Transforming growth factor-β: The breaking open of a black box

BioEssays

Volumn 19, Issue 7, 1997, Pages 581-591

  Alevizopoulos, Athanassios ^a   Mermod, Nicolas ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; VERTEBRATA;

EID: 0030849889     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.950190709     Document Type: Review

References (93)

1. Roberts, A. B., Anzano, M. A., Lamb, L. C., Smith, J. M. and Sporn, M. B. (1981). New class of Transforming Growth Factors potentiated by Epidermal Growth Factor. Proc. Natl Acad. Sci. USA 78, 5339-5343.
2. Massagué, J. (1990). The Transforming Growth Factor-β family. Annu. Rev. Cell Biol. 6, 597-641.
3. Moses, H. L. and Serra, R. (1996). Regulation of differentiation by TGF-β. Curr. Opin. Gen. Dev. 6, 581-586.
4. Massagué, J., Attisano, L. and Wrana, J. L. (1994). The TGF-β family and its composite receptors. Trends Cell Biol. 4, 172-178.
5. McCartney-Francis, N. L. and Wahl, S. M. (1994) Transforming Growth Factor β: a matter of life and death. J. Leukoc. Biol. 55, 401-409.
6. Cheifetz, S., Like, B. and Massagué, J. (1986). Cellular distribution of type I and type II receptors for Transforming Growth Factor-β. J. Biol. Chem. 261, 9972-9978.
7. Lin, H. Y., Wang, X.-F., Ng-Eaton, E., Weinberg, R. A. and Lodish, H. F. (1992). Expression cloning of the TGF-β type II receptor, a functional transmembrane serine/threonine kinase. Cell 68, 775-785.
8. Franzén, P. et al. (1993). Cloning of a TGFβ type I receptor that forms a heteromeric complex with the TGFβ type II receptor. Cell 75, 681-692.
9. Bassing, C. H. et al. (1994). A Transforming Growth Factor β type I receptor that signals to activate gene expression. Science 263, 87-89.
10. ten Dijke, P., Miyazono, K. and Heldin, C.-H. (1996). Signaling via heterooligomeric complexes of type I and type II serine/threonine kinase receptors. Curr. Opin. Cell. Biol. 8, 139-145.
11. Derynck, R. (1994). TGF-β-receptor mediated signaling. Trends Biochem. Sci. 19, 548-553.
12. Laiho, M., Weis, F. M. B. and Massagué, J. (1990). Concomitant loss of Transforming Growth Factor (TGF)-β receptor types I and II in TGF-β-resistant cell mutants implicates both receptor types in signal transduction. J. Biol. Chem. 265, 18518-18524.
13. Wrana, J. L. et al. (1992). TGFβ signals through a heteromeric protein kinase receptor complex. Cell 71, 1003-1014.
14. Laiho, M., Weis, F. M. B., Boyd, F. T., Ignotz, R. A. and Massagué, J. (1990). Responsiveness to Transforming Growth Factor-β (TGF)-β restored by genetic complementation between cells defective in TGF-β receptors I and II. J. Biol. Chem. 266, 9108-9112.
15. Anders, R. A. and Leof, E. B. (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.
16. Weis-Garcia, F. and Massagué, J. (1996). Complementation between kinase-defective and activation-defective TGF-β receptors reveals a novel form of receptor cooperativity essential for signaling. EMBO J. 15, 276-289.
17. Wrana, J. L., Attisano, L., Wieser, R., Ventura, F. and Massagué, J. (1994). Mechanism of activation of the TGFβ receptor. Nature 370, 341-347.
18. ten Dijke, P. et al. (1994). Characterization of type I receptors for Transforming Growth Factor β and activin. Science 264, 101-104.
19. Attisano, L., Carcámo, J., Ventura, F., Weis, F. M. B., Massagué, J. and Wrana, J. L. (1993). Identification of human activin and TGFβ type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75, 671-680.
20. Pietenpol, J. A. et al. (1990). TGF-β1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains. Cell 61, 777-785.
21. Barlat, I. et al. (1995). TGF-β1 and cAMP attenuate cyclin A gene transcription via a cAMP responsive element through independent pathways. Oncogens 11, 1309-1318.
22. Hannon, G. J. and Beach, D. (1994). p15/INK4B is a potential effector of the TGFβ-induced cell cycle arrest. Nature 371, 257-261.
23. Datto, M. B., Yu, Y. and Wang, X.-F. (1995). Functional analysis of the Transforming Growth Factor β responsive elements in the WAF1/CIP1/p21 promoter. J. Biol. Chem. 270, 28623-28628.
24. Pertovaara, L., Sistonen, L., Bos, T. J., Vogt, P. K., Keski-Oja, J. and Alitalo, K. (1989). Enhanced jun expression is an early genomic response to Transforming Growth Factor β stimulation. Mol. Cell. Biol. 9, 1255-1262.
25. Li, L., Hu, J.-S. and Olson, E. N. (1990). Different members of the jun protooncogene family exhibit distinct patterns of expression in response to type β Transforming Growth Factor. J. Biol. Chem. 265, 1556-1562.
26. Bascom, C. C. et al. (1989). Complex regulation of Transforming Growth Factor β1, β2, and β3 mRNA expression in mouse fibroblasts and keratinocytes by Transforming Growth Factor β1 and β2. Mol. Cell. Biol. 9, 5508-5515.
27. Lastres, P. et al. (1996). Endoglin modulates cellular responses to TGF-β1. J. Cell. Biol. 133, 1109-1121.
28. Turner, M., Chantry, D., Katsikis, P., Berger, A., Brennan, F. M. and Feldmann, M. (1991). Induction of the Interleukin 1 receptor antagonist protein by Transforming Growth Factor-β. Eur. J. Immun. 21, 1635-1639.
29. Hou, X., Johnson, A. C. and Rosner, M. R. (1994) Induction of Epidermal Growth Factor receptor gene transcription by Transforming Growth Factor β1: association with loss of protein binding to a negative regulatory element. Cell Growth Differ. 5, 801-809.
30. Rossi, P. et al. (1988). A Nuclear Factor 1 binding site mediates the transcriptional activation of a type I collagen promoter by Transforming Growth Factor-β. Cell 52, 405-414.
31. Inagaki, Y., Truter, S. and Ramirez, F. (1994). Transforming Growth Factor-β stimulates α2(I) collagen gene expression through a cis-acting element that contains an Sp1-binding site. J. Biol. Chem. 269, 14828-14834.
32. Riccio, A., Pedone, P. V., Rund, L. R., Olesen, T., Olsen, H. S. and Andreasen, P. A. (1992). Transforming Growth Factor β1-responsive element: closely associated binding sites for USF and CCAAT-binding transcription factor-Nuclear Factor I in the type 1 plasminogen activator inhibitor gene. Mol. Cell. Biol. 12, 1846-1855.
33. Kim, S.-J. et al. (1990). Autoinduction of Transforming Growth Factor β1 is mediated by the AP-1 complex. Mol. Cell. Biol. 10, 1492-1497.
34. Chung, K.-Y., Agarwal, A., Uitto, J. and Mauviel, A. (1996). An AP-1 binding sequence is essential for the regulation of the human α2(I) collagen (COLIA2) promoter activity by Transforming Growth Factor-β. J. Biol. Chem. 271, 3272-3278.
35. MacLellan, W. R., Lee, T.-C., Schwartz, R. J. and Schneider, M. D. (1994). Transforming Growth Factor-β response elements of the skeletal α-actin gene. J. Biol. Chem. 269, 16754-16760.
36. Chen, X., Rubock, M. J. and Whitman, M. (1996). A transcriptional partner for MAD proteins in TGF-β signalling. Nature 383, 691-696.
37. Kerr, L. D., Miller, D. B. and Matrisian, L. M. (1990). TGF-β1 inhibition of transin/stromelysin gene expression is mediated through a FOS binding sequence. Cell 61, 267-278.
38. Brabletz, T., Pfeuffer, I., Schorr, E., Siebelt, F., Wirth, T. and Serfling, E. (1993). Transforming Growth Factor-β and cyclosporin A inhibit the inducible activity of the interleukin-2 gene in T cells through a noncanonical octamer binding site. Mol. Cell. Biol. 13, 1155-1162.
39. Chen, Y., Takeshita, A., Ozaki, K., Kitano, S. and Hanazawa, S. (1996). Transcriptional regulation by Transforming Growth Factor β of the expression of retinoic acid and retinoic X receptor genes in osteoblastic cells is mediated by AP-1. J. Biol. Chem. 271, 31602-31606.
40. Kramer, I. M., Koornneef, I., de Laat, S. W. and van den Eijnden-van Raaij A. J. M. (1991). TGF-β1 induces phosphorylation of the cyclic AMP responsive element binding protein in ML-CC164 cells. EMBO J. 10, 1083-1089.
41. Alevizopoulos, A., Dusserre, Y., Tsai-Plugfelder, M., von der Weid, T., Wahli, W. and Mermod, N. (1995). A proline-rich TGF-β transcriptional activator interacts with histone H3. Genes Dev. 9, 3051-3066.
42. Alevizopoulos, A. and Mermod, N. (1996). Antagonistic regulation of a proline-rich transcription factor by Transforming Growth factor β and Tumor Necrosis Factor α. J. Biol. Chem. 271, 29672-29681.
43. Kähäri, V.-M., Chen, Y. Q., Su, M. W., Ramirez, F. and Uitto, J. (1990). Tumour Necrosis Factor-α and Interferon-γ suppress the activation of human type I collagen gene expression by Transforming Growth Factor-β1. J. Clin. Invest. 86, 1489-1495.
44. Sekelsky, J. J., Newfeld, S. J., Raftery, L. A., Chartoff, E. H. and Gelbart, W. M. (1995). Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139, 1347-1358.
45. Savage, C. et al. (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.
46. Hahn, S. A. et al. (1996). DPC4, a candidate tumor supressor gene at human chromosome 18q21.1. Science 271, 350-353.
47. Derynck, R. et al. (1996). Nomeclature: vertebrate mediators of TGFβ family signals. Cell 87, 173.
48. Graft, J. M., Bansal, A. and Melton, D. A. (1996). Xenopus Mad proteins transduce distinct subsets of signals for the TGFβ superfamily. Cell 85, 479-487.
49. Hoodless, P. A. et al. (1996). MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500.
50. Liu, F. et al. (1996). A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381, 620-623.
51. Yingling, J. M., Das, P., Savage, C., Zhang, M., Padgett, R. W. and Wang, X.-F. (1996). Mammalian dwarfins are phosphorylated in response to Transforming Growth Factor β and are implicated in the control of cell growth. Proc. Natl Acad. Sci. USA 93, 8940-8944.
52. Macías-Silva, M. et al. (1996). MADR2 is a substrate of the TGFβ receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 87, 1215-1224.
53. Zhang, Y., Feng, X.-H., Wu, R.-Y. and Derynck, R. (1996). Receptor-associated MAD homologues synergize as effectors of the TGF-β response. Nature 383, 168-172.
54. Lagna, G., Hata, A., Hemmati-Brivanlou, A. and Massagué, J. (1996). Partnership between DPC4 and Smad proteins in TGF-β signaling pathways. Nature 383, 832-836.
55. Zhang, Y., Musci, T. and Derynck, R. (1997). The tumor suppressor Smad4/DPC4 as a central mediator of Smad function. Curr. Biol. 7, 270-276.
56. Reddy, K. B., Karode, M. C., Harmony, J. A. K. and Howe, P. H. (1996). Interaction of transforming growth factor β receptors with apolipoprotein J/clusterin. Biochemistry 35, 309-314.
57. Chen, R.-H., Miettinen, P. J., Maruoka, E. M., Choy, L. and Derynck, R. (1995). A WD-domain protein that is associated with and phosphorylated by the type II TGF-β receptor. Nature 377, 548-552.
58. Wang, T. et al. (1996). The immunophilin FKBP12 functions as a common inhibitor of the TGFβ family type I receptors. Cell 86, 435-444.
59. Okadome, T. et al. (1996). Characterization of the interaction of FKBP12 with the Transforming Growth Factor-β receptor in vivo. J. Biol. Chem. 271, 21687-21690.
60. Charng, M.-J., Kinnunen, P., Hawker, J., Brand, T. and Schneider, M. D. (1996). FKBP-12 recognition is dispensable for signal generation by type I Transforming Growth Factor-β receptors. J. Biol. Chem. 271, 22941-22944.
61. Ishiyama, N. et al. (1996). Calcium as the second messenger of the action of Transforming Growth Factor-β on insulin secretion. Mol. Cell. Endocrinol. 117, 1-6.
62. 2+ channel that is regulated by TGF-β. Science 257, 91-94.
63. Ventura, F., Liu, F., Doody, J. and Massagué, J. (1996) Interaction of Transforming Growth Factor-β receptor I with farnesyl-protein transferase-α in yeast and mammalian cells. J. Biol. Chem. 271, 13931-13934.
64. McAnultry, R. J., Chambers, R. C. and Laurent, G. J. (1995) Regulation of fibroblast procollagen production: Transforming Growth Factor-β1 induces prostaglandin E2 synthesis via a pertussis toxin-sensitive G protein. Biochem. J. 307, 63-68.
65. ras by Transforming Growth Factor β in epithelial cells. J. Biol. Chem. 267, 5029-5031.
66. Atfi, A., Djelloul, S., Chastre, E., Davis, R. and Gesprach, C. (1997). Evidence for a role of Rho-like GTPases and stress-activated protein kinase/c-Jun N-terminal kinase (SAPK/JNK) in Transforming Growth Factor β-mediated signaling. J. Biol. Chem. 272, 1429-1432.
67. Moriguchi, T. et al. (1996). A novel kinase cascade mediated by mitogen-activated protein kinase kinase 6 and MKK3. J. Biol. Chem. 271, 13675-13679.
68. Yamaguchi, K. et al. (1995). Identification of a member of the MAPKKK family as a potential mediator of TGF-β signal transduction. Science 270, 2008-2001.
69. Howe, P. H., Dobrowolski, S. F., Reddy, K. B. and Stacey, D. W. (1993). Release from G1 growth arrest by Transforming Growth Factor β requires cellular Ras activity. J. Biol. Chem. 268, 21448-21452.
70. Seifert, R. A., Coats, S. A., Raines, E. W., Ross, R. and Bowen-Pope, D. F. (1994). Platelet-derived growth factor (PDGF) receptor-α subunit mutant and reconstituted cell lines demonstrate that Transforming Growth Factor-β can be mitogenic through PDGF-A-chain-dependent and -independent pathways. J. Biol. Chem. 269, 13951-13955.
71. Ravitz, M. J., Yan, S., Herr, K. D. and Wenner, C. E. (1995). Transforming Growth Factor-β-induced activation of cyclin E-cdk2 kinase and down-regulation of p27/Kip1 in C3H10T1/2 mouse fibroblasts. Cancer Res. 55, 1413-1416.
72. Laiho, M., Decaprio, J. A., Ludlow, J. W., Livingston, D. M. and Massagué, J. (1990). Growth inhibition by TGF-β linked to suppression of retinoblastoma protein phosphorylation. Cell 62, 175-185.
73. Ewen, M. E., Sluss, H. K., Whitehouse, L. L. and Livingston, D. M. (1993). TGFβ inhibition of Cdk4 synthesis is linked to cell cycle arrest. Cell 74, 1009-1020.
74. Geng, Y. and Weinberg, R. A. (1993). Transforming Growth Factor β effects on expression of G1 cyclins and cyclin-dependent protein kinases. Procl. Natl Acad. Sci. USA 90, 10135-10139.
75. Polyak, K. et al. (1994). p27/Kip1, a cyclin-Cdk inhibitor, links Transforming Growth Factor-β and contact inhibition to cell cycle arrest. Genes Dev. 8, 9-22.
76. Nakayama, K. et al. (1996). Mice lacking p27/Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia and pituitary tumors. Cell 85, 707-720.
77. Reynisdóttir, I. and Massagué, J. (1997). The subcellular locations of p15/Ink4b and p27/Kip1 coordinate their inhibitory interactions with cdk4 and cdk2. Genes Dev. 11, 492-503.
78. Fan, G., Ma, X., Kren, B. T. and Steer, C. J. (1996). The retinoblastoma gene product inhibits TGF-β1 induced apoptosis in primary rat hepatocytes and human HuH-7 hepatoma cells. Oncogene 12, 1909-1919.
79. Li, C.-Y., Suardet, L. and Little, J. B. (1995). Potential role of Waf1/CIP1/p21 as a mediator of TGF-β cytoinhibitory effect. J. Biol. Chem. 270, 4971-4974.
80. Laiho, M. et al. (1991). Control of JunB and extracellular matrix protein expression by Transforming Growth Factor-β1 is independent of Simian Virus 40 T antigen-sensitive growth-inhibitory events. Mol. Cell. Biol. 11, 972-978.
81. Markowitz, S. D. and Roberts, A. B. (1996). Tumor suppressor activity of the TGF-β pathway in human cancers. Cyto. Growth Factor Rev. 7, 93-102.
82. Cui, W. et al. (1996). TGF-β1 inhibits the formation of benign skin tumors but enhances progression to invasive spindle carcinomas in transgenic mice. Cell 86, 531-542.
83. Knabbe, C. et al. (1987). Evidence that TGFβ is a hormonally regulated negative growth factor in human breast cancer cells. Cell 48, 417-428.
84. Pierce, D. F. J. et al. (1995). Mammary tumor suppression by Transforming Growth Factor β1 transgene expression. Proc. Natl Acad. Sci. USA 92, 4254-4258.
85. Kimchi, A., Wang, X.-F., Weinberg, R. A., Cheifetz, S. and Massagué, J. (1988). Absence of TGF-β receptors and growth inhibitory responses in retinoblastoma cells. Science 240, 196-199.
86. Markowitz, S. et al. (1995). Inactivation of the type II TGFβ receptor in colon cancer cells with microsatellite instability. Science 268, 1336-1338.
87. Eppert, K. et al. (1996). MADR2 maps to 18q21 and encodes a TGFβ-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86, 543-552.
88. Border, W. A. and Noble, N. A. (1995). Targeting TGF-β for treatment of disease. Nature Medicine 1, 1000-1001.
89. Sporn, M. B. and Roberts, A. B. (1992). Transforming Growth Factor-β: recent progress and new challenges. J. Cell Biol. 119, 1017-1021.
90. Atfi, A., Drobetsky, E., Boissonneault, M., Chapdelaine, A. and Chevalier, S. (1994). Transforming Growth Factor β downregulates src family protein tyrosine kinase signaling pathways. J. Biol. Chem. 269, 30688-30693.
91. Halstead, J., Kemp, K. and Ignotz, R. A. (1995) Evidence for involvement of phosphatidylcholine-phospholipase C and protein kinase C in Transforming Growth Factor-β signaling. J. Biol. Chem. 270, 13600-13603.
92. Bang, O.-S., Ruscetti, F. W., Lee, M.-H., Kim, S.-J. and Birchenall-Roberts, M. C. (1996). Transforming Growth Factor-β1 modulates p107 function in myeloid cells. J. Biol. Chem. 271, 7811-7819.
93. Herzinger, T., Wolf, D. A., Eick, D. and Kind, P. (1995). The Rb-related protein p130 is a possible effector of Transforming Growth Factor β1 induced cell cycle arrest in keratinocytes. Oncogene 10, 2079-2084.