The immunopharmacological properties of transforming growth factor beta

International Immunopharmacology

Volumn 5, Issue 13-14, 2005, Pages 1771-1782

  Le, Yingying ^a   Yu, Xiaojing ^a   Ruan, Lingfei ^a,b   Wang, Oumei ^a,b   Qi, Dongfei ^a,b   Zhu, Jingjing ^a   Lu, Xiaofeng ^a   Kong, Yan ^a,b   Cai, Kun ^a,b   Pang, Shanshan ^a,b   Shi, Xianglin ^a   Wang, Ji Ming ^c  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Alzheimer's disease; Inflammation; Transforming growth factor beta

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA;

ALZHEIMER DISEASE; AUTOIMMUNE DISEASE; CELL ACTIVITY; CELL PROLIFERATION; DENDRITIC CELL; DRUG EFFECT; HUMAN; IMMUNE RESPONSE; IMMUNOPHARMACOLOGY; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATORY DISEASE; METASTASIS; MOLECULAR GENETICS; PATHOGENESIS; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR GROWTH;

EID: 27744432242     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2005.07.006     Document Type: Review

References (103)

1. A.B. Roberts, M.A. Anzano, L.C. Lamb, J.M. Smith, and M.B. Sporn New class of transforming growth factors potentiated by epidermal growth factor: isolation from non-neoplastic tissues Proc Natl Acad Sci U S A 78 1981 5339 5343
2. R. Govinden, and K.D. Bhoola Genealogy, expression, and cellular function of transforming growth factor-beta Pharmacol Ther 98 2000 257 265
3. J. Massague The transforming growth factor-beta family Annu Rev Cell Biol 6 1990 597 641
4. D.W. Burt, and A.S. Law Evolution of the transforming growth factor-beta superfamily Prog Growth Factor Res 5 1994 99 118
5. A.B. Roberts Molecular and cell biology of TGF-beta Miner Electrolyte Metab 24 1998 111 119
6. S.J. Kim, K.T. Jeang, A.B. Glick, M.B. Sporn, and A.B. Roberts Promoter sequences of the human transforming growth factor-beta 1 gene responsive to transforming growth factor-beta 1 autoinduction J Biol Chem 264 1989 7041 7045
7. R. Lafyatis, R. Lechleider, S.J. Kim, S. Jakowlew, A.B. Roberts, and M.B. Sporn Structural and functional characterization of the transforming growth factor beta 3 promoter. A cAMP-responsive element regulates basal and induced transcription J Biol Chem 265 1990 19128 19136
8. M.A. O'Reilly, A.G. Geiser, S.J. Kim, L.A. Bruggeman, A.X. Luu, and A.B. Roberts Identification of an activating transcription factor (ATF) binding site in the human transforming growth factor-beta 2 promoter J Biol Chem 267 1992 19938 19943
9. J.S. Munger, J.G. Harpel, P.E. Gleizes, R. Mazzieri, I. Nunes, and D.B. Rifkin Latent transforming growth factor-beta: structural features and mechanisms of activation Kidney Int 51 1997 1376 1382
10. G.A. McMahon, J.D. Dignam, and L.E. Gentry Structural characterization of the latent complex between transforming growth factor beta 1 and beta 1-latency-associated peptide Biochem J 313 1996 343 351
11. K. Miyazono, A. Olofsson, P. Colosetti, and C.H. Heldin A role of the latent TGF-beta 1-binding protein in the assembly and secretion of TGF-beta 1 EMBO J 10 1991 1091 1101
12. S. Sinha, C. Nevett, C.A. Shuttleworth, and C.M. Kielty Cellular and extracellular biology of the latent transforming growth factor-beta binding proteins Matrix Biol 17 1998 529 545
13. R.M. Lyons, L.E. Gentry, A.F. Purchio, and H.L. Moses Mechanism of activation of latent recombinant transforming growth factor beta 1 by plasmin J Cell Biol 110 1990 1361 1367
14. J. Taipale, J. Lohi, J. Saarinen, P.T. Kovanen, and J. Keski-Oja Human mast cell chymase and leukocyte elastase release latent transforming growth factor-beta 1 from the extracellular matrix of cultured human epithelial and endothelial cells J Biol Chem 270 1995 4689 4696
15. J.E. Murphy-Ullrich, and M. Poczatek Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology Cytokine Growth Factor Rev 11 2000 59 69
16. A. Fontana, D.B. Constam, K. Frei, U. Malipiero, and H.W. Pfister Modulation of the immune response by transforming growth factor beta Int Arch Allergy Immunol 99 1992 1 7
17. J.H. Kehrl, L.M. Wakefield, A.B. Roberts, S. Jakowlew, M. Alvarez-Mon, and R. Derynck Production of transforming growth factor beta by human T lymphocytes and its potential role in the regulation of T cell growth J Exp Med 163 1986 1037 1050
18. Y. Le, P. Iribarren, W. Gong, Y. Cui, X. Zhang, and J.M. Wang TGF-beta1 disrupts endotoxin signaling in microglial cells through Smad3 and MAPK pathways J Immunol 173 2004 962 968
19. M.J. Ravitz, and C.E. Wenner Cyclin-dependent kinase regulation during G1 phase and cell cycle regulation by TGF-beta Adv Cancer Res 71 1997 165 207
20. L.P. Sanford, I. Ormsby, A.C. Gittenberger-de Groot, H. Sariola, R. Friedman, and G.P. Boivin TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes Development 124 1997 2659 2670
21. V. Kaartinen, J.W. Voncken, C. Shuler, D. Warburton, D. Bu, and N. Heisterkamp Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction Nat Genet 11 1995 415 421
22. Y. Taya, S. O'Kane, and M.W. Ferguson Pathogenesis of cleft palate in TGF-beta3 knockout mice Development 126 1999 3869 3879
23. A.C. Lidral, P.A. Romitti, A.M. Basart, T. Doetschman, N.J. Leysens, and S. Daack-Hirsch Association of MSX1 and TGFB3 with nonsyndromic clefting in humans Am J Hum Genet 63 1998 557 568
24. M.S. Pepper Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity Cytokine Growth Factor Rev 8 1997 21 43
25. M.C. Dickson, J.S. Martin, F.M. Cousins, A.B. Kulkarni, S. Karlsson, and R.J. Akhurst Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice Development 121 1995 1845 1854
26. M. Oshima, H. Oshima, and M.M. Taketo TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis Dev Biol 179 1996 297 302
27. M.M. Shull, I. Ormsby, A.B. Kier, S. Pawlowski, R.J. Diebold, and M. Yin Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease Nature 359 1992 693 699
28. A.B. Kulkarni, C.G. Huh, D. Becker, A. Geiser, M. Lyght, and K.C. Flanders Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death Proc Natl Acad Sci U S A 90 1993 770 774
29. E. Forrester, A. Chytil, B. Bierie, M. Aakre, A.E. Gorska, and A.R. Sharif-Afshar 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. S. Biswas, A. Chytil, K. Washington, J. Romero-Gallo, A.E. Gorska, and P.S. Wirth Transforming growth factor beta receptor type II inactivation promotes the establishment and progression of colon cancer Cancer Res 64 2004 4687 4692
31. N.A. Bhowmick, A. Chytil, D. Plieth, A.E. Gorska, N. Dumont, and S. Shappell TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia Science 303 2004 848 851
32. M.O. Baffi, E. Slattery, P. Sohn, H.L. Moses, and A. Chytil Conditional deletion of the TGF-beta type II receptor in Col2a expressing cells results in defects in the axial skeleton without alterations in chondrocyte differentiation or embryonic development of long bones Dev Biol 276 2004 124 142
33. B.B. Cazac, and J. Roes TGF-beta receptor controls B cell responsiveness and induction of IgA in vivo Immunity 13 2000 443 451
34. A.B. Roberts, and M.B. Sporn Transforming growth factor-β R.A.F. Clark The molecular and cellular biology of wound repair 2nd ed. 1996 Plenum New York 275 308
35. A.B. Roberts, M.B. Sporn, R.K. Assoian, J.M. Smith, N.S. Roche, and L.M. Wakefield Transforming growth factor type beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro Proc Natl Acad Sci U S A 83 1986 4167 4171
36. H. Strobl Molecular mechanisms of dendritic cell sublineage development from human hematopoietic progenitor/stem cells Int Arch Allergy Immunol 131 2003 73 79
37. J.J. Letterio, and A.B. Roberts Regulation of immune responses by TGF-beta Annu Rev Immunol 16 1998 137 161
38. N.L. McCartney-Francis, M. Frazier-Jessen, and S.M. Wahl TGF-beta: a balancing act Int Rev Immunol 16 1998 553 580
39. R.J. Diebold, M.J. Eis, M. Yin, I. Ormsby, G.P. Boivin, and B.J. Darrow Early-onset multifocal inflammation in the transforming growth factor beta 1-null mouse is lymphocyte mediated Proc Natl Acad Sci U S A 92 1995 12215 12219
40. L. Yaswen, A.B. Kulkarni, T. Fredrickson, B. Mittleman, R. Schiffman, and S. Payne Autoimmune manifestations in the transforming growth factor-beta 1 knockout mouse Blood 87 1996 1439 1445
41. L. Gorelik, and R.A. Flavell Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease Immunity 12 2000 171 181
42. L. Gorelik, P.E. Fields, and R.A. Flavell Cutting edge: TGF-beta inhibits Th type 2 development through inhibition of GATA-3 expression J Immunol 165 2000 4773 4777
43. W. Chen, M.E. Frank, W. Jin, and S.M. Wahl TGF-beta released by apoptotic T cells contributes to an immunosuppressive milieu Immunity 14 2001 715 725
44. B.B. Cazac, and J. Roes TGF-beta receptor controls B cell responsiveness and induction of IgA in vivo Immunity 13 2000 443 451
45. M.B. Datto, J.P. Frederick, L. Pan, A.J. Borton, Y. Zhuang, and X.F. Wang Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction Mol Cell Biol 19 1999 2495 2504
46. X. Yang, J.J. Letterio, R.J. Lechleider, L. Chen, R. Hayman, and H. Gu Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-beta EMBO J 18 1999 1280 1291
47. A. Suzumura, M. Sawada, H. Yamamoto, and T. Marunouchi Transforming growth factor-beta suppresses activation and proliferation of microglia in vitro J Immunol 151 1993 2150 2158
48. P. Shrikant, S.J. Lee, I. Kalvakolanu, R.M. Ransohoff, and E.N. Benveniste Stimulus-specific inhibition of intracellular adhesion molecule-1 gene expression by TGF-beta J Immunol 157 1996 892 900
49. M.K. Winkler, and E.N. Beveniste Transforming growth factor-beta inhibition of cytokine-induced vascular cell adhesion molecule-1 expression in human astrocytes Glia 22 1998 171 179
50. J.J. Letterio, A.G. Geiser, A.B. Kulkarni, H. Dang, L. Kong, and T. Nakabayashi Autoimmunity associated with TGF-beta1-deficiency in mice is dependent on MHC class II antigen expression J Clin Invest 98 1996 2109 2119
51. W. Chen, and S.M. Wahl Manipulation of TGF-beta to control autoimmune and chronic inflammatory diseases Microbes Infect 1 1999 1367 1380
52. H. Cheon, S.J. Yu, D.H. Yoo, I.J. Chae, G.G. Song, and J. Sohn Increased expression of pro-inflammatory cytokines and metalloproteinase-1 by TGF-beta1 in synovial fibroblasts from rheumatoid arthritis and normal individuals Clin Exp Immunol 127 2002 547 552
53. D.R. Edwards, K.J. Leco, P.P. Beaudry, P.W. Atadja, C. Veillette, and K.T. Riabowol Differential effects of transforming growth factor-beta 1 on the expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in young and old human fibroblasts Exp Gerontol 31 1996 207 223
54. R.A. Fava, N.J. Olsen, A.E. Postlethwaite, K.N. Broadley, J.M. Davidson, and L.B. Nanney Transforming growth factor beta 1 (TGF-beta 1) induced neutrophil recruitment to synovial tissues: implications for TGF-beta-driven synovial inflammation and hyperplasia J Exp Med 173 5 1991 (May 1) 1121 1132
55. A. Kawakami, K. Eguchi, N. Matsuoka, M. Tsuboi, Y. Kawabe, and T. Aoyagi Inhibition of Fas antigen-mediated apoptosis of rheumatoid synovial cells in vitro by transforming growth factor beta 1 Arthritis Rheum 39 1996 1267 1276
56. B. Berse, J.A. Hunt, R.J. Diegel, P. Morganelli, K. Yeo, and F. Brown Hypoxia augments cytokine (transforming growth factor-beta (TGF-beta) and IL-1)-induced vascular endothelial growth factor secretion by human synovial fibroblasts Clin Exp Immunol 115 1999 176 182
57. C. Duvernelle, V. Freund, and N. Frossard Transforming growth factor-beta and its role in asthma Pulm Pharmacol Ther 16 2003 181 196
58. W. Chen, W. Jin, N. Hardegen, K.J. Lei, L. Li, and N. Marinos Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3 J Exp Med 198 2003 1875 1886
59. H.B. Park, D.J. Paik, E. Jang, S. Hong, and J. Youn Acquisition of anergic and suppressive activities in transforming growth factor-beta- costimulated CD4+CD25- T cells Int Immunol 16 2004 1203 1213
60. C. Schramm, S. Huber, M. Protschka, P. Czochra, J. Burg, and E. Schmitt TGFbeta regulates the CD4+CD25+ T-cell pool and the expression of Foxp3 in vivo Int Immunol 16 2004 1241 1249
61. J.C. Marie, J.J. Letterio, M. Gavin, and A.Y. Rudensky TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells J Exp Med 201 2005 1061 1067
62. L. Gorelik, and R.A. Flavell Transforming growth factor-beta in T-cell biology Nat Rev Immunol 2 2002 46 53
63. K. Nakamura, A. Kitani, I. Fuss, A. Pedersen, N. Harada, and H. Nawata TGF-beta 1 plays an important role in the mechanism of CD4+CD25+ regulatory T cell activity in both humans and mice J Immunol 172 2004 834 842
64. C.A. Piccirillo, J.J. Letterio, A.M. Thornton, R.S. McHugh, M. Mamura, and H. Mizuhara CD4(+)CD25(+) regulatory T cells can mediate suppressor function in the absence of transforming growth factor beta1 production and responsiveness J Exp Med 196 2002 237 246
65. J. Rogers, S. Webster, L.F. Lue, L. Brachova, W.H. Civin, and M. Emmerling Inflammation and Alzheimer's disease pathogenesis Neurobiol Aging 17 1996 681 686
66. E.K. Luedecking, S.T. DeKosky, H. Mehdi, M. Ganguli, and M.I. Kamboh Analysis of genetic polymorphisms in the transforming growth factor-beta1 gene and the risk of Alzheimer's disease Hum Genet 106 2000 565 569
67. C.C. Chao, T.A. Ala, S. Hu, K.B. Crossley, R.E. Sherman, and P.K. Peterson Serum cytokine levels in patients with Alzheimer's disease Clin Diagn Lab Immunol 1 1994 433 436
68. C.C. Chao, S. Hu, W.H. Frey II, T.A. Ala, W.W. Tourtellotte, and P.K. Peterson Transforming growth factor beta in Alzheimer's disease Clin Diagn Lab Immunol 1 1994 109 110
69. T. Wyss-Coray, E. Masliah, M. Mallory, L. McConlogue, K. Johnson-Wood, and C. Lin Amyloidogenic role of cytokine TGF-beta1 in transgenic mice and in Alzheimer's disease Nature 389 1997 603 606
70. E.A. van der Wal, F. Gomez-Pinilla, and C.W. Cotman Transforming growth factor-beta 1 is in plaques in Alzheimer and Down pathologies Neuroreport 4 1993 69 72
71. N.S. Peress, and E. Perillo Differential expression of TGF-beta 1, 2 and 3 isotypes in Alzheimer's disease: a comparative immunohistochemical study with cerebral infarction, aged human and mouse control brains J Neuropathol Exp Neurol 54 1995 802 811
72. K.C. Flanders, C.F. Lippa, T.W. Smith, D.A. Pollen, and M.B. Sporn Altered expression of transforming growth factor-beta in Alzheimer's disease Neurology 45 1995 1561 1569
73. S. Bodmer, M.B. Podlisny, D.J. Selkoe, I. Heid, and A. Fontana Transforming growth factor-beta bound to soluble derivatives of the beta amyloid precursor protein of Alzheimer's disease Biochem Biophys Res Commun 171 1990 890 897
74. S.A. Frautschy, F. Yang, L. Calderon, and G.M. Cole Rodent models of Alzheimer's disease: rat a beta infusion approaches to amyloid deposits Neurobiol Aging 17 1996 311 321
75. C.W. Gray, and A.J. Patel Regulation of beta-amyloid precursor protein isoform mRNAs by transforming growth factor-beta 1 and interleukin-1 beta in astrocytes Brain Res Mol Brain Res 19 1993 251 256
76. U. Monning, R. Sandbrink, R.B. Banati, C.L. Masters, and K. Beyreuther Transforming growth factor beta mediates increase of mature transmembrane amyloid precursor protein in microglial cells FEBS Lett 342 1994 267 272
77. S. Lesne, F. Docagne, C. Gabriel, G. Liot, D.K. Lahiri, and L. Buee Transforming growth factor-beta 1 potentiates amyloid-beta generation in astrocytes and in transgenic mice J Biol Chem 278 2003 18408 18418
78. J. Apelt, and R. Schliebs Beta-amyloid-induced glial expression of both pro- and anti-inflammatory cytokines in cerebral cortex of aged transgenic Tg2576 mice with Alzheimer plaque pathology Brain Res 894 2001 21 30
79. C.C. Chao, S. Hu, F.H. Kravitz, M. Tsang, W.R. Anderson, and P.K. Peterson Transforming growth factor-beta protects human neurons against beta-amyloid-induced injury Mol Chem Neuropathol 23 1994 159 178
80. J.H. Prehn, V.P. Bindokas, J. Jordan, M.F. Galindo, G.D. Ghadge, and R.P. Roos Protective effect of transforming growth factor-beta 1 on beta-amyloid neurotoxicity in rat hippocampal neurons Mol Pharmacol 49 1996 319 328
81. R.F. Ren, and K.C. Flanders Transforming growth factors-beta protect primary rat hippocampal neuronal cultures from degeneration induced by beta-amyloid peptide Brain Res 732 1996 16 24
82. T. Wyss-Coray, C. Lin, F. Yan, G.Q. Yu, M. Rohde, and L. McConlogue TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice Nat Med 7 2001 612 618
83. Y. Le, P.M. Murphy, and J.M. Wang Formyl-peptide receptors revisited Trends Immunol 23 2002 541 548
84. Y. Le, W. Gong, H.L. Tiffany, A. Tumanov, S. Nedospasov, and W. Shen Amyloid (beta)42 activates a G-protein-coupled chemoattractant receptor, FPR-like-1 J Neurosci 21 2001 RC123
85. H.L. Tiffany, M.C. Lavigne, Y.H. Cui, J.M. Wang, T.L. Leto, and J.L. Gao Amyloid-beta induces chemotaxis and oxidant stress by acting at formylpeptide receptor 2, a G protein-coupled receptor expressed in phagocytes and brain J Biol Chem 276 2001 23645 23652
86. H. Yazawa, Z.X. Yu, Takeda, Y. Le, W. Gong, and V.J. Ferrans Beta amyloid peptide (Abeta42) is internalized via the G-protein-coupled receptor FPRL1 and forms fibrillar aggregates in macrophages FASEB J 15 2001 2454 2462
87. G. Ying, P. Iribarren, Y. Zhou, W. Gong, N. Zhang, and Z.X. Yu Humanin, a newly identified neuroprotective factor, uses the G protein-coupled formylpeptide receptor-like-1 as a functional receptor J Immunol 172 2004 7078 7085
88. Y.H. Cui, Y. Le, W. Gong, P. Proost, J. Van Damme, and W.J. Murphy Bacterial lipopolysaccharide selectively up-regulates the function of the chemotactic peptide receptor formyl peptide receptor 2 in murine microglial cells J Immunol 168 2002 434 442
89. Y.H. Cui, Y. Le, X. Zhang, W. Gong, K. Abe, and R. Sun Up-regulation of FPR2, a chemotactic receptor for amyloid beta 1-42 (A beta 42), in murine microglial cells by TNF alpha Neurobiol Dis 10 2002 366 377
90. S. Olschwang, R. Hamelin, P. Laurent-Puig, B. Thuille, Y. De Rycke, and Y.J. Li Alternative genetic pathways in colorectal carcinogenesis Proc Natl Acad Sci U S A 94 1997 12122 12127
91. P. Tannergard, T. Liu, A. Weger, M. Nordenskjold, and A. Lindblom Tumorigenesis in colorectal tumors from patients with hereditary non-polyposis colorectal cancer Hum Genet 101 1997 51 55
92. W.M. Grady, L.L. Myeroff, S.E. Swinler, A. Rajput, S. Thiagalingam, and J.D. Lutterbaugh Mutational inactivation of transforming growth factor receptor type II in microsatellite stable colon cancers Cancer Res 59 1999 320 324
93. S. Markowitz, J. Wang, L. Myeroff, R. Parsons, L. Sun, and J. Lutterbaugh Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability Science 268 1995 1336 1338
94. S.A. Hahn, M. Schutte, A.T. Hoque, C.A. Moskaluk, L.T. da Costa, and E. Rozenblum DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1 Science 271 1996 350 353
95. M. Miyaki, T. Iijima, M. Konishi, K. Sakai, A. Ishii, and M. Yasuno Higher frequency of Smad4 gene mutation in human colorectal cancer with distant metastasis Oncogene 18 1999 3098 3103
96. B. Tang, E.P. Bottinger, S.B. Jakowlew, K.M. Bagnall, J. Mariano, and M.R. Anver Transforming growth factor-beta1 is a new form of tumor suppressor with true haploid insufficiency Nat Med 4 1998 802 807
97. B. Pasche, P. Kolachana, K. Nafa, J. Satagopan, Y.G. Chen, and R.S. Lo TbetaR-I(6A) is a candidate tumor susceptibility allele Cancer Res 59 1999 5678 5682
98. K.S. Shim, K.H. Kim, W.S. Han, and E.B. Park Elevated serum levels of transforming growth factor-1 in patients with colorectal carcinoma: its association with tumor progression and its significant decrease after curative surgical resection Cancer 85 1999 554 561
99. P.J. Lu, Q.L. Lu, A. Rughetti, and J. Taylor-Papadimitriou bcl-2 overexpression inhibits cell death and promotes the morphogenesis, but not tumorigenesis of human mammary epithelial cells J Cell Biol 129 1995 1363 1378
100. G. Portella, S.A. Cumming, J. Liddell, W. Cui, H. Ireland, and R.J. Akhurst Transforming growth factor beta is essential for spindle cell conversion of mouse skin carcinoma in vivo: implications for tumor invasion Cell Growth Differ 9 1998 393 404
101. W. Cui, D.J. Fowlis, S. Bryson, E. Duffie, H. Ireland, and A. Balmain TGF 1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice Cell 86 1996 531 542
102. M. Oft, J. Peli, C. Rudaz, H. Schwarz, H. Beug, and E. Reichmann TGF-1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells Genes Dev 10 1996 2462 2477
103. W. Chen, and S.M. Wahl Manipulation of TGF-beta to control autoimmune and chronic inflammatory diseases Microbes Infect 1 1999 1367 1380