Major basic protein-1 promotes fibrosis of dystrophic muscle and attenuates the cellular immune response in muscular dystrophy

Human Molecular Genetics

Volumn 17, Issue 15, 2008, Pages 2280-2292

  Wehling henricks, Michelle ^a   Sokolow, Sophie ^a   Lee, Jamie J ^c   Myung, Kyu H ^d   Villalta, S Armando ^a   Tidball, James G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAYO CLINIC   (United States)

^d Chonnam National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR ANTAGONIST; CHEMOKINE RECEPTOR CCR3; DYSTROPHIN; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; MAJOR BASIC PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; DISEASE MODEL; DUCHENNE MUSCULAR DYSTROPHY; EOSINOPHIL; GENE EXPRESSION; GENE MUTATION; HEART MUSCLE FIBROSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MORTALITY; MOUSE; MUSCLE CELL; MUSCLE FIBER MEMBRANE; MYOFIBROSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN SECRETION; SPLEEN CELL; TH1 CELL; TH2 CELL;

ANIMALS; ANTIBODIES, MONOCLONAL; DIAPHRAGM; DISEASE MODELS, ANIMAL; EOSINOPHIL MAJOR BASIC PROTEIN; EOSINOPHILS; FIBROSIS; HUMANS; LEUKOCYTE REDUCTION PROCEDURES; MICE; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCLES; MUSCULAR DYSTROPHY, DUCHENNE; MUTATION; MYOCARDIUM; RECEPTORS, CCR3; REGENERATION; SPLEEN; T-LYMPHOCYTES, CYTOTOXIC;

MUS;

EID: 48049084529     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn129     Document Type: Article

References (53)

1. Spencer, M.J., Walsh, C.M., Dorshkind, K.A., Rodriguez, E.M. and Tidball, J.G. (1997) Myonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity. J. Clin. Invest., 99 2745-2751.
2. Spencer, M.J., Rodriguez, E., Dorshkind, K. and Tidball, J.G. (2001) Helper (CD4 +) and cytotoxic, (CD8 +) T cells promote the pathology of dystrophin-deficient muscle. Clin. Immunol., 98, 235-243.
3. Wehling, M., Spencer, M.J. and Tidball, J.G. (2001) A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J. Cell Biol., 155, 123-131.
4. Hodgetts, S., Radley, H., Davies, M. and Grounds, M.D. (2006) Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking of TNFalpha function with Etanercept in mdx mice. Neuromuscul. Disord., 16, 591-602.
5. Morrison, J., Lu, Q.L., Pastoret, C., Partridge, T. and Bou-Gharios, G. (2000) T-cell-dependent fibrosis in the mdx dystrophic mouse. Lab. Invest., 80, 881-891.
6. Morrison, J., Palmer, D.B., Cobbold, S., Partridge, T. and Bou-Gharios, G. (2005) Effects of T-lymphocyte depletion on muscle fibrosis in the mdx mouse. Am. J. Pathol., 166, 1701-1710.
7. Cai, B., Spencer, M.J., Nakamura, G., Tseng-Ong, L. and Tidball, J.G. (2000) Eosinophilia of dytrophin-deficient muscle is promoted by perforin-mediated cytotoxicity by T cell effectors. Am. J Pathol., 156, 1789-1796.
8. Gleich, G.J., Frigas, E., Loegering, D.A., Wassom, D.L. and Steimmuller, D. (1979) Cytotoxic properties of the eosinophil major basic protein. J. Immunol., 123, 2925-2927.
9. Frigas, E., Loegering, D.A. and Gleich, G.J. (1980) Cytotoxic effects of guinea pig eosinophil major basic protein on tracheal epithelium. Lab. Invest., 42, 35-43.
10. Tai, P.C., Hayes, D.J., Clark, J.B. and Spry, C.J. (1982) Toxic effects of human eosinophil products on isolated rat heart cells in vitro. Biochem. J., 204, 475-80.
11. Rothenberg, M.E. and Hogan, S.P. (2006) The eosinophil. Annu. Rev. Immunol., 24, 147-174.
12. Agosti, J.M., Altman, L.C., Ayars, G.H., Loegering, D.A., Gleich, G.J. and Klebanoff, S.J. (1987) The injurious effect of eosinophil peroxidase, hydrogen peroxide, and halides on pneumocytes in vitro. J. Allergy Clin. Immunol., 79, 496-504.
13. MacPherson, J.C., Comhair, S.A., Erzurum, S.C., Klein, D.F., Lipscomb, M.F., Kavuru, M.S., Samoszuk, M.K. and Hazen, S.L. (2001) Eosinophils are a major source of nitric oxide-derived oxidants in severe asthma: characterization of pathways available to eosinophils for generating reactive nitrogen species. J. Inimunol., 166, 5763-5772.
14. Piliponsky, A.M., Pickholtz, D., Gleich, G.J. and Levi-Schaffer, F. (2001) Human eosinophils induce histamine release from antigen-activated rat peritoneal mast cells: A possible role for mast cells in late-phase allergic reactions. J. Allergy Clin. Immunol., 107, 993-1000.
15. Nakajima, H., Gleich, G.J. and Kita, H. (1996) Constitutive production of IL-4 and IL-10 stimulated production of IL-8 by normal peripheral blood eosinophils. J. Immunol., 156, 4859-4866.
16. Horsley, V., Jansen, K.M., Mills, S.T. and Pavlath, G.K. (2003) IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell, 113, 483-494.
17. Silver, R.M., Miller, K.S., Kinsella, M.B., Smith, E.A. and Schabel, S.I. (1990) Evaluation and management of scleroderma lung disease using bronchoalveolar lavage. Am. J. Med., 88, 470-476.
18. Todd, R., Donoff, B.R., Chiang, T., Chou, M.Y., Elovic, A., Gallagher, G.T. and Wong, D.T. (1991) The eosinophil as a cellular source of transforming growth factor alpha in healing cutaneous wounds. Am. J. Pathol., 138, 1307-1313.
19. Noguchi, H., Kephart, G.M., Colby, T.V. and Gleich, G.J. (1992) Tissue eosinophilia and eosinophil degranulation in syndromes associated with fibrosis. Am. J. Pathol., 140, 521-528.
20. Gussoni, E., Pavlath, G.K., Miller, R.G., Panzara, M.A., Powell, M., Blau, H.M. and Steinman, L. (1994) Specific T cell receptor gene rearrangements at the site of muscle degeneration in Duchenne muscular dystrophy. J. Immunol., 153, 4798-4805.
21. Mawhorter, S.D., Kazura, J.W. and Boom, W.H. (1994) Human eosinophils as antigen-presenting cells: Relative efficiency for superantigen- and antigen-induced CD4+ T-cell proliferation. Immunology, 81, 584-591.
22. Shi, H.Z., Humbles, A., Gerard, C., Jin, Z. and Weller, P.F. (2000) Lymph node trafficking and antigen presentation by endobronchial eosinophils. J. Clin. Invest., 105, 945-953.
23. Peterson, C.G., Skoog, V. and Venge, P. (1986) Human eosinophil cationic proteins (ECP and EPX) and their suppressive effects on lymphocyte proliferation. Immunobiology, 171, 1-13.
24. Lee, J.J. and Lee, N.A. (2005) Eosinophil degranulation: An evolutionary vestige or a universally destructive effector function? Clin. Exp. Allergy, 35, 986-994.
25. Temkin, V., Aingorn, H., Puxeddu, I., Goldshmidt, O., Zcharia, E., Gleich, G.J., Vlodavsky, I. and Levi-Schaffer, F. (2004) Eosinophil major basic protein: First identified natural heparanase-inhibiting protein. J. Allergy Clin. Immunol., 113, 703-709.
26. Rochester, C.L., Ackerman, S.J., Zheng, T. and Elias, J.A. (1996) Eosinophil-fibroblast interactions. Granule major basic protein interacts with IL-1 and transforming growth factor-beta in the stimulation of lung fibroblast IL-6-type cytokine production. J. Immunol., 156, 4449-4456.
27. Stedman, H.H., Sweeney, H.L., Shrager, J.B., Maguire, H.C., Panettieri, R.A., Petrof, B., Narusawa, M., Leferovich, J.M., Sladky, J.T. and Kelly, A.M. (1991) The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature, 352, 536-539.
28. Goldspink, G., Fernandes, K., Williams, P.E. and Wells, D.J. (1994) Age-related changes in collagen gene expression in the muscles of mdx dystrophic and normal mice. Neuromuscul. Disord., 4, 183-191.
29. Wehling-Henricks, M., Jordan, M.C., Roos, K.P., Deng, B. and Tidball, J.G. (2005) Cardiomyopathy in dystrophin-deficient hearts is prevented by expression of a neuronal nitric oxide synthase transgene in the myocardium. Hum. Molec. Genet., 14, 1921-1933.
30. Finsterer, J. and Stollberger, C. (2003) The heart in human dystrophinopathies. Cardiology, 99, 1-19.
31. Moriuchi, T., Fujii, Y., Kagawa, N. and Hizawa, K. (1991) Autopsy study on the weight of the heart, liver, kidney and brain in Duchenne muscular dystrophy. Tokushima J. Exp. Med., 38, 5-13.
32. Fenoglio, J.J., Jr, Pham, T.D., Harken, A.H., Horowitz, L.N., Josephson, M.E. and Wit, A.L. (1983) Recurrent sustained ventricular tachycardia: structure and ultrastructure of subendocardial regions in which tachycardia originates. Circulation, 68, 518-533.
33. Pastoret, C. and Sebille, A. (1995) Mdx mice show progressive weakness and muscle deterioration with age. J. Neurol. Sci., 129, 97-105.
34. Yamazaki, M., Minota, S., Sakurai, H., Miyazono, K., Yamada, A., Kanazawa, I. and Kawai, M. (1994) Expression of transforming growth factor-beta 1 and its relation to endomysial fibrosis in progressive muscular dystrophy. Am. J. Pathol., 144, 221-226.
35. Bernasconi, P., Torchiana, E., Confalonieri, P., Brugnoni, R., Barresi, R., Mora, M., Cornelioi, F., Morandi, L. and Mantegazza, R. (1995) Expression of transforming growth factor-beta 1 in dystrophic patient muscles correlates with fibrosis. Pathogenetic role of a fibrogenic cytokine. J. Clin. Invest., 96, 1137-1144.
36. Passerini, L., Bernasconi, P., Baggi, F., Confalonieri, P., Cozzi, F., Cornelio, F. and Mantegazza, R. (2002) Fibrogenic cytokines and extent of fibrosis in muscle of dogs with X-linked golden retriever muscular dystrophy. Neuromuscul. Disord., 12, 828-835.
37. Gosselin, L.E., Williams, J.E., Deering, M., Brazeau, D., Koury, S. and Martinez, D.A. (2004) Localization and early time course of TGF-beta 1 mRNA expression in dystrophic muscle. Muscle Nerve, 30, 645-653.
38. Andreetta, F., Bernsaconi, P., Baggi, F., Ferro, P., Oliva, L., Arnoldi, E., Cornelio, F., Mantegazza, R. and Confalonieri, P. (2006) Immunomodulation of TGF-beta 1 in mdx mouse inhibits connective tissue proliferation in diaphragm but increases inflammatory response: implications for antifibrotic therapy. J. Neuroimmunol., 175 77-86.
39. Tai, P.C., Ackerman, S.J., Spry, C.J., Dunnette, S., Olsen, E.G. and Geich, G.J. (1987) Deposits of eosinophil granule proteins in cardiac tissues of patients with eosinophilic endomyocardial disease. Lancet 1, 643-647.
40. Heufelder, A.E., Goellner, JR., Bahn, R.S., Gleich, G.J. and Hay, I.D. (1996) Tissue eosinophilia and eosinophil degranulation in Riedel's invasive fibrous thyroiditis. J. Clin. Endocrinol. Metab., 81 977-984.
41. deMello, D.E., Liapis, H., Jureidini, S., Nouri, S., Kephart, G.M. and Gleich, G.J. (1990) Cardiac localization of eosinophil-granule major basic protein in acute necrotizing myocarditis. N. Engl. J. Med., 323, 1542-1545.
42. Schwarze, J., Cieslewicz, G., Joetham, A., Ikemura, T., Hamelmann, E. and Gelfand, E.W. (1999) CD8 T cells are essential in the development of respiratory syncytial virus-induced lung eosinophila and airway hyperresponsiveness. J. Immunol., 162, 4207-4211.
43. Milici, A.J., Carroll, L.A., Stukenbrok, H.A., Shay, A.K., Gladue, R.P. and Showell, H.J. (1998) Early eosinophil infiltration into the optic nerve of mice with experimental allergic encephalomyeliltis. Lab. Invest., 78, 1239-1244.
44. Denzler, K.L., Farmer, S.C., Crosby, J.R., Borchers, M., Cieslewicz, G., Larson, K.A., Cormier-Regard, S., Lee,N.A. andLee, J.J. (2000) Eosinophil major basic protein-1 does not contribute to allergen-induced airway pathologies in mouse models of asthma. J. Immunol., 165 5509-5517.
45. Amalfitano, A. and Chamberlain, J.S. (1996) The mdx-amplification-resistant mutation system assay, a simple and rapid polymerase chain reaction-based detection of the mdx allele. Muscle Nerve, 19, 1549-1553.
46. Anderson, J.E., Bressler, B.H. and Ovalle, W.K. (1988) Functional regeneration in the hindlimb skeletal muscle of the mdx mouse. J. Muscle Res. Cell Motil., 9, 499-515.
47. Lee, J.J., McGarry, M.P., Farmer, S.C., Dcnzler, K.L., Larson, K.A., Carrigan, P.E., Brenneise, I.E., Horton, M.A., Haczku, A., Gelfand, E.W. et al. (1997) Interleukin-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J. Exp. Med., 185, 2143-2456.
48. Gersch, C., Dewald, O., Zoerlein, M., Michael, L.H., Entman, M.L. and Frangogiannis, N.G. (2002) Mast cells and macrophages in normal C57/BL/6 mice. Histochem. Cell. Biol., 118, 41-49.
49. Nguyen, H.X. and Tidball, J.G. (2003) Interactions between neutrophils and macrophages promote killing of rat muscle cells in vitro. J. Physiol., 547, 125-132.
50. Kroegel, C., Yukawa, T., Dent, G., Venge, P., Chung, K.F. and Barnes, P.J. (1989) Stimulation of degranulation from human eosinophils by platelet-activating factor. J. Immunol., 142, 3518-3526.
51. Kivirikko, K.I., Laitinen, O. and Prockop, D.J. (1967) Modifications of a specific assay for hydroxyproline in urine. Anal. Biochem., 19, 249-255.
52. Ohnuki, L.E., Wagner, L.A., Georgelas, A., Loegering, D.A., Checkel, J.L., Plager, D.A. and Glcich, G.J. (2005) Differential extraction of eosinopbil granule proteins. J. Immunol. Methods, 307, 54-61.
53. Popken-Harris, P., Checkel, J., Loegering, D., Madden, B., Springett, M., Kephart G. and Glcich, G.J. (1998) Regulation and processing of a precursor form of eosinophil granule major basic protein (ProMBP) in differentiating eosinophils. Blood, 92, 623-631.