Thrombospondin-1 is a major activator of TGF-β1 in vivo

Cell

Volumn 93, Issue 7, 1998, Pages 1159-1170

  Crawford, Susan E ^a,b   Stellmach, Veronica ^a   Murphy Ullrich, Joanne E ^c   Ribeiro, Solange M F ^c   Lawler, Jack ^d   Hynes, Richard O ^e   Boivin, Gregory P ^f   Bouck, Noël ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b CHILDREN'S MEMORIAL HOSPITAL   (United States)

^c University of Alabama at Birmingham   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HISTOPATHOLOGY; HYPERPLASIA; IMMUNOPATHOLOGY; LUNG DISEASE; MOUSE; NONHUMAN; PANCREAS DISEASE; PRIORITY JOURNAL;

EID: 12344320716     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81460-9     Document Type: Article

References (72)

1. Abe, M., Harpel, J.G., Metz, C.N., Nunes, I., Loskutoff, D.J., and Rifkin, D.B. (1994). An assay for transforming growth factor-β using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal. Biochem. 216, 276-284.
2. Abe, M., Oda, N., and Sato, Y. (1998). Cell-associated activation of latent transforming growth factor-β by calpain. J. Cell. Physiol. 174, 186-193.
3. Barcellos-Hoff, M.H., and Dix, T.A. (1996). Redox-mediated activation of latent transforming growth factor β-1. Mol. Endocrinol. 10, 1077-1083.
4. Barnard, J.A., Lyons, R.M., and Moses, H.L. (1990). The cell biology of transforming growth factor β. Biochim. Biophys. Acta 1032, 79-87.
5. Barral-Netto, M., Barral, A., Brownell, C.E., Skeiky, Y.A., Ellingsworth, L.R., Twardzik, D.R., and Reed, S.G. (1992). Transforming growth factor-β in leishmanial infection: a parasite escape mechanism. Science 257, 545-548.
6. Boivin, G.P., O'Toole, B.A., Ormsby, I.E., Diebold, R.J., Eis, M.J., Doetschman, T., and Kier, A.B. (1995). Onset and progression of pathological lesions in transforming growth factor-β1-deficient mice. Am. J. Pathol. 146, 276-288.
7. Border, W.A., and Ruoslahti, E. (1992). Transforming growth factor-β in disease: the dark side of tissue repair. J. Clin. Invest. 90, 1-7.
8. Bornstein, P. (1995). Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J. Cell Biol. 130, 503-506.
9. Bottinger, E.P., Factor, V.M., Tsang, M.L.-S., Weatherbee, J.A., Kopp, J.B., Qian, S.W., Wakefield, L.M., Roberts, A.B., Thorgeirsson, S.S., and Sporn, M.B. (1996). The recombinant proregion of transforming growth factor β1 (latency-associated peptide) inhibits active transforming growth factor β1 in transgenic mice. Proc. Natl. Acad. Sci. USA 93, 5877-5882.
10. Brown, P.D., Wakefield, L.M., Levinson, A.D., and Sporn, M.B. (1990). Physicochemical activation of recombinant latent transforming growth factor β's 1, 2, and 3. Growth Factors 3, 35-43.
11. Bugge, T.H., Kombrinck, K.W., Flick, M.J., Daugherty, C.C., Danton, M.J., and Degen, J.L. (1996). Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell 87, 709-719.
12. Caver, T.E., O'Sullivan, F.X., Gold, L.I., and Gresham, H.D. (1996). Intracellular demonstration of active TGF-β1 in B cells and plasma cells of autoimmune mice. IgG bound TGF-β1 suppresses neutrophil function and host defense against staphylococcus aureus infection. J. Clin. Invest. 98, 2496-2506.
13. Dawson, D.W., and Bouck, N. (1998). Thrombospondin as an inhibitor of angiogenesis. In Angiogenic Agents, B.A. Teicher, ed. (Totowa, NJ: Humana Press), in press.
14. Dawson, D.W., Pearce, S.F., Zhong, R., Silverstein, R.L., Frazier, W.A., and Bouck, N.P. (1997). CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol. 138, 707-717.
15. De Bleser, P.J., Scott, C.D., Niki, T., Xu, G., Wisse, E., and Geerts, A. (1996). Insulin-like growth factor II/mannose 6-phosphate-receptor expression in liver and serum during acute CCI4 intoxication in the rat. Hepatology 23, 1530-1537.
16. Diebold, R.J., Eis, M.J., Yin, M., Ormsby, I., Boivin, G.P., Darrow, B.J., Saffitz, J.E., and Doetschman, T. (1995). Early-onset multifocal inflammation in the transforming growth factor β1-null mouse is lymphocyte mediated. Proc. Natl. Acad. Sci. USA 92, 12215-12219.
17. Ehrhart, E.J., Segarini, P., Tsang, M.L.-S., Carroll, A.G., and Barcellos-Hoff, M.H. (1997). Latent transforming growth factor B1 activation in situ: quantitative and functional evidence after low-dose γ-irradiation. FASEB J. 11, 991-1002.
18. Gentry, L.E., Webb, N.R., Lim, G.J., Brunner, A.M., Ranchalis, J.E., Twardzik, D.R., Lioubin, M.N., Marquardt, H., and Purchio, A.F. (1987). Type 1 transforming growth factor β: amplified expression and secretion of mature and precursor polypeptides in Chinese hamster ovary cells. Mol. Cell Biol. 7, 3418-3427.
19. Grainger, D.J., Kemp, P.R., Liu, A.C., Lawn, R.M., and Metcalfe, J.C. (1994). Activation of transforming growth factor-β is inhibited in transgenic apolipoprotein(a) mice. Nature 370, 460-462.
20. Jetten, A.M., Shirley, J.E., and Stoner, G. (1986). Regulation of proliferation and differentiation of respiratory tract epithelial cells by TGF β. Exp. Cell Res. 167, 539-549.
21. Jirtle, R.L., Carr, B.I., and Scott, C.D. (1991). Modulation of insulin-like growth factor-II/mannose 6-phosphate receptors and transforming growth factor-β1 during liver regeneration. J. Biol. Chem. 266, 22444-22450.
22. Kaartinen, V., Voncken, J.W., Shuler, C., Warburton, D., Bu, D., Heisterkamp, N., and Groffen, J. (1995). Abnormal lung development and cleft palate in mice lacking TGF-β3 indicates defects of epithelial-mesenchymal interaction. Nat. Genet. 11, 415-420.
23. Kojima, S., and Rifkin, D.B. (1993). Mechanism of retinoid-induced activation of latent transforming growth factor-β in bovine endothelial cells. J. Cell. Physiol. 155, 323-332.
24. Kulkarni, A.B., Huh, C.-G., Becker, D., Geiser, A., Lyght, M., Flanders, K.C., Roberts, A.B., Sporn, M.B., Ward, J.M., and Karlsson, S. (1993). Transforming growth factor β1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. USA 90, 770-774.
25. Lahav, J. (1993). The functions of thrombospondin and its involvement in physiology and pathophysiology. Biochim. Biophys. Acta 1182, 1-14.
26. Laiho, M., Ronnstrand, L., Heino, J., DeCaprio, J.A., Ludlow, J.W., Livingston, D.M., and Massague, J. (1991). Control of JunB and extracellular matrix protein expression by transforming growth factor-β1 is independent of simian virus 40 T antigen-sensitive growth-sensitive growth-inhibitory events. Mol. Cell. Biol. 11, 972-978.
27. Lawler, J., Sunday, M., Thibert, V., Duquette, M., George, E.L., Rayburn, H., and Hynes, R.O. (1998). Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia. J. Clin. Invest. 101, 982-992.
28. Lawrence, D.A. (1996). Transforming growth factor-β: a general review. Eur. Cytokine Netw. 7, 363-374.
29. Letterio, J.J., and Roberts, A.B. (1996). Transforming growth factor-β1-deficient mice: identification of isoform-specific activities in vivo. J. Leukoc. Biol. 59, 769-774.
30. Letterio, J.J., Geiser, A.G., Kulkarni, A.B., Roche, N.S., Sporn, M.B., and Roberts, A.B. (1994). Maternal rescue of transforming growth factor-β1 null mice. Science 264, 1936-1938.
31. Lioubin, M.N., Madisen, L., Marquardt, H., Roth, R., Kovacina, K.S., Purchio, A.F. (1991). Characterization of latent recombinant TGF-β2 produced by Chinese hamster ovary cells. J. Cell. Biochem. 45, 112-121.
32. Lyons, R.M., Gentry, L.E., Purchio, A.F., and Moses, H.L. (1990). Mechanism of activation of latent recombinant transforming growth factor β1 by plasmin. J. Cell Biol. 110, 1361-1367.
33. Majack, R.A. (1987). β-type transforming growth factor specifies organizational behavior in vascular smooth muscle cell cultures. J. Cell Biol. 105, 465-471.
34. Majack, R.A., Cook, S.C., and Bornstein, P. (1986). Control of smooth cell growth by components of the extracellular matrix: autorole for thrombospondin. Proc. Natl. Acad. Sci. USA 83, 9050-.
35. Majack, R.A., Majesky, M.W., and Goodman, L.V. (1990). Role of PDGF-A expression in the control of vascular smooth muscle cell by transforming growth factor-β. J. Cell Biol. 111, 239-247.
36. Markowitz, S.D., and Roberts, A.B. (1996). Tumor suppressor activity the TGF-β pathway in human cancers. Cytokine Growth Factor Rev. 7, 93-102.
37. Massague, J. (1990). The transforming growth factor-β family. Annu. . Cell Biol. 6, 597-641.
38. Masui, T., Wakefield, L.M., Lechner, J.F., LaVeck, M.A., Sporn, M.B., Harris, C.C. (1986). Type β transforming growth factor is the differentiation-inducing serum factor for normal human epithelial cells. Proc. Natl. Acad. Sci. USA 83, 2438-2442.
39. McCartney-Francis, N.L., and Wahl, S.M. (1994). Transforming factor β: a matter of life and death. J. Leukoc. Biol. 55, 401-409.
40. McMahon, G.A., Dignam, J.D., and Gentry, L.E. (1996). Structural of the latent complex between transforming growth β1 and β1-latency-associated peptide. Biochem. J. 313, 343-351.
41. Merwin, J.R., Newman, W., Beall, L.D., Tucker, A., and Madri, J. ). Vascular cells respond differentially to transforming growth β1 and β2 in vitro. Am. J. Pathol. 138, 37-51.
42. Miyazono, K., and Heldin, C.-H. (1991). Latent forms of TGF-β: mostructure and mechanisms of activation. Ciba Found. Symp. 157, 81-89.
43. Moses, H.L., and Serra, R. (1996). Regulation of differentiation by TGF-β. Curr. Opin. Genet. Dev. 6, 581-586.
44. Moses, H.L., Branum, E.L., Proper, J.A., and Robinson, R.A. (1981). Transforming growth factor production by chemically transformed cells. Cancer Res. 41, 2842-2848.
45. Moskaluk, C.A., and Kern, S.E. (1996). Cancer gets Mad: DPC4 and other TGFβ pathway genes in human cancer. Biochim. Biophys. Acta 1288, M31-M33.
46. Munger, J.S., Harpel, J.G., Gleizes, P.-E., Mazzieri, R., Nunes, I., and Rifkin, D.B. (1997). Latent transforming growth factor-β: structural features and mechanisms of activation. Kidney Int. 51, 1376-1382.
47. Murphy-Ullrich, J.E., Schultz-Cherry, S., and Hook, M. (1992). Transgrowth factor-β complexes with thrombospondin. Mol. Biol. Cell 3, 181-188.
48. Nunes, I., Gleizes, P.-E., Metz, C.N., and Rifkin, D.B. (1997). Latent transforming growth factor-β binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-β. J. Cell Biol. 136, 1151-1163.
49. Penttinen, R.P., Kobayashi, S., and Bornstein, P. (1988). Transgrowth factor β increases mRNA for matrix proteins both in the presence and in the absence of changes in mRNA stability. Proc. Natl. Acad. Sci. USA 85, 1105-1108.
50. Proetzel, G., Pawlowski, S.A., Wiles, M.V., Yin, M., Boivin, G.P., Howles, P.N., Ding, J., Ferguson, M.W., and Doetschman, T. (1995). Transforming growth factor-β3 is required for secondary palate fu. Nature Genet. 11, 409-419.
51. RayChaudhury, A., Frazier, W.A., and D'Amore, P.A. (1994). Comparof normal and tumorigenic endothelial cells: differences in thrombospondin production and responses to transforming growth factor-β. J. Cell Sci. 107, 39-46.
52. Roberts, A.B., and Sporn, M.B. (1988). Transforming growth factor β. Adv. Cancer Res. 51, 107-145.
53. 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: isolation from non-neoplastic tissues. Proc. Natl. Acad. Sci. USA 78, 5339-5343.
54. Sanford, L.P., Ormsby, I., Gittenberger-de Groot, A.C., Sariola, H., Friedman, R., Boivin, G.P., Cardell, E.L., and Doetschman, T. (1997). TGFβ2 knockout mice have multiple developmental defects that are non-overlapping with other TGFβ knockout phenotypes. Development 124, 2659-2670.
55. Sanvito, F., Herrera, P.L., Huarte, J., Nichols, A., Montesano, R., Orci, L., and Vassalli, J.D. (1994). TGF-β1 influences the relative development of the exocrine and endocrine pancreas in vitro. Development 120, 3451-3462.
56. Saperstein, L.A., Jirtle, R.L., Farouk, M., Thompson, H.J., Chung, K.S., and Meyers, W.C. (1994). Transforming growth factor-β1 and 6-phosphate/insulin-like growth factor-II receptor expresduring intrahepatic bile duct hyperplasia and biliary fibrosis in the rat. Hepatology 19, 412-417.
57. Sato, Y., Tsuboi, R., Lyons, R., Moses, H., and Rifkin, D.B. (1990). Characterization of the activation of latent TGF-β by co-culture of endothelial cells and pericytes or smooth muscle cells: a self-regusystem. J. Cell Biol. 111, 757-763.
58. Schultz-Cherry, S., and Murphy-Ullrich, J.E. (1993). Thrombosponcauses activation of latent transforming growth factor-β seby endothelial cells by a novel mechanism. J. Cell Biol. 122, 923-932.
59. Schultz-Cherry, S., Lawler, J., and Murphy-Ullrich, J.E. (1994a). The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-β. J. Biol. Chem. 269, 26783-26788.
60. Schultz-Cherry, S., Ribeiro, S., Gentry, L., and Murphy-Ullrich, J.E. (1994b). Thrombospondin binds and activates the small and large forms of latent transforming growth factor-β in a chemically defined system. J. Biol. Chem. 269, 26775-26782.
61. Schultz-Cherry, S., Chen, H., Mosher, D.F., Misenheimer, T.M., Krutzsch, H.C., Roberts, D.D., and Murphy-Ullrich, J.E. (1995). Reguof transforming growth factor-β activation by discrete seof thrombospondin 1. J. Biol. Chem. 270, 7304-7310.
62. Serra, R., and Moses, H.L. (1996). Tumor suppressor genes in the TGF-β signaling pathway? Nat. Med. 2, 390-391.
63. Shull, M.M., Ormsby, I., Kier, A.B., Pawlowski, S., Diebold, R.J., Yin, M., Allen, R., Sidman, C., Proetzel, G., Calvin, D., et al. (1992). Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359, 693-699.
64. Sjoholm, A., and Hellerstrom, C. (1991). TGF-β stimulates insulin secretion and blocks mitogenic response of pancreatic β cells to glucose. Am. J. Physiol. 260, C1046-C1051.
65. Souchelnitskiy, S., Chambaz, E.M., and Feige, J.-J. (1995). Thromselectively activate one of the two latent forms of transgrowth factor-β present in adrenocortical cell-conditioned medium. Endocrinol. 136, 5118-5126.
66. Tolsma, S.S., Volpert, O.V., Good, D.J., Frazier, W.F., Polverini, P.J., and Bouck, N. (1993). Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activ. J. Cell Biol. 722, 497-511.
67. Wahl, S.M. (1994). Transforming growth factor β: the good, the bad, and the ugly. J. Exper. Med. 180, 1587-1590.
68. Yamanaka, Y., Friess, H., Buchler, M., Beger, H.G., Gold, L.I., and Korc, M. (1993). Synthesis and expression of transforming growth factor β-1, β-2, and β-3 in the endocrine and exocrine pancreas. Diabetes 42, 746-756.
69. Yang, Y., Dignam, J.D., and Gentry, L.E. (1997). Role of carbohydrate in the binding of β1-latency-associated peptide to li. Biochemistry 36, 11923-11932.
70. Yaswen, L., Kulkarni, A.B., Fredrickson, T., Mittleman, B., Schiffman, ., Payne, S., Longenecker, G., Mozes, E., and Karlsson, S. (1996). Autoimmune manifestations in the transforming growth factor-β1 mouse. Blood 87, 1439-1445.
71. Yuspa, S.H., and Harris, C.C. (1974). Altered differentiation of mouse cells treated with retinyl acetate in vitro. Exp. Cell Res. 86, 95-105.
72. Zhou, L., Dey, C.R., Wert, S.E., and Whitsett, J.A. (1996). Arrested morphogenesis in transgenic mice bearing an SP-C-TGF-β1 chimeric gene. Dev. Biol. 175, 227-238.