Amelioration of Duchenne muscular dystrophy in mdx mice by elimination of matrix-associated fibrin-driven inflammation coupled to the α mβ 2 leukocyte integrin receptor

Human Molecular Genetics

Volumn 21, Issue 9, 2012, Pages 1989-2004

  Vidal, Berta ^a,d   Ardite, Esther ^a   Suelves, Mònica ^a,e   Ruiz Bonilla, Vanessa ^a   Janué, Anna ^a   Flick, Matthew J ^b   Degen, Jay L ^b   Serrano, Antonio L ^a   Muñoz Cánoves, Pura ^a,c  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d NewYork Presbyterian Hospital   (United States)

^e Institut de Medicina Predictiva i Personalitzada del Cancer IMPPC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA M BETA2 INTEGRIN; BETA2 INTEGRIN; FIBRIN; FIBRINOGEN; FIBRINOGEN GAMMA 377-395; PEPTIDE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; DISEASE COURSE; DUCHENNE MUSCULAR DYSTROPHY; FEMALE; FIBRIN DEPOSITION; GENE DELETION; GENE MUTATION; LEUKOCYTE; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE INJURY; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SATELLITE CELL; SIGNAL TRANSDUCTION; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; EXTRACELLULAR MATRIX; FIBRIN; FIBRINOGEN; HUMANS; INFLAMMATION; LEUKOCYTES; MACROPHAGE ACTIVATION; MACROPHAGE-1 ANTIGEN; MALE; MICE; MICE, INBRED MDX; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MODELS, BIOLOGICAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; MUTANT PROTEINS; PEPTIDE FRAGMENTS; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

MUS;

EID: 84859308196     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds012     Document Type: Article

References (63)

1. Campbell, K.P. (1995) Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell, 80, 675-679.
2. Sicinski, P., Geng, Y., Ryder-Cook, A.S., Barnard, E.A., Darlison, M.G. and Barnard, P.J. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science, 244, 1578-1580.
3. Durbeej, M. and Campbell, K.P. (2002) Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr. Opin. Genet. Dev., 12, 349-361.
4. Tidball, J.G. (2005) Mechanical signal transduction in skeletal muscle growth and adaptation. J. Appl. Physiol., 98, 1900-1908.
5. 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.
6. Serrano, A.L., Mann, C.J., Vidal, B., Ardite, E., Perdiguero, E. and Munoz-Canoves, P. (2011) Cellular and molecular mechanisms regulating fibrosis in skeletal muscle repair and disease. Curr. Top. Dev. Biol., 96, 167-201.
7. Mann, C.J., Perdiguero, E., Kharraz, Y., Aguilar, S., Pessina, P., Serrano, A.L. and Munoz-Canoves, P. (2011) Aberrant repair and fibrosis development in skeletal muscle. Skelet. Muscle, 1, 21.
8. Goyenvalle, A., Vulin, A., Fougerousse, F., Leturcq, F., Kaplan, J.C., Garcia, L. and Danos, O. (2004) Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science, 306, 1796-1799.
9. Shi, X. and Garry, D.J. (2006) Muscle stem cells in development, regeneration, and disease. Genes Dev., 20, 1692-1708.
10. Montarras, D., Morgan, J., Collins, C., Relaix, F., Zaffran, S., Cumano, A., Partridge, T. and Buckingham, M. (2005) Direct isolation of satellite cells for skeletal muscle regeneration. Science, 309, 2064-2067.
11. Sampaolesi, M., Blot, S., D'Antona, G., Granger, N., Tonlorenzi, R., Innocenzi, A., Mognol, P., Thibaud, J.L., Galvez, B.G., Barthelemy, I. et al. (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature, 444, 574-579.
12. Gregorevic, P., Allen, J.M., Minami, E., Blankinship, M.J., Haraguchi, M., Meuse, L., Finn, E., Adams, M.E., Froehner, S.C., Murry, C.E. et al. (2006) rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat. Med., 12, 787-789.
13. Welch, E.M., Barton, E.R., Zhuo, J., Tomizawa, Y., Friesen, W.J., Trifillis, P., Paushkin, S., Patel, M., Trotta, C.R., Hwang, S. et al. (2007) PTC124 targets genetic disorders caused by nonsense mutations. Nature, 447, 87-91.
14. Gargioli, C., Coletta, M., De Grandis, F., Cannata, S.M. and Cossu, G. (2008) PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nat. Med., 14, 973-978.
15. Chen, S.E., Gerken, E., Zhang, Y., Zhan, M., Mohan, R.K., Li, A.S., Reid, M.B. and Li, Y.P. (2005) Role of TNF-{alpha} signaling in regeneration of cardiotoxin-injured muscle. Am. J. Physiol. Cell Physiol, 289, C1179-C1187.
16. Collins, R.A. and Grounds, M.D. (2001) The role of tumor necrosis factor-alpha (TNF-alpha) in skeletal muscle regeneration. Studies in TNF-alpha(-/-) and TNF-alpha(-/-)/LT-alpha(-/-) mice. J. Histochem. Cytochem, 49, 989-1001.
17. Grounds, M.D. and Torrisi, J. (2004) Anti-TNFalpha (Remicade) therapy protects dystrophic skeletal muscle from necrosis. FASEB J., 18, 676-682.
18. Germani, A., Di Carlo, A., Mangoni, A., Straino, S., Giacinti, C., Turrini, P., Biglioli, P. and Capogrossi, M.C. (2003) Vascular endothelial growth factor modulates skeletal myoblast function. Am. J. Pathol., 163, 1417-1428.
19. Brunelli, S., Sciorati, C., D'Antona, G., Innocenzi, A., Covarello, D., Galvez, B.G., Perrotta, C., Monopoli, A., Sanvito, F., Bottinelli, R. et al. (2007) Nitric oxide release combined with nonsteroidal antiinflammatory activity prevents muscular dystrophy pathology and enhances stem cell therapy. Proc. Natl Acad. Sci. USA, 104, 264-269.
20. 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.
21. Tidball, J.G. (2005) Inflammatory processes in muscle injury and repair. Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R345-R353.
22. Pereira, M., Rybarczyk, B.J., Odrljin, T.M., Hocking, D.C., Sottile, J. and Simpson-Haidaris, P.J. (2002) The incorporation of fibrinogen into extracellular matrix is dependent on active assembly of a fibronectin matrix. J. Cell Sci., 115, 609-617.
23. Rybarczyk, B.J., Lawrence, S.O. and Simpson-Haidaris, P.J. (2003) Matrix-fibrinogen enhances wound closure by increasing both cell proliferation and migration. Blood, 102, 4035-4043.
24. Vidal, B., Serrano, A.L., Tjwa, M., Suelves, M., Ardite, E., De Mori, R., Baeza-Raja, B., Martinez de Lagran, M., Lafuste, P., Ruiz-Bonilla, V. et al. (2008) Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/ alternative macrophage activation pathway. Genes Dev., 22, 1747-1752.
25. Ryu, J.K., Davalos, D. and Akassoglou, K. (2009) Fibrinogen signal transduction in the nervous system. J. Thromb. Haemost., 7(Suppl. 1), 151-154.
26. Bell, W., Shapiro, S., Martinez, J. and Nossel, H.L. (1978) The effects of ancrod, the coagulating enzyme from the venom of Malayan pit viper (A. Rhodostoma) or prpthrombin and fibrinogen metabolism and fibrinopeptide A release in man. J. Lab. Clin. Med., 69, 592-604.
27. Lluis, F., Roma, J., Suelves, M., Parra, M., Aniorte, G., Gallardo, E., Illa, I., Rodriguez, L., Hughes, S.M., Carmeliet, P. et al. (2001) Urokinase-dependent plasminogen activation is required for efficient skeletal muscle regeneration in vivo. Blood, 97, 1703-1711.
28. McRitchie, D.I., Girotti, M.J., Glynn, M.F., Goldberg, J.M. and Rotstein, O.D. (1991) Effect of systemic fibrinogen depletion on intraabdominal abscess formation. J. Lab. Clin. Med., 118, 48-55.
29. Tang, L. and Eaton, J.W. (1993) Fibrin(ogen) mediates acute inflammatory responses to biomaterials. J. Exp. Med., 178, 2147-2156.
30. Akassoglou, K., Adams, R.A., Bauer, J., Mercado, P., Tseveleki, V., Lassmann, H., Probert, L. and Strickland, S. (2004) Fibrin depletion decreases inflammation and delays the onset of demyelination in a tumor necrosis factor transgenic mouse model for multiple sclerosis. Proc. Natl Acad. Sci. USA, 101, 6698-6703.
31. Idell, S. (2003) Coagulation, fibrinolysis, and fibrin deposition in acute lung injury. Crit. Care Med., 31, S213-S220.
32. Serrano, A.L. and Munoz-Canoves, P. (2010) Regulation and dysregulation of fibrosis in skeletal muscle. Exp. Cell Res., 316, 3050-3058.
33. Flick, M.J., Du, X., Witte, D.P., Jirouskova, M., Soloviev, D.A., Busuttil, S.J., Plow, E.F. and Degen, J.L. (2004) Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J. Clin. Invest., 113, 1596-1606.
34. Adams, R.A., Bauer, J., Flick, M.J., Sikorski, S.L., Nuriel, T., Lassmann, H., Degen, J.L. and Akassoglou, K. (2007) The fibrin-derived gamma377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J. Exp. Med., 204, 571-582.
35. Flick, M.J., LaJeunesse, C.M., Talmage, K.E., Witte, D.P., Palumbo, J.S., Pinkerton, M.D., Thornton, S. and Degen, J.L. (2007) Fibrin(ogen) exacerbates inflammatory joint disease through a mechanism linked to the integrin alphaMbeta2 binding motif. J. Clin. Invest., 117, 3224-3235.
36. Steinbrecher, K.A., Horowitz, N.A., Blevins, E.A., Barney, K.A., Shaw, M.A., Harmel-Laws, E., Finkelman, F.D., Flick, M.J., Pinkerton, M.D., Talmage, K.E. et al. (2010) Colitis-associated cancer is dependent on the interplay between the hemostatic and inflammatory systems and supported by integrin alpha(M)beta(2) engagement of fibrinogen. Cancer Res., 70, 2634-2643.
37. Ugarova, T.P., Solovjov, D.A., Zhang, L., Loukinov, D.I., Yee, V.C., Medved, L.V. and Plow, E.F. (1998) Identification of a novel recognition sequence for integrin alphaM beta2 within the gamma-chain of fibrinogen. J. Biol. Chem., 273, 22519-22527.
38. Ugarova, T.P. and Yakubenko, V.P. (2001) Recognition of fibrinogen by leukocyte integrins. Ann. NY Acad. Sci., 936, 368-385.
39. Sitrin, R.G., Pan, P.M., Srikanth, S. and Todd, R.F. 3rd (1998) Fibrinogen activates NF-kappa B transcription factors in mononuclear phagocytes. J. Immunol., 161, 1462-1470.
40. Rubel, C., Gomez, S., Fernandez, G.C., Isturiz, M.A., Caamano, J. and Palermo, M.S. (2003) Fibrinogen-CD11b/CD18 interaction activates the NF-kappa B pathway and delays apoptosis in human neutrophils. Eur. J. Immunol., 33, 1429-1438.
41. Dhawan, J. and Rando, T.A. (2005) Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol., 15, 666-673.
42. Sanes, J.R. (2003) The basement membrane/basal lamina of skeletal muscle. J. Biol. Chem., 278, 12601-12604.
43. Sinanan, A.C., Machell, J.R., Wynne-Hughes, G.T., Hunt, N.P. and Lewis, M.P. (2008) Alpha v beta 3 and alpha v beta 5 integrins and their role in muscle precursor cell adhesion. Biol. Cell, 100, 465-477.
44. Lygoe, K.A., Norman, J.T., Marshall, J.F. and Lewis, M.P. (2004) AlphaV integrins play an important role in myofibroblast differentiation. Wound Repair Regen., 12, 461-470.
45. Liu, H., Niu, A., Chen, S.E. and Li, Y.P. (2011) Beta3-integrin mediates satellite cell differentiation in regenerating mouse muscle. FASEB J., 25, 1914-1921.
46. Pizza, F.X., Peterson, J.M., Baas, J.H. and Koh, T.J. (2005) Neutrophils contribute to muscle injury and impair its resolution after lengthening contractions in mice. J. Physiol., 562, 899-913.
47. Pizza, F.X., McLoughlin, T.J., McGregor, S.J., Calomeni, E.P. and Gunning, W.T. (2001) Neutrophils injure cultured skeletal myotubes. Am. J. Physiol. Cell Physiol., 281, C335-C341.
48. Spencer, M.J., Montecino-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.
49. Hodgetts, S., Radley, H., Davies, M. and Grounds, M.D. (2006) Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking TNFalpha function with Etanercept in mdx mice. Neuromuscul. Disord., 16, 591-602.
50. Flick, M.J., Du, X. and Degen, J.L. (2004) Fibrin(ogen)-alpha M beta 2 interactions regulate leukocyte function and innate immunity in vivo. Exp. Biol. Med., 229, 1105-1110.
51. Nguyen, H.X. and Tidball, J.G. (2003) Interactions between neutrophils and macrophages promote macrophage killing of rat muscle cells in vitro. J. Physiol., 547, 125-132.
52. Cheung, E.V. and Tidball, J.G. (2003) Administration of the non-steroidal anti-inflammatory drug ibuprofen increases macrophage concentrations but reduces necrosis during modified muscle use. Inflamm. Res., 52, 170-176.
53. Pelosi, L., Giacinti, C., Nardis, C., Borsellino, G., Rizzuto, E., Nicoletti, C., Wannenes, F., Battistini, L., Rosenthal, N., Molinaro, M. et al. (2007) Local expression of IGF-1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines. FASEB J., 21, 1393-1402.
54. Radley, H.G., Davies, M.J. and Grounds, M.D. (2008) Reduced muscle necrosis and long-term benefits in dystrophic mdx mice after cV1q (blockade of TNF) treatment. Neuromuscul. Disord., 18, 227-238.
55. Peterson, J.M. and Guttridge, D.C. (2008) Skeletal muscle diseases, inflammation, and NF-kappaB signaling: insights and opportunities for therapeutic intervention. Int. Rev. Immunol., 27, 375-387.
56. Ahn, H.J., Zamolodchikov, D., Cortes-Canteli, M., Norris, E.H., Glickman, J.F. and Strickland, S. (2010) Alzheimer's disease peptide beta-amyloid interacts with fibrinogen and induces its oligomerization. Proc. Natl Acad. Sci. USA, 107, 21812-21817.
57. Cortes-Canteli, M., Paul, J., Norris, E.H., Bronstein, R., Ahn, H.J., Zamolodchikov, D., Bhuvanendran, S., Fenz, K.M. and Strickland, S. (2010) Fibrinogen and beta-amyloid association alters thrombosis and fibrinolysis: a possible contributing factor to Alzheimer's disease. Neuron, 66, 695-709.
58. Suh, T.T., Holmback, K., Jensen, N.J., Daugherty, C.C., Small, K., Simon, D.I., Potter, S. and Degen, J.L. (1995) Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev., 9, 2020-2033.
59. Hamer, P.W., McGeachie, J.M., Davies, M.J. and Grounds, M.D. (2002) Evans Blue Dye as an in vivo marker of myofibre damage: optimising parameters for detecting initial myofibre membrane permeability. J. Anat., 200, 69-79.
60. Suelves, M., Lopez-Alemany, R., Lluis, F., Aniorte, G., Serrano, E., Parra, M., Carmeliet, P. and Munoz-Canoves, P. (2002) Plasmin activity is required for myogenesis in vitro and skeletal muscle regeneration in vivo. Blood, 99, 2835-2844.
61. Celada, A., Gray, P.W., Rinderknecht, E. and Schreiber, R.D. (1984) Evidence for a gamma-interferon receptor that regulates macrophage tumoricidal activity. J. Exp. Med., 160, 55-74.
62. Ugarova, T.P., Lishko, V.K., Podolnikova, N.P., Okumura, N., Merkulov, S.M., Yakubenko, V.P., Yee, V.C., Lord, S.T. and Haas, T.A. (2003) Sequence gamma 377-395(P2), but not gamma 190-202(P1), is the binding site for the alpha MI-domain of integrin alpha M beta 2 in the gamma C-domain of fibrinogen. Biochemistry, 42, 9365-9373.
63. Perdiguero, E., Ruiz-Bonilla, V., Gresh, L., Hui, L., Ballestar, E., Sousa-Victor, P., Baeza-Raja, B., Jardi, M., Bosch-Comas, A., Esteller, M. et al. (2007) Genetic analysis of p38 MAP kinases in myogenesis: fundamental role of p38alpha in abrogating myoblast proliferation. EMBO J., 7, 1245-1256.