Biological significance of local TGF-β activation in liver diseases

Frontiers in Physiology

Volumn 3 FEB, Issue , 2012, Pages

  Hayashi, Hiromitsu ^a   Sakai, Takao ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

6 integrin; Fibronectin; Liver disease; Local bioavailability; TGF , TSP 1

Indexed keywords

EID: 84864131030     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00012     Document Type: Review

References (128)

1. Adams, J. C. (2001). Thrombospondins: multifunctional regulators of cell interactions. Annu.Rev. Cell Dev. Biol. 17, 25-51.
2. Annes, J. P., Chen, Y., Munger, J. S., and Rifkin, D. B. (2004). Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J. Cell Biol. 165, 723-734.
3. Annes, J. P., Munger, J. S., and Rifkin, D. B. (2003). Mak- ing sense of latent TGFbeta activation. J. Cell. Sci. 116(Pt 2), 217-224.
4. Annes, J. P., Rifkin, D. B., and Munger, J. S. (2002). The inte- grin alphaVbeta6 binds and activates latent TGFbeta3. FEBS Lett. 511, 65-68.
5. Apte, S. S. (2009). A disintegrin- like and metalloprotease (reprolysin-type) with throm- bospondin type 1 motif (ADAMTS) superfamily: functions and mech- anisms. J. Biol. Chem. 284, 31493-31497.
6. Araya, J., Cambier, S., Morris, A., Finkbeiner, W., and Nishimura, S. L. (2006). Integrin-mediated trans- forming growth factor-beta activa- tion regulates homeostasis of the pulmonary epithelial-mesenchymal trophic unit. Am. J. Pathol. 169, 405-415.
7. Beninati, S., and Piacentini, M. (2004). The transglutaminase family: an overview: minireview article. Amino Acids 26, 367-372.
8. Bhowmick, N. A., Chytil, A., Plieth, D., Gorska, A. E., Dumont, N., Shappell, S., Washington, M. K., Neilson, E. G., and Moses, H. L. (2004). TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303, 848-851.
9. Bissell, D. M., Roulot, D., and George, J. (2001). Transforming growth fac- tor beta and the liver. Hepatology 34, 859-867.
10. Blanchette, F., Day, R., Dong, W., Laprise, M. H., and Dubois, C. M. (1997). TGFbeta1 regulates gene expression of its own converting enzyme furin. J. Clin. Invest. 99, 1974-1983.
11. Blobe, G. C., Schiemann, W. P., and Lodish, H. F. (2000). Role of transforming growth factor beta in human disease. N.Engl.J.Med.342, 1350-1358.
12. Bornstein, P. (2009). Thrombospondins function as regulators of angio- genesis. J. Cell Commun. Signal. 3, 189-200.
13. Boulanger, J., Reyes-Moreno, C., and Koutsilieris, M. (1995). Mediation of glucocorticoid receptor function by the activation of latent transform- ing growth factor beta 1 in MG- 63 human osteosarcoma cells. Int. J. Cancer 61, 692-697.
14. Bourd-Boittin, K., Bonnier, D., Leyme, A., Mari, B., Tuffery, P., Samson, M., Ezan, F., Baffet, G., and Theret, N. (2011). Protease profiling of liver fibrosis reveals the adam metal- lopeptidase with thrombospondin type 1 motif, 1 as a central acti- vator of TGF-beta. Hepatology 54, 2173-2184.
15. Bugge, T. H., Flick, M. J., Daugherty, C. C., and Degen, J. L. (1995). Plas- minogen deficiency causes severe thrombosis but is compatible with development and reproduction. Genes Dev. 9, 794-807.
16. Caccamo, D., Curro, M., and Ientile, R. (2010). Potential of transglutami- nase 2 as a therapeutic target. Expert Opin. Ther. Targets 14, 989-1003.
17. Chen, Y., Wang, X., Weng, D., Tao, S., Lv, L., and Chen, J. (2009). A TSP-1 functional fragment inhibits activa- tion of latent transforming growth factor-beta1 derived from rat alve- olar macrophage after bleomycin treatment. Exp. Toxicol. Pathol. 61, 67-73.
18. Chen, Y., Wang, X., Weng, D., Tian, L., Lv, L., Tao, S., and Chen, J. (2009). A TSP-1 synthetic peptide inhibits bleomycin-induced lung fibrosis in mice. Exp. Toxicol. Pathol. 61, 59-65.
19. Crawford, S. E., Stellmach, V., Murphy- Ullrich, J. E., Ribeiro, S. M., Lawler, J., Hynes, R. O., Boivin, G. P., and Bouck, N. (1998). Thrombospondin-1 is a major acti- vator of TGF-beta1 in vivo. Cell 93, 1159-1170.
20. Dabovic, B., Chen, Y., Colarossi, C., Obata, H., Zambuto, L., Perle, M. A., and Rifkin, D. B. (2002). Bone abnormalities in latent TGF-[beta] binding protein (Ltbp)-3-null mice indicate a role for Ltbp-3 in mod- ulating TGF-[beta] bioavailability. J. Cell Biol. 156, 227-232.
21. Dallas, S. L., Park-Snyder, S., Miya- zono, K., Twardzik, D., Mundy, G. R., and Bonewald, L. F. (1994). Characterization and autoregulation of latent transforming growth fac- tor beta (TGF beta) complexes in osteoblast-like cell lines. Production of a latent complex lacking the latent TGF beta-binding protein. J. Biol. Chem. 269, 6815-6821.
22. Dallas, S. L., Sivakumar, P., Jones, C. J., Chen, Q., Peters, D. M., Mosher, D. F., Humphries, M. J., and Kielty, C. M. (2005). Fibronectin regulates latent transforming growth factor- beta (TGF beta) by controlling matrix assembly of latent TGF beta- binding protein-1. J. Biol. Chem.280, 18871-18880.
23. Derynck, R., Jarrett, J. A., Chen, E. Y., Eaton, D. H., Bell, J. R., Assoian, R. K., Roberts, A. B., Sporn, M. B., and Goeddel, D.V. (1985). Human trans- forming growth factor-beta comple- mentary DNA sequence and expres- sion in normal and transformed cells. Nature 316, 701-705.
24. Dickson, M. C., Martin, J. S., Cousins, F. M., Kulkarni, A. B., Karlsson, S., and Akhurst, R. J. (1995). Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121, 1845-1854.
25. Dooley, S., Hamzavi, J., Breitkopf, K., Wiercinska, E., Said, H. M., Loren- zen, J., Ten Dijke, P., and Gressner, A. M. (2003). Smad7 prevents activa- tion of hepatic stellate cells and liver fibrosis in rats. Gastroenterology 125, 178-191.
26. Dubois, C. M., Laprise, M. H., Blanchette, F., Gentry, L. E., and Leduc, R. (1995). Processing of transforming growth factor beta 1 precursor by human furin convertase. J. Biol. Chem. 270, 10618-10624.
27. Evrard, S., Bluteau, O., Tulliez, M., Rameau, P., Gonin, P., Zetter- berg, E., Palmblad, J., Bonnefoy, A., Villeval, J. L., Vainchenker, W., Giraudier, S., and Wagner-Ballon, O. (2011). Thrombospondin-1 is not the major activator of TGF- beta1 in thrombopoietin-induced myelofibrosis. Blood 117, 246-249.
28. Ezzie, M. E., Piper, M. G., Montague, C., Newland, C. A., Opalek, J. M., Baran, C., Ali, N., Brigstock, D., Lawler, J., and Marsh, C. B. (2011). Thrombospondin-1-deficient mice are not protected from bleomycin- induced pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 44, 556-561.
29. Feng, X. H., and Derynck, R. (2005). Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 21, 659-693.
30. Fontana, L., Chen, Y., Prijatelj, P., Sakai, T., Fassler, R., Sakai, L. Y., and Rifkin, D. B. (2005). Fibronectin is required for integrin alphavbeta6-mediated activation of latent TGF-beta com- plexes containing LTBP-1. FASEB J. 19, 1798-1808.
31. Galbreath, E., Kim, S. J., Park, K., Bren- ner, M., and Messing, A. (1995). Overexpression of TGF-beta 1 in the central nervous system of trans- genic mice results in hydrocephalus. J. Neuropathol. Exp. Neurol. 54, 339-349.
32. Ge, G., and Greenspan, D. S. (2006). BMP1 controls TGFbeta1 activa- tion via cleavage of latent TGFbeta- binding protein. J. Cell Biol. 175, 111-120.
33. Gentry, L. E., and Nash, B. W. (1990). The pro domain of pre-pro- transforming growth factor beta 1 when independently expressed is a functional binding protein for the mature growth factor. Biochemistry 29, 6851-6857.
34. Goundis, D., and Reid, K. B. (1988). Properdin, the terminalcomplement components, thrombospondin and the circumsporozoite protein of malaria parasites contain similar sequence motifs. Nature 335, 82-85.
35. Gray, A. M., and Mason, A. J. (1990). Requirement for activinA and trans- forming growth factor - beta 1 pro- regions in homodimer assembly. Sci- ence 247, 1328-1330.
36. Grenard, P., Bresson-Hadni, S., El Alaoui, S., Chevallier, M., Vuit- ton, D. A., and Ricard-Blum, S. (2001). Transglutaminase-mediated cross-linking is involved in the sta- bilization of extracellular matrix in human liver fibrosis. J. Hepatol. 35, 367-375.
37. Gressner, A. M., and Weiskirchen, R. (2006). Modern pathogenetic con- cepts of liver fibrosis suggest stellate cells and TGF-beta as major players and therapeutic targets. J. Cell. Mol. Med. 10, 76-99.
38. Hanada, K., Vermeij, M., Garinis, G. A., de Waard, M. C., Kunen, M. G., Myers, L., Maas, A., Duncker, D. J., Meijers, C., Dietz, H. C., Kanaar, R., and Essers, J. (2007). Perturbations of vascular homeostasis and aortic valve abnormalities in fibulin-4 defi- cient mice. Circ. Res. 100, 738-746.
39. Hayashi, H., Sakai, K., Baba, H., and Sakai, T. (2011). Thrombospondin- 1 is a novel negative regulator of liver regeneration after par- tial hepatectomy via TGF-beta1 activation in mice. Hepatology. doi:10.1002/hep.24800. [Epub ahead of print].
40. Horan, G. S., Wood, S., Ona, V., Li, D. J., Lukashev, M. E., Weinreb, P. H., Simon, K. J., Hahm, K., Allaire, N. E., Rinaldi, N. J., Goyal, J., Feghali- Bostwick, C. A., Matteson, E. L., O'Hara, C., Lafyatis, R., Davis, G. S., Huang, X., Sheppard, D., and Vio- lette, S. M. (2008). Partial inhibition of integrin alpha(v)beta6 prevents pulmonary fibrosis without exacer- bating inflammation. Am. J. Respir. Crit. Care Med. 177, 56-65.
41. Hynes, R. O. (1986). Fibronectins. Sci. Am. 254, 42-51.
42. Hynes, R. O. (1992). Integrins: versatil- ity, modulation, and signaling in cell adhesion. Cell 69, 11-25.
43. Hynes, R. O. (2002). Integrins: bidirec- tional, allosteric signaling machines. Cell 110, 673-687.
44. Hynes, R. O. (2009). The extracellular matrix: not just pretty fibrils. Science 326 1216-1219.
45. Hyytiainen, M., Penttinen, C., and Keski-Oja, J. (2004). Latent TGF- beta binding proteins: extracellular matrix association and roles in TGF- beta activation. Crit. Rev. Clin. Lab. Sci. 41, 233-264.
46. Hyytiainen, M., Taipale, J., Heldin, C. H., and Keski-Oja, J. (1998). Recombi- nant latent transforming growth fac- tor beta-binding protein 2 assembles to fibroblast extracellular matrix and is susceptible to proteolytic process- ing and release. J. Biol. Chem. 273, 20669-20676.
47. Isogai, Z., Ono, R. N., Ushiro, S., Keene, D. R., Chen, Y., Mazzieri, R., Charbonneau, N. L., Reinhardt, D. P., Rifkin, D. B., and Sakai, L. Y. (2003). Latent transforming growth factor beta-binding protein 1 interacts with fibrillin and is a microfibril-associated protein. J. Biol. Chem. 278, 2750-2757.
48. Kanzaki, T., Olofsson, A., Moren, A., Wernstedt, C., Hellman, U., Miya- zono, K., Claesson-Welsh, L., and Heldin, C. H. (1990). TGF-beta 1 binding protein: a component of the large latent complex of TGF-beta 1 with multiple repeat sequences. Cell 61, 1051-1061.
49. Kojima, S., Nara, K., and Rifkin, D. B. (1993). Requirement for transglut- aminase in the activation of latent transforming growth factor-beta in bovine endothelial cells. J. Cell Biol. 121, 439-448.
50. Koli, K., Saharinen, J., Hyytiainen, M., Penttinen, C., and Keski- Oja, J. (2001). Latency, activation, and binding proteins of TGF-beta. Microsc. Res. Tech. 52, 354-362.
51. Koli, K., Wempe, F., Sterner-Kock, A., Kantola, A., Komor, M., Hofmann, W. K., von Melchner, H., and Keski- Oja, J. (2004). Disruption of LTBP-4 function reduces TGF-beta activa- tion and enhances BMP-4 signaling in the lung. J. Cell Biol. 167,123-133.
52. Kondou, H., Mushiake, S., Etani, Y., Miyoshi, Y., Michigami, T., and Ozono, K. (2003). A blocking pep- tide for transforming growth factor- beta1 activation prevents hepatic fibrosis in vivo. J. Hepatol. 39, 742-748.
53. 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). Trans- forming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. U.S.A. 90, 770-774.
54. Kyriakides, T. R., and Maclauchlan, S. (2009). The role of throm- bospondins in wound healing, ischemia, and the foreign body reac- tion. J. Cell Commun. Signal. 3, 215-225.
55. Loeys, B. L., Gerber, E. E., Riegert- Johnson, D., Iqbal, S., Whiteman, P., McConnell, V., Chillakuri, C. R., Macaya, D., Coucke, P. J., De Paepe, A., Judge, D. P., Wigley, F., Davis, E. C., Mardon, H. J., Handford, P., Keene, D. R., Sakai, L. Y., and Dietz, H. C. (2010). Mutations in fibrillin- 1 cause congenital scleroderma: stiff skin syndrome. Sci. Transl. Med. 2, 23ra20.
56. Lopez, A. R., Cook, J., Deininger, P. L., and Derynck, R. (1992). Domi- nant negative mutants of transform- ing growth factor-beta 1 inhibit the secretion of different transforming growth factor-beta isoforms. Mol. Cell. Biol. 12, 1674-1679.
57. Lyons, R. M., Gentry, L. E., Purchio, A. F., and Moses, H. L. (1990). Mechanism of activation of latent recombinant transforming growth factor beta 1 by plasmin. J. Cell Biol. 110, 1361-1367.
58. Lyons, R. M., Keski-Oja, J., and Moses, H. L. (1988). Proteolytic activation of latent transforming growth factor-beta from fibroblast- conditioned medium. J. Cell Biol. 106, 1659-1665.
59. Maeda, T., Sakabe, T., Sunaga, A., Sakai, K., Rivera, A. L., Keene, D. R., Sasaki, T., Stavnezer, E., Iannotti, J., Schweitzer, R., Ilic, D., Baskaran, H., and Sakai, T. (2011). Conversion of mechanical force into TGF-beta- mediated biochemical signals. Curr. Biol. 21, 933-941.
60. Mallat, Z., Gojova, A., Marchiol- Fournigault, C., Esposito, B., Kamate, C., Merval, R., Fradelizi, D., and Tedgui, A. (2001). Inhibition of transforming growth factor-beta signaling accelerates atherosclerosis and induces an unstable plaque phenotype in mice. Circ. Res. 89, 930-934.
61. Massague, J., Seoane, J., and Wotton, D. (2005). Smad transcription factors. Genes Dev. 19, 2783-2810.
62. Massam-Wu, T., Chiu, M., Choud- hury, R., Chaudhry, S. S., Bald- win, A. K., McGovern, A., Baldock, C., Shuttleworth, C. A., and Kielty, C. M. (2010). Assembly of fib- rillin microfibrils governs extracel- lular deposition of latent TGF beta. J. Cell Sci. 123(Pt 17), 3006-3018.
63. Matsuzaki, K. (2012). Smad phospho- isoform signals in acute and chronic liver injury: similarities and differ- ences between epithelial and mes- enchymal cells. Cell Tissue Res. 347, 225-243.
64. Mazzieri, R., Jurukovski, V., Obata, H., Sung, J., Platt, A., Annes, E., Karaman-Jurukovska, N., Gleizes, P. E., and Rifkin, D. B. (2005). Expres- sion of truncated latent TGF-beta- binding protein modulates TGF- beta signaling. J. Cell Sci. 118(Pt 10), 2177-2187.
65. Miyazono, K., Olofsson, A., Colosetti, P., and Heldin, C. H. (1991). A role of the latent TGF-beta 1-binding pro- tein in the assembly and secretion of TGF-beta 1. EMBO J. 10,1091-1101.
66. Miyazono, K., Thyberg, J., and Heldin, C. H. (1992). Retention of the trans- forming growth factor-beta 1 pre- cursor in the Golgi complex in a latent endoglycosidase H-sensitive form. J. Biol. Chem. 267, 5668-5675.
67. Moriya, K., Bae, E., Honda, K., Sakai, K., Sakaguchi, T., Tsujimoto, I., Kamisoyama, H., Keene, D. R., Sasaki, T., and Sakai, T. (2011). A fibronectin-independent mecha- nism of collagen fibrillogenesis in adult liver remodeling. Gastroen- terology 140, 1653-1663.
68. Mosher, D. F. (1989). Fibronectin. San Diego: Academic Press.
69. Mosher, D. F. (1990). Physiology of thrombospondin. Annu.Rev.Med. 41, 85-97.
70. Moustakas, A.,and Heldin, C.H. (2009). The regulation of TGFbeta sig- nal transduction. Development 136, 3699-3714.
71. Mu, D., Cambier, S., Fjellbirkeland, L., Baron, J. L., Munger, J. S., Kawakatsu, H., Sheppard, D., Broaddus, V. C., and Nishimura, S. L. (2002). The integrin alpha(v)beta8 medi- ates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J. Cell Biol.157, 493-507.
72. Munger, J. S., Harpel, J. G., Gleizes, P. E., Mazzieri, R., Nunes, I., and Rifkin, D. B. (1997). Latent transforming growth factor-beta: structural fea- tures and mechanisms of activation. Kidney Int. 51, 1376-1382.
73. Munger, J. S., Huang, X., Kawakatsu, H., Griffiths, M. J., Dalton, S. L., Wu, J., Pittet, J. F., Kaminski, N., Garat, C., Matthay, M. A., Rifkin, D. B., and Sheppard, D. (1999). The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96, 319-328.
74. Murphy-Ullrich, J. E., and Poczatek, M. (2000). Activation of latent TGF- beta by thrombospondin-1: mech- anisms and physiology. Cytokine Growth Factor Rev. 11, 59-69.
75. Nardacci, R., O. Lo Iacono, Ciccosanti, F., Falasca, L., Addesso, M., Amen- dola, A., Antonucci, G., Craxi, A., Fimia, G. M., Iadevaia, V., Melino, G., Ruco, L., Tocci, G., Ippolito, G., and Piacentini, M. (2003). Transglutam- inase type II plays a protective role in hepatic injury. Am. J. Pathol. 162, 1293-1303.
76. Neptune, E. R., Frischmeyer, P. A., Ark- ing, D. E., Myers, L., Bunton, T. E., Gayraud, B., Ramirez, F., Sakai, L. Y., and Dietz, H. C. (2003). Dysregu- lation of TGF-beta activation con- tributes to pathogenesis in Marfan syndrome. Nat. Genet. 33, 407-411.
77. Nunes, I., Gleizes, P. E., Metz, C. N., and Rifkin, D. B. (1997). Latent trans- forming growth factor-beta bind- ing protein domains involved in activation and transglutaminase- dependent cross-linking of latent transforming growth factor-beta. J. Cell Biol. 136, 1151-1163.
78. Oe, S., Lemmer, E. R., Conner, E. A., Factor, V. M., Leveen, P., Larsson, J., Karlsson, S., and Thorgeirsson, S. S. (2004). Intact signaling by trans- forming growth factor beta is not required for termination of liver regeneration in mice. Hepatology 40, 1098-1105.
79. Okuno, M., Akita, K., Moriwaki, H., Kawada, N., Ikeda, K., Kaneda, K., Suzuki, Y., and Kojima, S. (2001). Prevention of rat hepatic fibrosis by the protease inhibitor, camo- stat mesilate, via reduced generation of active TGF-beta. Gastroenterology 120, 1784-1800.
80. Olofsson, A., Miyazono, K., Kanzaki, T., Colosetti, P., Engstrom, U., and Heldin, C. H. (1992). Transform- ing growth factor-beta 1, -beta 2, and -beta 3 secreted by a human glioblastoma cell line. Identification of small and different forms of large latent complexes. J. Biol. Chem. 267, 19482-19488.
81. Patsenker, E., Popov, Y., Stickel, F., Jon- czyk, A., Goodman, S. L.,and Schup- pan, D. (2008). Inhibition of inte- grin alphavbeta6 on cholangiocytes blocks transforming growth factor- beta activation and retards biliary fibrosis progression. Gastroenterol- ogy 135, 660-670.
82. Popov, Y., Patsenker, E., Stickel, F., Zaks, J., Bhaskar, K. R., Niedobitek, G., Kolb, A., Friess, H., and Schuppan, D. (2008). Integrin alphavbeta6 is a marker of the progression of biliary and portal liver fibrosis and a novel target for antifibrotic therapies. J. Hepatol. 48, 453-464.
83. Popov, Y., Sverdlov, D. Y., Sharma, A. K., Bhaskar, K. R., Li, S., Freitag, T. L., Lee, J., Dieterich, W., Melino, G., and Schuppan, D. (2011). Tis- sue transglutaminase does not affect fibrotic matrix stability or regression of liver fibrosis in mice. Gastroen- terology 140, 1642-1652.
84. 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). Transform- ing growth factor-beta 3 is required for secondary palate fusion. Nat. Genet. 11, 409-414.
85. Puthawala, K., Hadjiangelis, N., Jacoby, S. C., Bayongan, E., Zhao, Z., Yang, Z., Devitt, M. L., Horan, G. S., Wein- reb, P. H., Lukashev, M. E., Violette, S. M., Grant, K. S., Colarossi, C., For- menti, S. C.,and Munger, J. S. (2008). Inhibition of integrin alpha(v)beta6, an activator of latent transform- ing growth factor-beta, prevents radiation-induced lung fibrosis. Am. J. Respir. Crit. Care Med. 177, 82-90.
86. Ribeiro, S. M., Poczatek, M., Schultz- Cherry, S., Villain, M., and Murphy-Ullrich, J. E. (1999). The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J. Biol. Chem. 274, 13586-13593.
87. Russell, W. E., Coffey, R. J. Jr., Ouel- lette, A. J., and Moses, H. L. (1988). Type beta transforming growth fac- tor reversibly inhibits the early pro- liferative response to partial hepate- ctomy in the rat. Proc. Natl.Acad. Sci. U.S.A. 85, 5126-5130.
88. Saharinen, J., Taipale, J., and Keski-Oja, J. (1996). Association of the small latent transforming growth factor- beta with an eight cysteine repeat of its binding protein LTBP-1. EMBO J. 15, 245-253.
89. Sanderson, N., Factor, V., Nagy, P., Kopp, J., Kondaiah, P., Wakefield, L., Roberts, A. B., Sporn, M. B., and Thorgeirsson, S. S. (1995). Hepatic expression of mature transform- ing growth factor beta 1 in trans- genic mice results in multiple tissue lesions. Proc. Natl. Acad. Sci. U.S.A. 92, 2572-2576.
90. Sanford, L. P., Ormsby, I., Gittenberger- de Groot, A. C., Sariola, H., Fried- man, R., Boivin, G. P., Cardell, E. L., and Doetschman, T. (1997). TGF- beta2 knockout mice have multi- ple developmental defects that are non-overlapping with other TGF- beta knockout phenotypes. Develop- ment 124, 2659-2670.
91. Sato, Y., and Rifkin, D. B. (1989). Inhibi- tion of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture. J. Cell Biol. 109, 309-315.
92. Sato, Y., Tsuboi, R., Lyons, R., Moses, H., and Rifkin, D. B. (1990). Charac- terization of the activation of latent TGF-beta by co-cultures of endothe- lial cells and pericytes or smooth muscle cells:a self-regulating system. J. Cell Biol. 111, 757-763.
93. Schlunegger, M. P., and Grutter, M. G. (1992). An unusual feature revealed by the crystal structure at 2.2 A resolution of human transforming growth factor-beta 2. Nature 358, 430-434.
94. Schultz-Cherry, S., and Murphy- Ullrich, J. E. (1993). Throm- bospondin causes activation of latent transforming growth factor- beta secreted by endothelial cells by a novel mechanism. J. Cell Biol. 122, 923-932.
95. Schultz-Cherry, S., Ribeiro, S., Gen- try, L., and Murphy-Ullrich, J. E. (1994). Thrombospondin binds and activates the small and large forms of latent transforming growth factor-beta in a chemically defined system. J. Biol. Chem. 269, 26775-26782.
96. Schultz-Cherry, S., Lawler, J., and Murphy-Ullrich, J. E. (1994). The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J. Biol. Chem. 269, 26783-26788.
97. Sellheyer, K., Bickenbach, J. R., Roth- nagel, J. A., Bundman, D., Long- ley, M. A., Krieg, T., Roche, N. S., Roberts, A. B., and Roop, D. R. (1993). Inhibition of skin develop- ment by overexpression of trans- forming growth factor beta 1 in the epidermis of transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 90, 5237-5241.
98. Shi, M., Zhu, J., Wang, R., Chen, X., Mi, L., Walz, T., and Springer, T. A. (2011). Latent TGF-beta struc- ture and activation. Nature 474, 343-349.
99. Shull, M. M., Ormsby, I., Kier, A. B., Pawlowski, S., Diebold, R. J., Yin, M., Allen, R., Sidman, C., Proet- zel, G., Calvin, D., Annunziata, N., and Doetschman, T. (1992). Tar- geted disruption of the mouse trans- forming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359, 693-699.
100. Shweke, N., Boulos, N., Jouanneau, C., Vandermeersch, S., Melino, G., Dussaule, J. C., Chatziantoniou, C., Ronco, P., and Boffa, J. J. (2008). Tissue transglutaminase contributes to interstitial renal fibrosis by favor- ing accumulation of fibrillar col- lagen through TGF-beta activation and cell infiltration. Am. J. Pathol. 173, 631-642.
101. Siegel, P. M., and Massague, J. (2003). Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat. Rev. Cancer 3, 807-821.
102. Sottile, J., and Hocking, D. C. (2002). Fibronectin polymerization regu- lates the composition and stability of extracellular matrix fibrils and cell- matrix adhesions. Mol. Biol. Cell 13, 3546-3559.
103. Sottile, J., Shi, F., Rublyevska, I., Chi- ang, H. Y., Lust, J., and Chandler, J. (2007). Fibronectin-dependent col- lagen I deposition modulates the cell response to fibronectin. Am.J.Phys- iol. Cell Physiol. 293, C1934-C1946.
104. Sterner-Kock, A., Thorey, I. S., Koli, K., Wempe, F., Otte, J., Bangsow, T., Kuhlmeier, K., Kirchner, T., Jin, S., Keski-Oja, J., and von Melch- ner, H. (2002). Disruption of the gene encoding the latent transform- ing growth factor-beta binding pro- tein 4 (LTBP-4) causes abnormal lung development, cardiomyopathy, and colorectal cancer. Genes Dev. 16, 2264-2273.
105. Tahashi, Y., Matsuzaki, K., Date, M., Yoshida, K., Furukawa, F., Sugano, Y., Matsushita, M., Himeno, Y., Ina- gaki, Y., and Inoue, K. (2002). Dif- ferential regulation of TGF-beta sig- nal in hepatic stellate cells between acute and chronic rat liver injury. Hepatology 35, 49-61.
106. Taipale, J., Miyazono, K., Heldin, C. H., and Keski-Oja, J. (1994). Latent transforming growth factor-beta 1 associates to fibroblast extracellular matrix via latent TGF-beta binding protein. J. Cell Biol. 124, 171-181.
107. Taipale, J., Saharinen, J., Hedman, K., and Keski-Oja, J. (1996). Latent transforming growth factor-beta 1 and its binding protein are com- ponents of extracellular matrix microfibrils. J. Histochem. Cytochem. 44, 875-889.
108. ten Dijke, P., and Arthur, H. M. (2007). Extracellular control of TGFbeta sig- nalling in vascular development and disease. Nat. Rev. Mol. Cell Biol. 8, 857-869.
109. ten Dijke, P., Iwata, K. K., Thorikay, M., Schwedes, J., Stewart, A., and Pieler, C. (1990). Molecular characteriza- tion of transforming growth factor type beta 3. Ann. N. Y. Acad. Sci. 593, 26-42.
110. Theodorescu, D., Bergsma, D., Man, M. S., Elshourbagy, N., Sheehan, C., Rie- man, D., and Kerbel, R. S. (1991). Cloning and overexpression of TGF- beta 1 cDNA in a mammary ade- nocarcinoma: in vitro and in vivo effects. Growth Factors 5, 305-316.
111. Todorovic, V., Frendewey, D., Gutstein, D. E., Chen, Y., Freyer, L., Finnegan, E., Liu, F., Murphy, A., Valenzuela, D., Yancopoulos, G., and Rifkin, D. B. (2007). Long form of latent TGF- beta binding protein 1 (Ltbp1L) is essential for cardiac outflow tract septation and remodeling. Develop- ment 134, 3723-3732.
112. Ueberham, E., Low, R., Ueberham, U., Schonig, K., Bujard, H., and Gebhardt, R. (2003). Conditional tetracycline-regulated expression of TGF-beta1 in liver of transgenic mice leads to reversible intermediary fibrosis. Hepatology 37, 1067-1078.
113. Unsold, C., Hyytiainen, M., Bruckner- Tuderman, L., and Keski-Oja, J. (2001). Latent TGF-beta bind- ing protein LTBP-1 contains three potential extracellular matrix inter- acting domains. J. Cell Sci. 114(Pt 1), 187-197.
114. van Bezooijen, R. L., Deruiter, M. C., Vilain, N., Monteiro, R. M., Visser, A., van der Wee-Pals, L., van Munsteren, C. J., Hogendoorn, P. C., Aguet, M., Mummery, C. L., Papapoulos, S. E., Ten Dijke, P., and Lowik, C. W. (2007). SOST expression is restricted to the great arteries during embryonic and neonatal cardiovas- cular development. Dev. Dyn. 236, 606-612.
115. van der Flier, A., and Sonnenberg, A. (2001). Function and interactions of integrins. Cell Tissue Res. 305, 285-298.
116. Velling, T., Risteli, J., Wennerberg, K., Mosher, D. F., and Johansson, S. (2002). Polymerization of type I and III collagens is dependent on fibronectin and enhanced by inte- grins alpha 11beta 1 and alpha 2beta 1. J. Biol. Chem. 277, 37377-37381.
117. Verderio, E. A., Johnson, T., and Griffin, M. (2004). Tissue transglutaminase in normal and abnormal wound healing: review article. Amino Acids 26, 387-404.
118. Wakefield, L. M., and Stuelten, C. (2007). Keeping order in the neigh- borhood: new roles for TGFbeta in maintaining epithelial homeostasis. Cancer Cell 12, 293-295.
119. Wang, B., Dolinski, B. M., Kikuchi, N., Leone, D. R., Peters, M. G., Weinreb, P. H., Violette, S. M., and Bissell, D. M. (2007). Role of alphavbeta6 inte- grin in acute biliary fibrosis. Hepa- tology 46, 1404-1412.
120. Weinbaum, J. S., Broekelmann, T. J., Pierce, R. A., Werneck, C. C., Segade, F., Craft, C. S., Knutsen, R. H., and Mecham, R. P. (2008). Deficiency in microfibril-associated glycoprotein- 1 leads to complex phenotypes in multiple organ systems. J. Biol. Chem. 283, 25533-25543.
121. Wipff, P. J., and Hinz, B. (2008). Inte- grins and the activation of latent transforming growth factor beta1 - an intimate relationship. Eur. J. Cell Biol. 87, 601-615.
122. Xie, X. S., Li, F. Y., Liu, H. C., Deng, H. C., Li, Z., and Fan, J. M. (2010). LSKL, a peptide antagonist of thrombospondin-1, attenuates renal interstitial fibro- sis in rats with unilateral ureteral obstruction. Arch. Pharm. Res. 33, 275-284.
123. Yang, Z., Mu, Z., Dabovic, B., Jurukovski, V., Yu, D., Sung, J., Xiong, X., and Munger, J. S. (2007). Absence of integrin-mediated TGFbeta1 activa- tion in vivo recapitulates the pheno- type of TGFbeta1-null mice. J. Cell Biol. 176, 787-793.
124. Yoshinaga, K., Obata, H., Jurukovski, V., Mazzieri, R., Chen, Y., Zilberberg, L., Huso, D., Melamed, J., Prijatelj, P., Todorovic, V., Dabovic, B., and Rifkin, D. B. (2008). Perturbation of transforming growth factor (TGF)-beta1 association with latent TGF-beta binding protein yields inflammation and tumors. Proc. Natl. Acad. Sci. U.S.A. 105, 18758-18763.
125. Young, G. D., and Murphy-Ullrich, J. E. (2004). Molecular inter- actions that confer latency to transforming growth factor- beta. J. Biol. Chem. 279, 38032-38039.
126. Yu, Q., and Stamenkovic, I. (2000). Cell surface-localized matrix metalloproteinase-9 proteolyt- ically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 14, 163-176.
127. Zacchigna, L., Vecchione, C., Notte, A., Cordenonsi, M., Dupont, S., Maretto, S., Cifelli, G., Ferrari, A., Maffei, A., Fabbro, C., Braghetta, P., Marino, G., Selvetella, G., Aretini, A., Colonnese, C., Bettarini, U., Russo, G., Soligo, S., Adorno, M., Bonaldo, P., Volpin, D., Piccolo, S., Lembo, G., and Bressan, G. M. (2006). Emilin1 links TGF-beta maturation to blood pressure homeostasis. Cell 124, 929-942.
128. Zhou, L., Dey, C. R., Wert, S. E., and Whitsett, J. A. (1996). Arrested lung morphogenesis in transgenic mice bearing an SP-C-TGF-beta 1 chimeric gene. Dev. Biol. 175, 227-238.