Making sense of latent TGFβ activation

Journal of Cell Science

Volumn 116, Issue 2, 2003, Pages 217-224

  Annes, Justin P ^a   Munger, John S ^a   Rifkin, Daniel B ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Activation; Sensor; Transforming growth factor

Indexed keywords

BINDING PROTEIN; INTEGRIN; PEPTIDE DERIVATIVE; REACTIVE OXYGEN METABOLITE; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; CARRIER PROTEIN; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; PROTEIN; SIGNAL PEPTIDE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2;

COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE RELEASE; EXTRACELLULAR MATRIX; HUMAN; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REVIEW; ANIMAL; BIOLOGICAL MODEL; EUKARYOTIC CELL; MACROMOLECULE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CARRIER PROTEINS; EUKARYOTIC CELLS; EXTRACELLULAR MATRIX; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LATENT TGF-BETA BINDING PROTEINS; MACROMOLECULAR SUBSTANCES; MODELS, BIOLOGICAL; PROTEINS; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 2; TRANSFORMING GROWTH FACTOR BETA;

EID: 0037439630     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00229     Document Type: Review

References (78)

1. Akhurst, R. J., Lehnert, S. A., Faissner, A. and Duffle, E. (1990). TGF beta in murine morphogenetic processes: the early embryo and cardiogenesis. Development 108, 645-656.
2. Annes, J. P., Rifkin, D. B. and Munger, J. S. (2002). The integrin alphaVbeta6 binds and activates latent TGFbeta3. FEBS Lett. 511, 65-68.
3. Barcellos-Hoff, M. H. and Dix, T. A. (1996). Redox-mediated activation of latent transforming growth factor-beta 1. Mol. Endocrinol. 10, 1077-1083.
4. Barcellos-Hoff, M. H., Derynck, R., Tsang, M. L. and Weatherbee, J. A. (1994). Transforming growth factor-beta activation in irradiated murine mammary gland. J. Clin. Invest. 93, 892-899.
5. Blobe, G. C., Schiemann, W. P. and Lodish, H. F. (2000). Role of transforming growth factor beta in human disease. New Engl. J. Med. 342, 1350-1358.
6. Border, W. A. and Ruoslahti, E. (1992). Transforming growth factor-beta in disease: the dark side of tissue repair. J. Clin. Invest. 90, 1-7.
7. Breuss, J. M., Gillett, N., Lu, L., Sheppard, D. and Pytela, R. (1993). Restricted distribution of integrin beta 6 mRNA in primate epithelial tissues. J. Histochem. Cytochem. 41, 1521-1527.
8. Breuss, J. M., Gallo, J., DeLisser, H. M., Klimanskaya, I. V., Folkesson, H. G., Pittet, J. F., Nishimura, S. L., Aldape, K., Landers, D. V., Carpenter, W. et al. (1995). Expression of the beta 6 integrin subunit in development, neoplasia and tissue repair suggests a role in epithelial remodeling. J. Cell Sci. 108, 2241-2251.
9. Brunner, A. M., Marquardt, H., Malacko, A. R., Lioubin, M. N. and Purchio, A. F. (1989). Site-directed mutagenesis of cysteine residues in the pro region of the transforming growth factor beta 1 precursor. Expression and characterization of mutant proteins. J. Biol. Chem. 264, 13660-13664.
10. 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 activator of TGF-beta1 in vivo. Cell 93, 1159-1170.
11. 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 modulating TGF-[beta] bioavailability. J. Cell Biol. 156, 227-232.
12. Dallas, S. L., Miyazono, K., Skerry, T. M., Mundy, G. R. and Bonewald, L. F. (1995). Dual role for the latent transforming growth factor-beta binding protein in storage of latent TGF-beta in the extracellular matrix and as a structural matrix protein. J. Cell Biol. 131, 539-549.
13. De Laurenzi, V. and Melino, G. (2001). Gene disruption of tissue transglutaminase. Mol. Cell. Biol. 21, 148-155.
14. 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.
15. Filvaroff, E., Erlebacher, A., Ye, J., Gitelman, S. E., Lotz, J., Heillman, M. and Derynck, R. (1999). Inhibition of TGF-beta receptor signaling in osteoblasts leads to decreased bone remodeling and increased trabecular bone mass. Development 126, 4267-4279.
16. Flaumenhaft, R., Abe, M., Sato, Y., Miyazono, K., Harpel, J., Heldin, C. H. and Rifkin, D. B. (1993). Role of the latent TGF-beta binding protein in the activation of latent TGF-beta by co-cultures of endothelial and smooth muscle cells. J. Cell Biol. 120, 995-1002.
17. Frazier, W. A. (1991). Thrombospondins. Curr. Opin. Cell Biol. 3, 792-799.
18. Geiser, A. G., Zeng, Q. Q., Sato, M., Helvering, L. M., Hirano, T. and Turner, C. H. (1998). Decreased bone mass and bone elasticity in mice lacking the transforming growth factor-beta1 gene. Bone 23, 87-93.
19. 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.
20. Gleizes, P. E., Beavis, R. C., Mazzieri, R., Shen, B. and Rifkin, D. B. (1996). Identification and characterization of an eight-cysteine repeat of the latent transforming growth factor-beta binding protein-1 that mediates bonding to the latent transforming growth factor-beta1. J. Biol. Chem. 271, 29891-29896.
21. Gold, L. I. (1999). The role for transforming growth factor-beta (TGF-beta) in human cancer. Crit. Rev. Oncog. 10, 303-360.
22. Gualandris, A., Annes, J. P., Arese, M., Noguera, I., Jurukovski, V. and Rifkin, D. B. (2000). The latent transforming growth factor-beta-binding protein-1 promotes In vitro differentiation of embryonic stem cells into endothelium. Mol. Biol. Cell 11, 4295-4308.
23. Ignotz, R. A. and Massague, J. (1986). Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem. 261, 4337-4345.
24. Iruela-Arispe, M. L., Liska, D. J., Sage, E. H. and Bornstein, P. (1993). Differential expression of thrombospondin 1, 2, and 3 during murine development. Dev. Dyn. 197, 40-56.
25. Janssens, K., Gershoni-Baruch, R., Guanabens, N., Migone, N., Ralston, S., Bonduelle, M., Lissens, W., van Maldergem, L., Vanhoenacker, F., Verbruggen, L. et al. (2000). Mutations in the gene encoding the latency-associated peptide of TGF-beta 1 cause Camurati-Engelmann disease. Nat. Genet. 26, 273-275.
26. 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-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat. Genet. 11, 415-421.
27. Kanzaki, T., Olofsson, A., Moren, A., Wernstedt, C., Hellman, U., Miyazono, 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.
28. Kinoshita, A., Saito, T., Tomita, H., Makita, Y., Yoshida, K., Ghadami, M., Yamada, K., Kondo, S., Ikegawa, S., Nishimura, G. et al. (2000). Domain-specific mutations in TGFB1 result in Camurati-Engelmann disease. Nat. Genet. 26, 19-20.
29. Kojima, S. and Rifkin, D. B. (1993). Mechanism of retinoid-induced activation of latent transforming growth factor-beta in bovine endothelial cells. J. Cell Physiol. 155, 323-332.
30. 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.
31. Koski, C., Saharinen, J. and Keski-Oja, J. (1999). Independent promoters regulate the expression of two amino terminally distinct forms of latent transforming growth factor-beta binding protein-1 (LTBP-1) in a cell type-specific manner. J. Biol. Chem. 274, 32619-32630.
32. Lawrence, D. A., Pircher, R., Kryceve-Martinerie, C. and Jullien, P. (1984). Normal embryo fibroblasts release transforming growth factors in a latent form. J. Cell Physiol. 121, 184-188.
33. Lawrence, D. A., Pircher, R. and Jullien, P. (1985). Conversion of a high molecular weight latent beta-TGF from chicken embryo fibroblasts into a low molecular weight active beta-TGF under acidic conditions. Biochem. Biophys. Res. Commun. 133, 1026-1034.
34. Lee, R., Kermani, P., Teng, K. K. and Hempstead, B. L. (2001). Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-1948.
35. Leitlein, J., Aulwurm, S., Waltereit, R., Naumann, U., Wagenknecht, B., Garten, W., Weller, M. and Platten, M. (2001). Processing of immunosuppressive pro-TGF-beta 1,2 by human glioblastoma cells involves cytoplasmic and secreted furin-like proteases. J. Immunol. 166, 7238-7243.
36. 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.
37. Majack, R. A., Mildbrandt, J. and Dixit, V. M. (1987). Induction of thrombospondin messenger RNA levels occurs as an immediate primary response to platelet-derived growth factor. J. Biol. Chem. 262, 8821-8825.
38. McMahon, G. A., Dignam, J. D. and Gentry, L. E. (1996). Structural characterization of the latent complex between transforming growth factor beta 1 and beta 1-latency-associated peptide. Biochem. J. 313, 343-351.
39. Millan, F. A., Denhez, F., Kondaiah, P. and Akhurst, R. J. (1991). Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development 111, 131-143.
40. Miller, L. A., Barnett, N. L., Sheppard, D. and Hyde, D. M. (2001). Expression of the beta6 integrin subunit is associated with sites of neutrophil influx in lung epithelium. J. Histochem. Cytochem. 49, 41-48.
41. Miyazono, K., Olofsson, A., Colosetti, P. and Heldin, C. H. (1991). A role of the latent TGF-beta 1-binding protein in the assembly and secretion of TGF-beta 1. EMBO J. 10, 1091-1101.
42. 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{beta}8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-{beta} 1. J. Cell Biol. 157, 493-507.
43. Munger, J. S., Harpel, J. G., Gleizes, P. E., Mazzieri, R., Nunes, I. and Rifkin, D. B. (1997). Latent transforming growth factor-beta: structural features and mechanisms of activation. Kidney Int. 51, 1376-1382.
44. 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. et al. (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.
45. Murphy-Ullrich, J. E. and Poczatek, M. (2000). Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev. 11, 59-69.
46. Nakajima, Y., Miyazono, K., Kato, M., Takase, M., Yamagishi, T. and Nakamura, H. (1997). Extracellular fibrillar structure of latent TGF beta binding protein-1: role in TGF beta-dependent endothelial-mesenchymal transformation during endocardial cushion tissue formation in mouse embryonic heart. J. Cell Biol. 136, 193-204.
47. Nanda, N., Iismaa, S. F., Owens, W. A., Husain, A., Mackay, F. and Graham, R. M. (2001). Targeted inactivation of Gh/tissue transglutaminase II. J. Biol. Chem. 276, 20673-20678.
48. Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. (1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10, 1-6.
49. Nishimura, G., Nishimura, H., Tanaka, Y., Makita, Y., Ikegawa, S., Ghadami, M., Kinoshita, A. and Niikawa, N. (2002). Camurati-Engelmann disease type II: progressive diaphyseal dysplasia with striations of the bones. Am. J. Med. Genet. 107, 5-11.
50. Nunes, I., Gleizes, P. E., Metz, C. N. and Rifkin, D. B. (1997). Latent transforming growth factor-beta binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-beta. J. Cell Biol. 136, 1151-1163.
51. Olofsson, A., Ichijo, H., Moren, A., ten Dijke, P., Miyazono, K. and Heldin, C. H. (1995). Efficient association of an amino-terminally extended form of human latent transforming growth factor-beta binding protein with the extracellular matrix. J. Biol. Chem. 270, 31294-31297.
52. Oreffo, R. O., Mundy, G. R., Seyedin, S. M. and Bonewald, L. F. (1989). Activation of the bone-derived latent TGF beta complex by isolated osteoclasts. Biochem. Biophys. Res. Commun. 158, 817-823.
53. Oursler, M. J. (1994). Osteoclast synthesis and secretion and activation of latent transforming growth factor beta. J. Bone Miner. Res. 9, 443-452.
54. Ramirez, F. and Pereira, L. (1999). The fibrillins. Int. J. Biochem. Cell Biol. 31, 255-259.
55. Ribeiro, S. M., Poczatek, M., Schultz-Cherry, S., Villain, M. and Murphy-Ullbrich, 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.
56. Saharinen, J. and Keski-Oja, J. (2000). Specific sequence motif of 8-Cys repeats of TGF-beta binding proteins, LTBPs, creates a hydrophobic interaction surface for binding of small latent TGF-beta. Mol. Biol. Cell 11, 2691-2704.
57. 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.
58. Saito, T., Kinoshita, A., Yoshiura, K., Makita, Y., Wakui, K., Honke, K., Niikawa, N. and Taniguchi, N. (2001). Domain-specific mutations of a transforming growth factor (TGF)-beta 1 latency-associated peptide cause Camurati-Engelmann disease because of the formation of a constitutively active form of TGF-beta 1. J. Biol. Chem. 276, 11469-11472.
59. Sanford, L. P., Ormsby, I., Gittenberger-de Groot, A. C., Sariola, H., Friedman, R., Boivin, G. P., Cardell, E. L. and Doetschman, T. (1997). TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124, 2659-2670.
60. Sato, Y. and Rifkin, D. B. (1989). Inhibition 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.
61. Schultz Jel, J., Witt, S. A., Glascock, B. J., Nieman, M. L., Reiser, P. J., Nix, S. L., Kimball, T. R. and Doetschman, T. (2002). TGF-beta1 mediates the hypertrophic cardiomyocyte growth induced by angiotensin II. J. Clin. Invest. 109, 787-796.
62. Schultz-Cherry, S. and Murphy-Ullrich, J. E. (1993). Thrombospondin causes activation of latent transforming growth factor- beta secreted by endothelial cells by a novel mechanism. J. Cell Biol. 122, 923-932.
63. Sinha, S., Nevett, C., Shuttleworth, C. A. and Kielty, C. M. (1998). Cellular and extracellular biology of the latent transforming growth factor-beta binding proteins. Matrix Biol. 17, 529-545.
64. Sterner-Kock, A., Thorey, I. S., Koli, K., Wempe, F., Otte, J., Bangsow, T., Kuhlmeier, K., Kirchner, T., Jin, S., Keski-Oja, J. et al. (2002). Disruption of the gene encoding the latent transforming growth factor- beta binding protein 4 (LTBP-4) causes abnormal lung development, cardiomyopathy, and colorectal cancer. Genes Dev. 16, 2264-2273.
65. 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.
66. Taipale, J., Saharinen, J., Hedman, K. and Keski-Oja, J. (1996). Latent transforming growth factor-beta 1 and its binding protein are components of extracellular matrix microfibrils. J. Histochem. Cytochem. 44, 875-889.
67. Taipale, J., Saharinen, J. and Keski-Oja, J. (1998). Extracellular matrix-associated transforming growth factor-beta: role in cancer cell growth and invasion. Adv. Cancer Res. 75, 87-134.
68. Teitelbaum, S. L. (2000). Bone resorption by osteoclasts. Science 289, 1504-1508.
69. Tsuji, T., Okada, F., Yamaguchi, K. and Nakamura, T. (1990). Molecular cloning of the large subunit of transforming growth factor type beta masking protein and expression of the mRNA in various rat tissues. Proc. Natl. Acad. Sci. USA 87, 8835-8839.
70. Unsold, C., Hyytiainen, M., Bruckner-Tuderman, L. and Keski-Oja, J. (2001). Latent TGF-beta binding protein LTBP-1 contains three potential extracellular matrix interacting domains. J. Cell Sci. 114, 187-197.
71. van der Flier, A. and Sonnenberg, A. (2001). Function and interactions of integrins. Cell Tissue Res. 305, 285-298.
72. Verrecchia, F., Chu, M. L. and Mauviel, A. (2001). Identification of novel TGF-beta /Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. J. Biol. Chem. 276, 17058-17062.
73. Wang, A., Yokosaki, Y., Ferrando, R., Balmes, J. and Sheppard, D. (1996). Differential regulation of airway epithelial integrins by growth factors. Am. J. Respir. Cell Mol Biol. 15, 664-672.
74. Werb, Z. (1997). ECM and cell surface proteolysis: regulating cellular ecology. Cell 91, 439-442.
75. Yang, X., Chen, L., Xu, X., Li, C., Huang, C. and Deng, C. X. (2001). TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. J. Cell Biol. 153, 35-46.
76. Yehualaeshet, T., O'Connor, R., Green-Johnson, J., Mai, S., Silverstein, R., Murphy-Ullrich, J. E. and Khalil, N. (1999). Activation of rat alveolar macrophage-derived latent transforming growth factor beta-1 by plasmin requires interaction with thrombospondin-1 and its cell surface receptor, CD36. Am. J Pathol. 155, 841-851.
77. Yu, Q. and Stamenkovic, I. (2000). Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 14, 163-176.
78. 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.