T and B lymphocyte depletion has a marked effect on the fibrosis of dystrophic skeletal muscles in the scid/mdx mouse

Journal of Pathology

Volumn 213, Issue 2, 2007, Pages 229-238

  Farini, A ^a   Meregalli, M ^a   Belicchi, M ^a   Battistelli, M ^a   Parolini, D ^a   D'Antona, G ^b   Gavina, M ^a   Ottoboni, L ^c   Constantin, G ^c   Bottinelli, R ^b   Torrente, Y ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c UNIVERSITY OF VERONA   (Italy)

Author keywords

Duchenne muscular dystrophy (DMD); Fibrosis; MDX; SCID

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOFLUOROMETRY; DUCHENNE MUSCULAR DYSTROPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROSIS; HISTOPATHOLOGY; IMMUNE SYSTEM; LYMPHOCYTE DEPLETION; MOUSE; MUSCLE ATROPHY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCID MOUSE; SKELETAL MUSCLE; T LYMPHOCYTE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; B-LYMPHOCYTES; CELL ADHESION MOLECULES; CROSSES, GENETIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROSIS; MALE; MICE; MICE, INBRED MDX; MICE, SCID; MUSCLE FIBERS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; PEDIGREE; T-LYMPHOCYTES;

EID: 35349000178     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2213     Document Type: Article

References (63)

1. Hoffman EP, Brown RHJ, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987;51:919-928.
2. Ervasti JM, Campbell KP. Membrane organization of the dystrophin-glycoprotein complex. Cell 1991;66:1121-1131.
3. Arahata K, Ishiura S, Ishiguro T, Tsukahara T, Suhara Y, Eguchi C, et al. Immunostaining of skeletal and cardiac muscle surface membrane with antibody against Duchenne muscular dystrophy peptide. Nature 1988;333(6176):861-863.
4. Bonilla E, Samitt CE, Miranda AF, Hays AP, Salviati G, DiMauro S, et al. Duchenne muscular dystrophy: deficiency of dystrophin at the muscle cell surface. Cell 1988;54(4):447-452.
5. Morrison J, Palmer DB, Cobbold S, Partridge T, Bou-Gharios G. Effects of T-lymphocyte depletion on muscle fibrosis in the mdx mouse. Am J Pathol 2005;166(6):1701-1710.
6. Arahata K, Engel AG. Monoclonal antibody analysis of mononuclear cells in myopathies. IV: cell-mediated cytotoxicity and muscle fiber necrosis. Ann Neurol 1988;23:168-173.
7. Emslie-Smith AM, Arahata K, Engel AG. Major histocompatibility complex class I antigen expression, immunolocalization of interferon subtypes, and T cell-mediated cytotoxicity in myopathies. Hum Pathol 1989;20:224- 231.
8. McDouall RM, Dunn MJ, Dubowitz V. Nature of the mononuclear infiltrate and the mechanism of muscle damage in juvenile dermatomyositis and Duchenne muscular dystrophy. J Neurol Sci 1990;99:199-217.
9. Tidball JG, Wehling-Henricks M. Damage and inflammation in muscular dystrophy: potential implications and relationships with autoimmune myositis. Curr Opin Rheumatol 2005;17:707-713.
10. Acharyya S, Villalta SA, Bakkar N, Bupha-Intr T, Janssen PM, Carathers M, et al. Interplay of IKK/NF-κB signalling in macrophages and myofibres promotes muscle degeneration in Duchenne muscular dystrophy. J Clin Invest 2007;117(4):889-901.
11. Spencer MJ, Walsh CM, Dorshkind KA, Rodriguez EM, Tidball JG. Myonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity. J Clin Invest 1997;99(11):2745-2751.
12. Confalonieri P, Oliva L, Andreetta F, Lorenzoni R, Dassi P, Mariani E, et al. Muscle inflammation and MHC class I up-regulation in muscular dystrophy with lack of dysferlin: an immunopathological study. J Neuroimmunol 2003;142(1-2):130-136.
13. Kovacs EJ. Fibrogenic cytokines: role of immune mediators in the development of scar tissue. Immunol Today 1991;12:17-23.
14. Lyons R, Gentry L, Purchio AF, Moses HL. Mechanism of activation of latent recombinant transforming growth factor-β from fibroblast conditioned medium. J Cell Biol 1990;110:1361-1367.
15. Tapiale J, Lohi J, Saarinen J, Kovanen PT, Keski-Oja J. Human mast cell chymase and leukocyte elastase release latent transforming growth factor-b from the extracellular matrix of cultured human epithelial and endothelial cells. J Biol Chem 1995;270:4689-4696.
16. Brugge TH, Kombrinck KW, Flick MJ, Daugherty CC, Danton MJS, Degen JL. Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell 1996;87:709-719.
17. Miyazono K, Heldin C-H. Role of carbohydrate structures in TGF-β1 latency. Nature 1989;338:158-160.
18. Barcellos-Hoff M, Dix TA. Redox-mediated activation of latent transforming growth factor-β1. Mol Endocrinol 1996;10:1077- 1083.
19. Roberts AB, Sporn MB. Physiological actions and clinical applications of transforming growth factor-β1 (TGF-β). Growth Factors 1993;8(1):1-9.
20. Kingsley DM. The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 1994;8(2):133-146.
21. Bonniaud P, Margetts PJ, Kolb M, Haberberger T, Kelly M, Robertson J, et al. Adenoviral gene transfer of connective tissue growth factor in the lung induces transient fibrosis. Am J Respir Crit Care Med 2003;168(7):770-778.
22. Amoroso SR, Huang N, Roberts AB, Potter M, Letterio JJ. Consistent loss of functional transforming growth factor beta receptor expression in murine plasmacytomas. Proc Natl Acad Sci USA 1998;95(1):189-194.
23. Gosselin LE, Williams JE, Deering M, Brazeau D, Koury S, Martinez DA. Localization and early time course of TGF-β1 mRNA expression in dystrophic muscle. Muscle Nerve 2004;30:645-653.
24. Bernasconi P, Torchiana E, Confalonieri P, Morandi L, Brugnoni R, Barresi R, et al. Expression of transforming growth factor-β1 in dystrophic patient muscles correlates with fibrosis: pathogenetic role of fibrogenic cytokines. J Clin Invest 1995;96:1137-1144.
25. Yamazaki M, Minota S, Sakurai H, Miyazono K, Yamada A, Kanazawa I, et al. Expression of transforming growth factor-β1 and its relation to endomysial fibrosis in progressive muscular dystrophy. Am J Pathol 1994;144:221-226.
26. DiMario JX, Uzman A, Strohman RC. Fiber regeneration is not persistent in dystrophic (MDX) mouse skeletal muscle. Dev Biol 1991;148(1):314-321.
27. Anderson JE, Ovalle WK, Bressler BH. Electron microscopic and autoradiographic characterization of hindlimb muscle regeneration in the mdx mouse. Anat Rec 1987;219:243-257.
28. Dangain J, Vrbova G. Muscle development in mdx mutant mice. Muscle Nerve 1984;7:700-704.
29. Bulfield G, Siller WG, Wight PA, Moore KJ. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 1984;81:1189-1192.
30. Torres LF, Duchen LW. The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and endplates. Brain 1987;110(2):269-299.
31. Pastoret C, Sebille A. Mdx mice show progressive weakness and muscle deterioration with age. J Neurol Sci 1995;129:97-105.
32. Perryman LE, Torbeck RL. Combined immunodeficiency of Arabian horses: confirmation of autosomal recessive mode of inheritance. J Am Vet Med Assoc 1980;176(11):1250-1251.
33. Schuler W, Weiler IJ, Schuler A, Philips RA, Rosenberg N, Mak TW, et al. Rearrangement of antigen receptor genes is defective in mice with severe combined immune deficiency. Cell 1986;46(7):963-972.
34. Torrente Y, D'Angelo MG, Li Z, Del Bo R, Corti S, Mericskay M, et al. Transplacental injection of somite-derived cells in mdx mouse embryos for the correction of dystrophin deficiency. Hum Mol Genet 2000;9(12):1843-1852.
35. Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D'Antona G, Pellegrino M, et al. Cell therapy of α-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblast. Science 2003;301:487-492.
36. Rossi R, Bottinelli R, Sorrentino V, Reggiani C. Response to caffeine and ryanodine receptor isoforms in mouse skeletal muscles. Am J Physiol Cell Physiol 2001;281:C585-594.
37. Denti MA, Rosa A, D'Antona G, Sthandier O, De Angelis FG, Nicoletti C, et al. Body-wide gene therapy of Duchenne muscular dystrophy in the mdx mouse model. Proc Natl Acad Sci USA 2006;103(10):3758- 3756.
38. + stem cells after intra-arterial transplantation. Blood 2006;108(8):2857-2866.
39. Laws N, Hoey A. Progression of kyphosis in mdx mice. J Appl Physiol 2004;97:1970-1977.
40. Andreetta F, Bernasconi P, Baggi F, Ferro P, Oliva L, Arnoldi E, et al. Immunomodulation of TGF-β1 in mdx mouse inhibits connective tissue proliferation in diaphragm but increases inflammatory response: implications for antifibrotic therapy. J Neuroimmunol 2006;175:77-86.
41. Torrente Y, Camirand G, Pisati F, Belicchi M, Rossi B, Colombo F, et al. Identification of a putative pathway for the muscle homing of stem cell in a muscular dystrophy mode. J Cell Biol 2003;162(3):511-520.
42. Granchelli JA, Pollina C, Hudecki MS. Duchenne-like myopathy in double-mutant mdx mice expressing exaggerated mast cell activity. J Neurol Sci 1995;131(1):1-7.
43. Nahirney PC, Dow PR, Ovalle WK. Quantitative morphology of mast cells in skeletal muscle of normal and genetically dystrophic mice. Anat Rec 1997;247(3):341-349.
44. Gorospe JRM, Tharp M, Demitsu T, Hoffman EP. Dystrophin-deficient myofibers are vulnerable to mast cell granule-induced necrosis. Neuromusc Disord 1994;4(4):325-333.
45. Engel AG, Arahata K. Mononuclear cells in myopathies: quantitation of functionally distinct subsets, recognition of antigen-specific cell-mediated cytotoxicity in some diseases, and implications for the pathogenesis of the different inflammatory myopathies. Hum Pathol 1986;17:704-721.
46. Riley DA, Ellis S, Giornetti CS, et al. Muscle sarcomere lesions and thrombosis after spaceflight and suspension unloading. J Appl Physiol 1992;73(2, suppl):S 33-43.
47. Fielding RA, Manfredi TJ, Ding W, Fiatarone MA, Evans WJ, Cannon JG. Acute phase response in exercise. III. Neutrophil and IL-1β accumulation in skeletal muscle. Am J Physiol 1993;265(1 pt 2):R166-172.
48. Tidball JG, Berchenko E, Frenette J. Macrophage invasion does not contribute to muscle membrane injury during inflammation. J Leukocyte Biol 1999;65(4):492-498.
49. +) T cells promote the pathology of dystrophin-deficient muscle. Clin Immunol 2001;98(2):235-243.
50. Duchenne GBA. Recherches sur la paralysie musculaire pseudohypertrophique au paralysie myosclerotique. Arch Gen Med 1868;11:552-588.
51. Overall CM, Wrana JL, Sodek J. Transcriptional and post-transcriptional regulation of 72-kDa gelatinase/type IV collagenase by transforming growth factor-β1 in human fibroblasts. Comparisons with collagenase and tissue inhibitor of matrix metalloproteinase gene expression. J Biol Chem 1991;266:14064-14071.
52. Sharma K, Ziyadeh FN. The emerging role of transforming growth factor-β in kidney diseases. Am J Physiol Renal Physiol 1994;266:F829-842.
53. Hartel JV, Granchelli JA, Hudecki MS, Pollina CM, Gosselin LE. Impact of prednisone on TGF-β1 and collagen in diaphragm muscle from mdx mice. Muscle Nerve 2001;24:428-432.
54. Branton H, Kopp J. TGF-β and fibrosis. Microb Infect 1999;1:1349-1365.
55. Morrison J, Lu QL, Pastoret C, Partridge T, Bou-Gharios G. T cell-dependent fibrosis in the mdx dystrophic mouse. Lab Invest 2000;80:881-891.
56. Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, et al. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 1991;352:536-539.
57. Gillery P, Leperre A, Maquart FX, Borel JP. Insulin-like growth factor-1 (IGF-1) stimulates protein synthesis and collagen gene expression in monolayer and lattice cultures of fibroblasts. J Cell Physiol 1992;152:389- 396.
58. Wehling M, Spencer MJ, Tidball JG. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 2001;155:123-131.
59. Lurton J, Soto H, Narayanan AS, Raghu G. Regulation of human lung fibroblast C1q-receptors by transforming growth factor-β and tumor necrosis factor α. Exp Lung Res 1999;25:151-164.
60. Campbell J, Hedrick J, Zlotnik A, Siani M, Thompson D, Butcher E. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 1998;279:381-384.
61. Wright D, Bowman E, Wagers A, Butcher E, Weissman I. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med 2002;195:1145-1154.
62. (+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 2004;114(2):182-195.
63. Sampaolesi M, Blot S, D'Antona G, Granger N, Tonlorenzi R, Innocenzi A, et al. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 2006;444(7119):574-579.