (2007) 313-327
36. Gupta G.P., and Massagué J. Cancer metastasis: Building a framework. Cell 127 (2006) 679-695
37. Gupta G.P., Perk J., Acharyya S., de Candia P., Mittal V., Todorova-Manova K., Gerald W.L., Brogi E., Benezra R., and Massagué J. ID genes mediate tumor reinitiation during breast cancer lung metastasis. Proc. Natl. Acad. Sci. USA 104 (2007) 19506-19511
38. He W., Dorn D.C., Erdjument-Bromage H., Tempst P., Moore M.A., and Massagué J. Hematopoiesis controlled by distinct TIF1gamma and Smad4 branches of the TGFbeta pathway. Cell 125 (2006) 929-941
39. He X.C., Zhang J., Tong W.G., Tawfik O., Ross J., Scoville D.H., Tian Q., Zeng X., He X., Wiedemann L.M., et al. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat. Genet. 36 (2004) 1117-1121
40. Ijichi H., Chytil A., Gorska A.E., Aakre M.E., Fujitani Y., Fujitani S., Wright C.V., and Moses H.L. Aggressive pancreatic ductal adenocarcinoma in mice caused by pancreas-specific blockade of transforming growth factor-beta signaling in cooperation with active Kras expression. Genes Dev. 20 (2006) 3147-3160
41. Jaffee E.M., Hruban R.H., Canto M., and Kern S.E. Focus on pancreas cancer. Cancer Cell 2 (2002) 25-28
42. Javelaud D., Mohammad K.S., McKenna C.R., Fournier P., Luciani F., Niewolna M., Andre J., Delmas V., Larue L., Guise T.A., and Mauviel A. Stable overexpression of Smad7 in human melanoma cells impairs bone metastasis. Cancer Res. 67 (2007) 2317-2324
43. Jen J., Harper J.W., Bigner S.H., Bigner D.D., Papadopoulos N., Markowitz S., Willson J.K., Kinzler K.W., and Vogelstein B. Deletion of p16 and p15 genes in brain tumors. Cancer Res. 54 (1994) 6353-6358
44. Jennings M.T., and Pietenpol J.A. The role of transforming growth factor beta in glioma progression. J. Neurooncol. 36 (1998) 123-140
45. Jones S., Chen W.D., Parmigiani G., Diehl F., Beerenwinkel N., Antal T., Traulsen A., Nowak M.A., Siegel C., Velculescu V.E., et al. Comparative lesion sequencing provides insights into tumor evolution. Proc. Natl. Acad. Sci. USA 105 (2008) 4283-4288
46. *6A and prostate cancer. BMC Genet. 5 (2004) 28
47. Kakonen S.M., Selander K.S., Chirgwin J.M., Yin J.J., Burns S., Rankin W.A., Grubbs B.G., Dallas M., Cui Y., and Guise T.A. Transforming growth factor-beta stimulates parathyroid hormone-related protein and osteolytic metastases via Smad and mitogen-activated protein kinase signaling pathways. J. Biol. Chem. 277 (2002) 24571-24578
48. Kang Y., Chen C.R., and Massagué J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol. Cell 11 (2003) 915-926
49. Kang Y., Siegel P.M., Shu W., Drobnjak M., Kakonen S.M., Cordon-Cardo C., Guise T.A., and Massagué J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3 (2003) 537-549
50. Kang Y., He W., Tulley S., Gupta G.P., Serganova I., Chen C.R., Manova-Todorova K., Blasberg R., Gerald W.L., and Massagué J. Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc. Natl. Acad. Sci. USA 102 (2005) 13909-13914
51. Kim B.G., Li C., Qiao W., Mamura M., Kasprzak B., Anver M., Wolfraim L., Hong S., Mushinski E., Potter M., et al. Smad4 signalling in T cells is required for suppression of gastrointestinal cancer. Nature 441 (2006) 1015-1019
52. Kingsley L.A., Fournier P.G., Chirgwin J.M., and Guise T.A. Molecular biology of bone metastasis. Mol. Cancer Ther. 6 (2007) 2609-2617
53. Kobielak K., Stokes N., de la Cruz J., Polak L., and Fuchs E. Loss of a quiescent niche but not follicle stem cells in the absence of bone morphogenetic protein signaling. Proc. Natl. Acad. Sci. USA 104 (2007) 10063-10068
54. Kominsky S.L., Doucet M., Brady K., and Weber K.L. TGF-beta promotes the establishment of renal cell carcinoma bone metastasis. J. Bone Miner. Res. 22 (2007) 37-44
55. Korchynskyi O., and ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 277 (2002) 4883-4891
56. Krimpenfort P., Ijpenberg A., Song J.Y., van der Valk M., Nawijn M., Zevenhoven J., and Berns A. p15Ink4b is a critical tumour suppressor in the absence of p16Ink4a. Nature 448 (2007) 943-946
57. Letterio J.J. TGF-beta signaling in T cells: Roles in lymphoid and epithelial neoplasia. Oncogene 24 (2005) 5701-5712
58. Levy L., and Hill C.S. Alterations in components of the TGF-beta superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev. 17 (2006) 41-58
59. Li M.O., Wan Y.Y., Sanjabi S., Robertson A.K., and Flavell R.A. Transforming growth factor-beta regulation of immune responses. Annu. Rev. Immunol. 24 (2006) 99-146
60. Li W., Qiao W., Chen L., Xu X., Yang X., Li D., Li C., Brodie S.G., Meguid M.M., Hennighausen L., and Deng C.X. Squamous cell carcinoma and mammary abscess formation through squamous metaplasia in Smad4/Dpc4 conditional knockout mice. Development 130 (2003) 6143-6153
61. Lin X., Duan X., Liang Y.Y., Su Y., Wrighton K.H., Long J., Hu M., Davis C.M., Wang J., Brunicardi F.C., et al. PPM1A functions as a Smad phosphatase to terminate TGFbeta signaling. Cell 125 (2006) 915-928
62. Loeys B.L., Schwarze U., Holm T., Callewaert B.L., Thomas G.H., Pannu H., De Backer J.F., Oswald G.L., Symoens S., Manouvrier S., et al. Aneurysm syndromes caused by mutations in the TGF-beta receptor. N. Engl. J. Med. 355 (2006) 788-798
63. Lu S.L., Herrington H., Reh D., Weber S., Bornstein S., Wang D., Li A.G., Tang C.F., Siddiqui Y., Nord J., et al. Loss of transforming growth factor-beta type II receptor promotes metastatic head-and-neck squamous cell carcinoma. Genes Dev. 20 (2006) 1331-1342
64. Lu T., Tian L., Han Y., Vogelbaum M., and Stark G.R. Dose-dependent cross-talk between the transforming growth factor-beta and interleukin-1 signaling pathways. Proc. Natl. Acad. Sci. USA 104 (2007) 4365-4370
65. Maggio-Price L., Treuting P., Zeng W., Tsang M., Bielefeldt-Ohmann H., and Iritani B.M. Helicobacter infection is required for inflammation and colon cancer in SMAD3-deficient mice. Cancer Res. 66 (2006) 828-838
66. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., Brooks M., Reinhard F., Zhang C.C., Shipitsin M., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133 (2008) 704-715
67. Massagué J., and Chen Y.G. Controlling TGF-beta signaling. Genes Dev. 14 (2000) 627-644
68. Massagué J., Seoane J., and Wotton D. Smad transcription factors. Genes Dev. 19 (2005) 2783-2810
69. Minn A.J., Gupta G.P., Siegel P.M., Bos P.D., Shu W., Giri D.D., Viale A., Olshen A.B., Gerald W.L., and Massagué J. Genes that mediate breast cancer metastasis to lung. Nature 436 (2005) 518-524
70. Monteleone G., Mann J., Monteleone I., Vavassori P., Bremner R., Fantini M., Del Vecchio Blanco G., Tersigni R., Alessandroni L., Mann D., et al. A failure of transforming growth factor-beta1 negative regulation maintains sustained NF-kappaB activation in gut inflammation. J. Biol. Chem. 279 (2004) 3925-3932
71. Muñoz N.M., Upton M., Rojas A., Washington M.K., Lin L., Chytil A., Sozmen E.G., Madison B.B., Pozzi A., Moon R.T., et al. Transforming growth factor beta receptor type II inactivation induces the malignant transformation of intestinal neoplasms initiated by Apc mutation. Cancer Res. 66 (2006) 9837-9844
72. Muraoka R.S., Koh Y., Roebuck L.R., Sanders M.E., Brantley-Sieders D., Gorska A.E., Moses H.L., and Arteaga C.L. Increased malignancy of Neu-induced mammary tumors overexpressing active transforming growth factor beta1. Mol. Cell. Biol. 23 (2003) 8691-8703
73. Nguyen A.V., and Pollard J.W. Transforming growth factor beta3 induces cell death during the first stage of mammary gland involution. Development 127 (2000) 3107-3118
74. Niehrs C., and Pollet N. Synexpression groups in eukaryotes. Nature 402 (1999) 483-487
75. Ozdamar B., Bose R., Barrios-Rodiles M., Wang H.R., Zhang Y., and Wrana J.L. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 307 (2005) 1603-1609
76. Padua D., Zhang X.H., Wang Q., Nadal C., Gerald W.L., Gomis R.R., and Massagué J. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133 (2008) 66-77
77. Pardali K., Kurisaki A., Moren A., ten Dijke P., Kardassis D., and Moustakas A. Role of Smad proteins and transcription factor Sp1 in p21(Waf1/Cip1) regulation by transforming growth factor-beta. J. Biol. Chem. 275 (2000) 29244-29256
78. Pardali K., and Moustakas A. Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim. Biophys. Acta 1775 (2007) 21-62
79. Rich J.N., Zhang M., Datto M.B., Bigner D.D., and Wang X.F. Transforming growth factor-beta-mediated p15(INK4B) induction and growth inhibition in astrocytes is SMAD3-dependent and a pathway prominently altered in human glioma cell lines. J. Biol. Chem. 274 (1999) 35053-35058
80. Roberts A.B., and Wakefield L.M. The two faces of transforming growth factor beta in carcinogenesis. Proc. Natl. Acad. Sci. USA 100 (2003) 8621-8623
81. Rodgarkia-Dara C., Vejda S., Erlach N., Losert A., Bursch W., Berger W., Schulte-Hermann R., and Grusch M. The activin axis in liver biology and disease. Mutat. Res. 613 (2006) 123-137
82. Rubtsov Y.P., and Rudensky A.Y. TGFbeta signalling in control of T-cell-mediated self-reactivity. Nat. Rev. Immunol. 7 (2007) 443-453
83. Ruzinova M.B., and Benezra R. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13 (2003) 410-418
84. Sapkota G., Knockaert M., Alarcon C., Montalvo E., Brivanlou A.H., and Massagué J. Dephosphorylation of the linker regions of Smad1 and Smad2/3 by small C-terminal domain phosphatases has distinct outcomes for bone morphogenetic protein and transforming growth factor-beta pathways. J. Biol. Chem. 281 (2006) 40412-40419
85. Sapkota G., Alarcon C., Spagnoli F.M., Brivanlou A.H., and Massagué J. Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol. Cell 25 (2007) 441-454
86. Scandura J.M., Boccuni P., Massagué J., and Nimer S.D. Transforming growth factor beta-induced cell cycle arrest of human hematopoietic cells requires p57KIP2 up-regulation. Proc. Natl. Acad. Sci. USA 101 (2004) 15231-15236
87. Seoane J., Le H.V., and Massagué J. Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 419 (2002) 729-734
88. Seoane J., Le H.V., Shen L., Anderson S.A., and Massagué J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117 (2004) 211-223
89. Seton-Rogers S.E., Lu Y., Hines L.M., Koundinya M., LaBaer J., Muthuswamy S.K., and Brugge J.S. Cooperation of the ErbB2 receptor and transforming growth factor beta in induction of migration and invasion in mammary epithelial cells. Proc. Natl. Acad. Sci. USA 101 (2004) 1257-1262
90. Shi Y., and Massagué J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113 (2003) 685-700
91. Shipitsin M., Campbell L.L., Argani P., Weremowicz S., Bloushtain-Qimron N., Yao J., Nikolskaya T., Serebryiskaya T., Beroukhim R., Hu M., et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 11 (2007) 259-273
92. Siegel P.M., Shu W., Cardiff R.D., Muller W.J., and Massagué J. Transforming growth factor beta signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis. Proc. Natl. Acad. Sci. USA 100 (2003) 8430-8435
93. Silvestri C., Narimatsu M., von Both I., Liu Y., Tan N.B., Izzi L., McCaffery P., Wrana J.L., and Attisano L. Genome-wide identification of Smad/Foxh1 targets reveals a role for Foxh1 in retinoic acid regulation and forebrain development. Dev. Cell 14 (2008) 411-423
94. Sjoblom T., Jones S., Wood L.D., Parsons D.W., Lin J., Barber T.D., Mandelker D., Leary R.J., Ptak J., Silliman N., et al. The consensus coding sequences of human breast and colorectal cancers. Science 314 (2006) 268-274
95. Sneddon J.B., Zhen H.H., Montgomery K., van de Rijn M., Tward A.D., West R., Gladstone H., Chang H.Y., Morganroth G.S., Oro A.E., and Brown P.O. Bone morphogenetic protein antagonist gremlin 1 is widely expressed by cancer-associated stromal cells and can promote tumor cell proliferation. Proc. Natl. Acad. Sci. USA 103 (2006) 14842-14847
96. Staller P., Peukert K., Kiermaier A., Seoane J., Lukas J., Karsunky H., Moroy T., Bartek J., Massagué J., Hanel F., and Eilers M. Repression of p15INK4b expression by Myc through association with Miz-1. Nat. Cell Biol. 3 (2001) 392-399
97. Suzuki K., Wilkes M.C., Garamszegi N., Edens M., and Leof E.B. Transforming growth factor beta signaling via Ras in mesenchymal cells requires p21-activated kinase 2 for extracellular signal-regulated kinase-dependent transcriptional responses. Cancer Res. 67 (2007) 3673-3682
98. Swarbrick A., Roy E., Allen T., and Bishop J.M. Id1 cooperates with oncogenic Ras to induce metastatic mammary carcinoma by subversion of the cellular senescence response. Proc. Natl. Acad. Sci. USA 105 (2008) 5402-5407
99. Sweet K., Willis J., Zhou X.P., Gallione C., Sawada T., Alhopuro P., Khoo S.K., Patocs A., Martin C., Bridgeman S., et al. Molecular classification of patients with unexplained hamartomatous and hyperplastic polyposis. JAMA 294 (2005) 2465-2473
100. Takaku K., Oshima M., Miyoshi H., Matsui M., Seldin M.F., and Taketo M.M. Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell 92 (1998) 645-656
101. Tang B., Yoo N., Vu M., Mamura M., Nam J.S., Ooshima A., Du Z., Desprez P.Y., Anver M.R., Michalowska A.M., et al. Transforming growth factor-beta can suppress tumorigenesis through effects on the putative cancer stem or early progenitor cell and committed progeny in a breast cancer xenograft model. Cancer Res. 67 (2007) 8643-8652
102. Taylor I.W., and Wrana J.L. SnapShot: The TGFbeta pathway interactome. Cell 133 (2008) 378
103. Thiery J.P. Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 15 (2003) 740-746
104. Thomas D.A., and Massagué J. TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 8 (2005) 369-380
105. Thuault S., Valcourt U., Petersen M., Manfioletti G., Heldin C.H., and Moustakas A. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. J. Cell Biol. 174 (2006) 175-183
106. Tu W.H., Thomas T.Z., Masumori N., Bhowmick N.A., Gorska A.E., Shyr Y., Kasper S., Case T., Roberts R.L., Shappell S.B., et al. The loss of TGF-beta signaling promotes prostate cancer metastasis. Neoplasia 5 (2003) 267-277
107. Wang J., Xu N., Feng X., Hou N., Zhang J., Cheng X., Chen Y., Zhang Y., and Yang X. Targeted disruption of Smad4 in cardiomyocytes results in cardiac hypertrophy and heart failure. Circ. Res. 97 (2005) 821-828
108. Wang R.H., Li C., Xu X., Zheng Y., Xiao C., Zerfas P., Cooperman S., Eckhaus M., Rouault T., Mishra L., and Deng C.X. A role of SMAD4 in iron metabolism through the positive regulation of hepcidin expression. Cell Metab. 2 (2005) 399-409
109. Wolfraim L.A., Walz T.M., James Z., Fernandez T., and Letterio J.J. p21Cip1 and p27Kip1 act in synergy to alter the sensitivity of naive T cells to TGF-beta-mediated G1 arrest through modulation of IL-2 responsiveness. J. Immunol. 173 (2004) 3093-3102
110. Wrzesinski S.H., Wan Y.Y., and Flavell R.A. Transforming growth factor-beta and the immune response: implications for anticancer therapy. Clin. Cancer Res. 13 (2007) 5262-5270
111. Xie W., Mertens J.C., Reiss D.J., Rimm D.L., Camp R.L., Haffty B.G., and Reiss M. Alterations of Smad signaling in human breast carcinoma are associated with poor outcome: a tissue microarray study. Cancer Res. 62 (2002) 497-505
112. Xu L. Regulation of Smad activities. Biochim. Biophys. Acta 1759 (2006) 503-513
113. Yan M., Rerko R.M., Platzer P., Dawson D., Willis J., Tong M., Lawrence E., Lutterbaugh J., Lu S., Willson J.K., et al. 15-Hydroxyprostaglandin dehydrogenase, a COX-2 oncogene antagonist, is a TGF-beta-induced suppressor of human gastrointestinal cancers. Proc. Natl. Acad. Sci. USA 101 (2004) 17468-17473
114. Yang L., Huang J., Ren X., Gorska A.E., Chytil A., Aakre M., Carbone D.P., Matrisian L.M., Richmond A., Lin P.C., and Moses H.L. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 13 (2008) 23-35
115. Yin J.J., Selander K., Chirgwin J.M., Dallas M., Grubbs B.G., Wieser R., Massagué J., Mundy G.R., and Guise T.A. TGF-beta signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J. Clin. Invest. 103 (1999) 197-206
116. Ying Q.L., Nichols J., Chambers I., and Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115 (2003) 281-292
117. Zahnow C.A., Younes P., Laucirica R., and Rosen J.M. Overexpression of C/EBPbeta-LIP, a naturally occurring, dominant-negative transcription factor, in human breast cancer. J. Natl. Cancer Inst. 89 (1997) 1887-1891
118. Zhang F., Lee J., Lu S., Pettaway C.A., and Dong Z. Blockade of transforming growth factor-beta signaling suppresses progression of androgen-independent human prostate cancer in nude mice. Clin. Cancer Res. 11 (2005) 4512-4520
119. Zhu Q., Krakowski A.R., Dunham E.E., Wang L., Bandyopadhyay A., Berdeaux R., Martin G.S., Sun L., and Luo K. Dual role of SnoN in mammalian tumorigenesis. Mol. Cell. Biol. 27 (2007) 324-339