Angiogenic and inflammatory responses following skeletal muscle injury are altered by immune neutralization of endogenous basic fibroblast growth factor, insulin-like growth factor-1 and transforming growth factor-β1

Journal of Neuroimmunology

Volumn 70, Issue 1, 1996, Pages 37-44

  Lefaucheur, Jean Pascal ^a   Gjata, Bernard ^a   Lafont, Hélène ^a   Sebille, Alain ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

Basic fibroblast growth factor; Endothelial cell; Insulin like growth factor 1; Macrophage; Mast cell; Transforming growth factor 1

Indexed keywords

FIBROBLAST GROWTH FACTOR; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; HISTOLOGY; MACROPHAGE; MALE; MAST CELL; MOUSE; MUSCLE INJURY; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; SKELETAL MUSCLE;

EID: 0030272318     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-5728(96)00099-9     Document Type: Article

References (68)

1. Adams, D.H., Hathaway, M., Shaw, J., Burnett, D., Elias, E. and Strain, A.J. (1991) Transforming growth factor-β induced human T lymphocyte migration in vitro. J. Immunol. 147, 609-614.
2. Allen, R.E. and Boxhorn, L.K. (1989) Regulation of skeletal muscle satellite cell proliferation and differentiation by TGF-beta, IGF-I and FGF. J. Cell Physiol. 138, 311-315.
3. Arahata, K. and Engel, A.G. (1984) Monoclonal antibody analysis of mononuclear cells in myopathies. I. Quantitation of subsets according to diagnosis and sites of accumulation and demonstration and counts of muscle fibers invaded by T-cells. Ann. Neurol. 16, 193-208.
4. Baird, A. and Durkin, T. (1986) Inhibition of endothelial cell proliferation by type β-transforming growth factor: interactions with acidic and basic fibroblast growth factors. Biochem. Biophys. Res. Commun. 138, 476-482.
5. Bergstresser, P.R., Tigelaar, R.E. and Tharp, M.D. (1984) Conjugated avidin identifies cutaneous rodent and human mast cells. J. Invest. Dermatol. 83, 214-218.
6. 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.
7. Brandes, M.E., Mai, U.E.H., Ohura, K. and Wahl, S.M. (1991) Human neutrophils express type I TGF-β receptors and chemotax to TGF-β. J. Immunol. 147, 1600-1606.
8. Broadley, K.N., Aquino, A.M., Woodward, S.C., Buckley-Sturrock, A., Sato, Y., Rifkin, D.B. and Davidson, J.M. (1989) Monospecific antibodies implicate basic fibroblast growth factor in normal wound repair. Lab. Invest. 61, 571-575.
9. Bussolati, G. and Gugliotta, P. (1983) Non-specific staining of mast cells by avidin-biotin-peroxidase complexes (ABC). J. Histochem. Cytochem. 31, 1419-1421.
10. Cantini, M., Massimino, M.L., Bruson, A., Catani, C., Dalla Libera, L. and Carraro, U. (1994) Macrophages regulate proliferation and differentiation of satellite cells. Biochem. Biophys. Res. Commun. 202, 1688-1696.
11. Cantini, M. and Carraro, U. (1995) Macrophage-released factor stimulates selectively myogenic cells in primary muscle culture. J. Neuropath. Exp. Neurol. 54, 121-128.
12. Drosos, A.A. and Dalakas, M.C. (1995) Identification of macrophages in the muscle biopsy preparations: a comparative study using specific monoclonal antimacrophage antibodies and acid phosphatase reaction. Muscle Nerve 18, 242-244.
13. Engel, A.G. and Biesescker, G. (1982) Complement activation in muscle fiber necrosis: demonstration of the membrane attack complex of complement in necrotic fibers. Ann. Neurol. 12, 289-296.
14. Folkman, J. and Klagsbrun, M. (1987) Angiogenic factors. Science 235, 442-447.
15. Frater-Schroder, M., Muller, G., Birchmeier, W. and Bohlen, P. (1986) Transforming growth factor-beta inhibits endothelial cell proliferation. Biochem. Biophys. Res. Commun. 137, 295-302.
16. Gajdusek, C.M., Luo, Z. and Mayberg, M.R. (1993) Basic fibroblast growth factor and transforming growth factor beta-1: synergistic mediators of angiogenesis in vitro. J. Cell. Physiol. 157, 133-144.
17. Grounds, M.D. (1987) Phagocytosis of necrotic muscle in muscle isografts is influenced by the strain, age and sex of host mice. J. Pathol. 153, 71-82.
18. Grounds, M.D. (1991) Towards understanding skeletal muscle regeneration. Path. Res. Pract. 187, 1-22.
19. Gruber, B.L., Marchese, M.J. and Kew, R. (1995) Angiogenic factors stimulate mast-cell migration. Blood 86, 2488-2493.
20. Heimark, R., Twardzik, D. and Schwartz, S. (1986) Inhibition of endothelial regeneration by type-beta transforming growth factor from platelets. Science 233, 1078-1080.
21. Hirsch, S. and Gordon, S. (1983) Polymorphic expression of a neutrophil differentiation antigen revealed by monoclonal antibody 7/4. Immunogenetics 18, 229-239.
22. Kehrl, J.H., Wakefield, L.M., Roberts, A.B., Jakowlew, S., Alvarez-Mon, M., Derynck, R., Sporn, M.B. and Fauci, A.S. (1986) Production of transforming growth factor-β by human T-lymphocytes and its potential role in the regulation of T-cell growth. J. Exp. Med. 163, 1037-1050.
23. King, G.L., Goodman, A.D., Buzney, S., Moses, A. and Kahn, C.R. (1985) Receptors and growth-promoting effects of insulin and insulin-like growth factors on cells from bovine retinal capillaries and aorta. J. Clin. Invest 75, 1028-1036.
24. Kitayama, J., Nagawa, H., Yasuhara, H., Tsuno, N., Kimura, W., Shibata, Y. and Muto, T. (1994) Suppressive effect of basic fibroblast growth factor on transendothelial emigration of CD4(+) T-lymphocyte. Cancer Res. 54, 4729-4733.
25. Kulkarni, A.B., Huh, C., 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.
26. Kulkarni, A.B. and Karlsson, S. (1993) Transforming growth factor-β1 knockout mice: a mutation in one cytokine gene causes a dramatic inflammatory disease. Am. J. Path. 143, 3-9.
27. Lefaucheur, J.P. and Sebille, A. (1995a) Muscle regeneration following injury can be modified in vivo by immune neutralization of basic fibroblast growth factor, transforming growth factor beta 1 or insulin-like growth factor I. J. Neuroimmunol. 57, 85-91.
28. Lefaucheur, J.P. and Sebille, A. (1995b) The cellular events of injured muscle regeneration depend on the nature of the injury. Neuromusc. Disord. 5, 501-509.
29. Leo, O., Foo, M., Sachs, D.H., Samelson, L.E. and Bluestone, J.A. (1987) Identification of monoclonal antibody specific for a murine T3 polypeptide. Proc. Natl. Acad. Sci. USA 84, 1374-1378.
30. Letterio, J.J., Geiser, A.G., Kulkarni, A.B., Roche, N.S., Sporn, M.B., Roberts, A.B. (1994) Maternal rescue of transforming growth factor-β1 null mice. Science 264, 1936-1938.
31. Madri, J., Pratt, B. and Tucker, A. (1988) Phenotypic modulation of endothelial cells by transforming growth factor-beta depends upon the composition and organization of the extracellular matrix. J. Cell. Biol. 10, 1375-1384.
32. Merwin, J.R., Anderson, J.M., Kocher, O., van Itallie, CM and Madri, J. (1990) Transforming growth factor beta-1 modulates extracellular matrix organization and cell-cell junctional complex formation during angiogenesis. J. Cell. Physiol. 142, 117-128.
33. Mignatti, P., Tsuboi, R., Robbins, E. and Rifkin, D.B. (1989) In vitro angiogenesis on the human amniotic membrane: requirement for basic fibroblast growth factor-induced proteinases. J. Cell. Biol. 108, 671-682.
34. Mignatti, P., Morimoto, T. and Rifkin, D. (1991) Basic fibroblast growth factor released by single, isolated cells stimulates their migration in an autocrine manner. Proc. Natl. Acad. Sci. USA 88, 11007-11011.
35. Montesano, R., Vassalli, J.D., Baird, A., Guillemein, R. and Orci, L. (1986) Basic fibroblast growth factor induces angiogenesis in vitro. Proc. Natl. Acad. Sci. USA 83, 7297-7301.
36. Muller, G., Behrens, J., Nussbaumer, U., Bohlen, P. and Birchmeier, W. (1987) Inhibitory action of transforming growth factor β on endothelial cells. Proc. Natl. Acad. Sci. USA 85, 5600-5604.
37. Nathan, C.F. (1987) Secretory products of macrophages. J. Clin. Invest. 79, 319-326.
38. Orimo, S., Hiyamuta, E., Arahata, K. and Sugita, H. (1991) Analysis of inflammatory cells and complement C3 in bupivacaine-induced myonecrosis. Muscle Nerve 14, 515-520.
39. Pepper, M., Belin, D., Montesano, R., Orci, L. and Vassalli, J.D. (1990) Transforming growth factor-beta 1 modulates basic fibroblast growth factor-induced proteolytic and angiogenic properties of endothelial cells in vitro. J. Cell. Biol. 111, 743-755.
40. Phillips, G.D., Lu, D., Mitashov, V.I. and Carlson, B.M. (1987) Survival of myogenic cells in freely grafted rectus femoris and extensor digitorum longus muscles. Am. J. Anat. 180, 365-372.
41. Phillips, G.D. and Knighton, D.R. (1990) Angiogenic activity in damaged skeletal muscle. Proc. Soc. Exp. Biol. Med. 193, 197-202.
42. Phillips, G.D., Schilb, L.A., Fiegel V.D. and Knighton, D.R. (1991) An angiogenic extract from skeletal muscle stimulates monocyte and endothelial cell chemotaxis in vitro. Proc. Soc. Exp. Biol. Med. 197, 458-464.
43. Pierce, G.F., Tarpley, J.E., Yanogihara, D., Mustoe, T.A., Fox, G.M. and Thomason, A. (1992) Platelet-derived growth factor (BB homodimer), transforming growth factor-β1 and basic fibroblast growth factor in dermal wound healing. Neovessel and matrix formation and cessation of repair. Am. J. Pathol. 140, 1375-1388.
44. Plaghki, L. (1985) Régénération et myogénèse du muscle strié. J. Physiol. (Paris) 80, 51-110.
45. Presta, M., Moscatelli, D., Joseph-Silverman, J. and Rifkin, D.B. (1986) Purification from a human hepatoma cell line of a basic fibroblast growth factor-like molecule that stimulates capillary endothelial cell plasminogen activator production, DNA synthesis, and migration. Mol. Cell. Biol. 6, 4060-4066.
46. Ranges, G.E., Figari, I.S., Espevik, T. and Palladino, M.A. (1987) Inhibition of cytotoxic T-cell development by transforming growth factor-β and reversal by recombinant tumor necrosis factor-a. J. Exp. Med. 166, 991-998.
47. Reibman, J., Meixler, S., Lee, T.C., Gold, L.I., Cronstein, B.N., Haines, K.A., Kolasinski, S.L. and Weissman, G. (1991) Transforming growth factor β1, a potent chemoattractant for human neutrophils, bypasses classic signal-transduction pathways. Proc. Natl. Acad. Sci. USA 88, 6805-6809.
48. Roberts, A.B., Sporn, M.B., Assoian, R.K., Smith, J.M., Roche, N.S., Wakefield, L.M., Heine, U.I., Liotta, L.A., Falanga, V., Kehrl, J.H. and Fauci, A.S. (1986) Transforming growth factor type β: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc. Natl. Acad. Sci. USA 83, 4167-4171.
49. Roberts, P. and McGeachie, J.K. (1992) Propranolol retards revascularisation and impedes early myogenesis in regenerating skeletal muscle transplants: an autoradiographic and morphometric study in mice. J. Anat. 181, 101-111.
50. Robertson, T.A., Maley, M.A.L., Grounds, M.D. and Papadimitriou, J.M. (1993) The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Exp. Cell Res. 207, 321-331.
51. Roesel, J.F. and Nanney, L.B. (1995) Assessment of differential cytokine effects on angiogenesis using an in vivo model of cutaneous wound repair. J. Surg. Res. 58, 449-459.
52. Sato, Y. and Rifkin, D.B. (1988) Autocrine activities of basic fibroblast growth factor: regulation of endothelial cell movement, plasminogen activator synthesis and DNA synthesis. J. Cell Biol. 107, 1199-1205.
53. Schott, R.J. and Morrow, L.A. (1993) Growth factors and angiogenesis. Cardiovasc. Res. 27, 1155-1161.
54. Shipley, G.D., Tucker, R.F. and Moses, H.L. (1985) Type β transforming growth factor/growth inhibitor stimulates entry of monolayer cultures of AKR-2B cells into S phase after a prolonged prereplicative interval. Proc. Natl. Acad. Sci. USA 82, 4147-4151.
55. Shull, M.M., Ormsby, I., Kier, A.B., Pawlowski, S., Diebold, R.J., Yin, M., Allen, R., Sidman, C., Proetzel, G., Calvin, D., Annunziata, N. and Doetschman, T. (1992) Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359, 693-699.
56. Sunderkotter, C., Goebeler, M., Schulze-Osthoff, K., Bhardwaj, R. and Sorg, C. (1991) Macrophage-derived angiogenesis factors. Pharmacol. Ther. 51, 195-216.
57. Sunderkotter, C., Steinbrink, K., Goebeler, M., Bhardwaj, R. and Sorg, C. (1994) Macrophages and angiogenesis. J. Leukoc. Biol. 55, 410-422.
58. Thompson, J.A., Haudenschild, C.C., Anderson, K.D., DiPietro, J.M., Anderson, W.F. and Maciag, T. (1989) Heparin-binding growth factor 1 induces the formation of organoid neovascular structures in vivo. Proc. Natl. Acad. Sci. USA 86, 7928-7932.
59. Tsunawaki, S., Sporn, M.B., Ding, A. and Nathan, C.F. (1988) Deactivation of macrophage by transforming growth factor-β. Nature 334, 260-262.
60. Wahl, S.M., Hunt, D.A., Wakefield, L.M., McCartney-Francis, N., Wahl, L.M., Roberts, A.B. and Sporn, M.B. (1987) Transforming growth factor β (TGFβ) induces monocyte chemotaxis and growth factor production. Proc. Natl. Acad. Sci. USA 84, 5788-5792.
61. Wahl, S.M., Hunt, D.A., Wong, H.L., Dougherty, S., McCartney-Francis, N., Wahl, L.M., Ellingsworth, L., Schmidt, J.A., Hall, G., Roberts, A.B. and Sporn, M.B. (1988) Transforming growth factor β is a potent immunosuppressive agent that inhibits IL-1-dependent lymphocyte proliferation. J. Immunol. 140, 3026-3031.
62. Wahl, S.M. (1992) Transforming growth factor-β in inflammation: a cause and a cure. J. Clin. Immunol. 12, 61-72.
63. Walgenbach, K.J., Gratas, C., Shestak, K.C. and Becker, D. (1995) Ichaemia-induced expression of bFGF in normal skeletal muscle: a potential paracrine mechanism for mediating angiogenesis in ischaemic skeletal muscle. Nature Medicine, 1, 453-459.
64. Wallick, S., Figari, I., Wakefield, L., Sporn, M., Levinson, A.D. and Palladino, M.A. (1989) Transfectants secreting latent TGFβ1 suppress immune responsiveness. Cytokine 1, 133-138.
65. Weller, B., Karpati, G. and Carpenter, S. (1990) Dystrophin-deficient mdx muscle fibers are preferentially vulnerable to necrosis induced by experimental lengthening contractions. J. Neurol. Sci. 100, 9-13.
66. Wiseman, D.M., Polverini, P.J., Kamp, D.W. and Leibovich, S.J. (1988) Transforming growth factor-beta (TGF-β) is chemotactic for human monocytes and induces their expression of angiogenic activity. Biochem. Biophys. Res. Commun. 157, 793-800.
67. Yang, E.Y. and Moses, H.L. (1990) Transforming growth factor β1-induced changes in cell migration, proliferation, and angiogenesis in the chicken chorioallantoic membrane. J. Cell. Biol. 111, 731-741.
68. Ziada, A.M.A.R., Hudlicka, O., Tyler, K.R. and Wright, A.J.A. (1984) The effect of long-term vasodilatation on capillary growth and performance in rabbit heart and skeletal muscle. Cardiovasc. Res. 18, 724-732.