Osteopontin-stimulated expression of matrix metalloproteinase-9 causes cardiomyopathy in the mdx model of Duchenne muscular dystrophy

Journal of Immunology

Volumn 187, Issue 5, 2011, Pages 2723-2731

  Dahiya, Saurabh ^a   Givvimani, Srikanth ^a   Bhatnagar, Shephali ^a   Qipshidze, Natia ^a   Tyagi, Suresh C ^a   Kumar, Ashok ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; INTERLEUKIN 1BETA; MACROPHAGE ELASTASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OSTEOPONTIN; PROTEIN KINASE B; STROMELYSIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOMYOPATHY; CONTROLLED STUDY; DISEASE MODEL; DUCHENNE MUSCULAR DYSTROPHY; ECHOCARDIOGRAPHY; ENZYME ACTIVATION; HEART FUNCTION; HEART INJURY; HEART MUSCLE; HEART MUSCLE FIBROSIS; IMMUNOMODULATION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; BLOTTING, WESTERN; CARDIOMYOPATHIES; IMMUNOHISTOCHEMISTRY; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED MDX; MICE, KNOCKOUT; MUSCULAR DYSTROPHY, DUCHENNE; OSTEOPONTIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 80052668815     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101342     Document Type: Article

References (79)

1. Cox, G. F., and L. M. Kunkel. 1997. Dystrophies and heart disease. Curr. Opin. Cardiol. 12: 329-343. (Pubitemid 27252541)
2. Frankel, K. A., and R. J. Rosser. 1976. The pathology of the heart in progressive muscular dystrophy: epimyocardial fibrosis. Hum. Pathol. 7: 375-386.
3. Nigro, G., L. I. Comi, L. Politano, and R. J. Bain. 1990. The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int. J. Cardiol. 26: 271-277. (Pubitemid 20061348)
4. Melacini, P., M. Fanin, D. J. Duggan, M. P. Freda, A. Berardinelli, G. A. Danieli, A. Barchitta, E. P. Hoffman, S. Dalla Volta, and C. Angelini. 1999. Heart involvement in muscular dystrophies due to sarcoglycan gene mutations. Muscle Nerve 22: 473-479. (Pubitemid 29173545)
5. Melacini, P., A. Gambino, A. Caforio, A. Barchitta, M. L. Valente, A. Angelini, M. Fanin, G. Thiene, C. Angelini, D. Casarotto, et al. 2001. Heart transplantation in patients with inherited myopathies associated with end-stage cardiomyopathy: molecular and biochemical defects on cardiac and skeletal muscle. Transplant. Proc. 33: 1596-1599. (Pubitemid 32237987)
6. Sicinski, P., Y. Geng, A. S. Ryder-Cook, E. A. Barnard, M. G. Darlison, and P. J. Barnard. 1989. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244: 1578-1580. (Pubitemid 19189735)
7. Emery, A. E. 2002. The muscular dystrophies. Lancet 359: 687-695. (Pubitemid 34203773)
8. Quinlan, J. G., H. S. Hahn, B. L. Wong, J. N. Lorenz, A. S. Wenisch, and L. S. Levin. 2004. Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscul. Disord. 14: 491-496. (Pubitemid 39141704)
9. Wehling-Henricks, M., M. C. Jordan, K. P. Roos, B. Deng, and J. G. Tidball. 2005. Cardiomyopathy in dystrophin-deficient hearts is prevented by expression of a neuronal nitric oxide synthase transgene in the myocardium. Hum. Mol. Genet. 14: 1921-1933. (Pubitemid 41418029)
10. Bia, B. L., P. J. Cassidy, M. E. Young, J. A. Rafael, B. Leighton, K. E. Davies, G. K. Radda, and K. Clarke. 1999. Decreased myocardial nNOS, increased iNOS and abnormal ECGs in mouse models of Duchenne muscular dystrophy. J. Mol. Cell. Cardiol. 31: 1857-1862. (Pubitemid 29458703)
11. Wilding, J. R., J. E. Schneider, A. E. Sang, K. E. Davies, S. Neubauer, and K. Clarke. 2005. Dystrophin- and MLP-deficient mouse hearts: marked differences in morphology and function, but similar accumulation of cytoskeletal proteins. FASEB J. 19: 79-81. (Pubitemid 40069924)
12. Page-McCaw, A., A. J. Ewald, and Z. Werb. 2007. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8: 221-233.
13. Vu, T. H., and Z. Werb. 2000. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. 14: 2123-2133.
14. Mott, J. D., and Z. Werb. 2004. Regulation of matrix biology by matrix metalloproteinases. Curr. Opin. Cell Biol. 16: 558-564. (Pubitemid 39201241)
15. Chandler, S., K. M. Miller, J. M. Clements, J. Lury, D. Corkill, D. C. Anthony, S. E. Adams, and A. J. Gearing. 1997. Matrix metalloproteinases, tumor necrosis factor and multiple sclerosis: an overview. J. Neuroimmunol. 72: 155-161. (Pubitemid 27062771)
16. Hu, J., P. E. Van den Steen, Q. X. Sang, and G. Opdenakker. 2007. Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat. Rev. Drug Discov. 6: 480-498. (Pubitemid 47064570)
17. Waubant, E., D. E. Goodkin, L. Gee, P. Bacchetti, R. Sloan, T. Stewart, P. B. Andersson, G. Stabler, and K. Miller. 1999. Serum MMP-9 and TIMP-1 levels are related to MRI activity in relapsing multiple sclerosis. Neurology 53: 1397-1401. (Pubitemid 29491927)
18. Höyhtyä, M., E. Hujanen, T. Turpeenniemi-Hujanen, U. Thorgeirsson, L. A. Liotta, and K. Tryggvason. 1990. Modulation of type-IV collagenase activity and invasive behavior of metastatic human melanoma (A2058) cells in vitro by monoclonal antibodies to type-IV collagenase. Int. J. Cancer 46: 282-286. (Pubitemid 20252091)
19. Turpeenniemi-Hujanen, T., U. P. Thorgeirsson, I. R. Hart, S. S. Grant, and L. A. Liotta. 1985. Expression of collagenase IV (basement membrane collagenase) activity in murine tumor cell hybrids that differ in metastatic potential. J. Natl. Cancer Inst. 75: 99-103. (Pubitemid 15005962)
20. Kumar, A., S. Bhatnagar, and A. Kumar. 2010. Matrix metalloproteinase inhibitor batimastat alleviates pathology and improves skeletal muscle function in dystrophin-deficient mdx mice. Am. J. Pathol. 177: 248-260.
21. Kherif, S., M. Dehaupas, C. Lafuma, M. Fardeau, and H. S. Alameddine. 1998. Matrix metalloproteinases MMP-2 and MMP-9 in denervated muscle and injured nerve. Neuropathol. Appl. Neurobiol. 24: 309-319. (Pubitemid 28389128)
22. Miyazaki, D., A. Nakamura, K. Fukushima, K. Yoshida, S. Takeda, and S. I. Ikeda. 2011. Matrix metalloproteinase-2 ablation in dystrophin-deficient mdx muscles reduces angiogenesis resulting in impaired growth of regenerated muscle fibers. Hum. Mol. Genet. 20: 1787-1799.
23. Li, H., A. Mittal, D. Y. Makonchuk, S. Bhatnagar, and A. Kumar. 2009. Matrix metalloproteinase-9 inhibition ameliorates pathogenesis and improves skeletal muscle regeneration in muscular dystrophy. Hum. Mol. Genet. 18: 2584-2598.
24. Kherif, S., C. Lafuma, M. Dehaupas, S. Lachkar, J. G. Fournier, M. Verdière-Sahuqué, M. Fardeau, and H. S. Alameddine. 1999. Expression of matrix metalloproteinases 2 and 9 in regenerating skeletal muscle: a study in experimentally injured and mdx muscles. Dev. Biol. 205: 158-170. (Pubitemid 29042665)
25. Beggs, A. H. 1997. Dystrophinopathy, the expanding phenotype. Dystrophin abnormalities in X-linked dilated cardiomyopathy. Circulation 95: 2344-2347. (Pubitemid 27224725)
26. Wang, K. X., and D. T. Denhardt. 2008. Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev. 19: 333-345.
27. Chen, Y. J., Y. Y. Wei, H. T. Chen, Y. C. Fong, C. J. Hsu, C. H. Tsai, H. C. Hsu, S. H. Liu, and C. H. Tang. 2009. Osteopontin increases migration and MMP-9 up-regulation via alphavbeta3 integrin, FAK, ERK, and NF-kappaB-dependent pathway in human chondrosarcoma cells. J. Cell. Physiol. 221: 98-108.
28. Rangaswami, H., A. Bulbule, and G. C. Kundu. 2004. Nuclear factor-inducing kinase plays a crucial role in osteopontin-induced MAPK/IkappaBalpha kinase-dependent nuclear factor kappaB-mediated promatrix metalloproteinase-9 activation. J. Biol. Chem. 279: 38921-38935. (Pubitemid 39296053)
29. Vetrone, S. A., E. Montecino-Rodriguez, E. Kudryashova, I. Kramerova, E. P. Hoffman, S. D. Liu, M. C. Miceli, and M. J. Spencer. 2009. Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-beta. J. Clin. Invest. 119: 1583-1594.
30. Waller, A. H., M. Sanchez-Ross, E. Kaluski, and M. Klapholz. 2010. Osteopontin in cardiovascular disease: a potential therapeutic target. Cardiol. Rev. 18: 125-131.
31. Kumar, A., S. Bhatnagar, and A. Kumar. 2010. Matrix metalloproteinase inhibitor batimastat alleviates pathology and improves skeletal muscle function in dystrophin-deficient mdx mice. Am. J. Pathol. 177: 248-260.
32. Mishra, P. K., S. Givvimani, N. Metreveli, and S. C. Tyagi. 2010. Attenuation of beta2-adrenergic receptors and homocysteine metabolic enzymes cause diabetic cardiomyopathy. Biochem. Biophys. Res. Commun. 401: 175-181.
33. Qipshidze, N., N. Tyagi, U. Sen, S. Givvimani, N. Metreveli, D. Lominadze, and S. C. Tyagi. 2010. Folic acid mitigated cardiac dysfunction by normalizing the levels of tissue inhibitor of metalloproteinase and homocysteine-metabolizing enzymes postmyocardial infarction in mice. Am. J. Physiol. Heart Circ. Physiol. 299: H1484-H1493.
34. Straub, V., J. A. Rafael, J. S. Chamberlain, and K. P. Campbell. 1997. Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J. Cell Biol. 139: 375-385. (Pubitemid 27459311)
35. Khurana, T. S., and K. E. Davies. 2003. Pharmacological strategies for muscular dystrophy. Nat. Rev. Drug Discov. 2: 379-390. (Pubitemid 37361708)
36. Kumar, A., and A. M. Boriek. 2003. Mechanical stress activates the nuclear factor-kappaB pathway in skeletal muscle fibers: a possible role in Duchenne muscular dystrophy. FASEB J. 17: 386-396. (Pubitemid 36292954)
37. Miner, E. C., and W. L. Miller. 2006. A look between the cardiomyocytes: the extracellular matrix in heart failure. Mayo Clin. Proc. 81: 71-76. (Pubitemid 43054320)
38. McCawley, L. J., and L. M. Matrisian. 2001. Matrix metalloproteinases: they're not just for matrix anymore! Curr. Opin. Cell Biol. 13: 534-540. (Pubitemid 32817010)
39. Nagase, H., and J. F. Woessner Jr. 1999. Matrix metalloproteinases. J. Biol. Chem. 274: 21491-21494. (Pubitemid 129519680)
40. Li, Y. Y., and A. M. Feldman. 2001. Matrix metalloproteinases in the progression of heart failure: potential therapeutic implications. Drugs 61: 1239-1252.
41. Fingleton, B. 2007. Matrix metalloproteinases as valid clinical targets. Curr. Pharm. Des. 13: 333-346. (Pubitemid 46085282)
42. Bhatnagar, S., and A. Kumar. 2010. Therapeutic targeting of signaling pathways in muscular dystrophy. J. Mol. Med. 88: 155-166.
43. Lapidos, K. A., R. Kakkar, and E. M. McNally. 2004. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ. Res. 94: 1023-1031. (Pubitemid 38579696)
44. Towbin, J. A., K. R. Bowles, and N. E. Bowles. 1999. Etiologies of cardiomyopathy and heart failure. Nat. Med. 5: 266-267. (Pubitemid 29124355)
45. McNally, E., M. Allikian,M. T. Wheeler, J.M.Mislow, and A. Heydemann. 2003. Cytoskeletal defects in cardiomyopathy. J. Mol. Cell. Cardiol. 35: 231-241. (Pubitemid 36379168)
46. Rando, T. A. 2001. The dystrophin-glycoprotein complex, cellular signaling, and the regulation of cell survival in the muscular dystrophies. Muscle Nerve 24: 1575-1594. (Pubitemid 33101403)
47. Fingleton, B. 2008. MMPs as therapeutic targets - still a viable option? Semin. Cell Dev. Biol. 19: 61-68. (Pubitemid 350235985)
48. Mann, D. L., and F. G. Spinale. 1998. Activation of matrix metalloproteinases in the failing human heart: breaking the tie that binds. Circulation 98: 1699-1702. (Pubitemid 28492487)
49. Romanic, A. M., C. L. Burns-Kurtis, B. Gout, I. Berrebi-Bertrand, and E. H. Ohlstein. 2001. Matrix metalloproteinase expression in cardiac myocytes following myocardial infarction in the rabbit. Life Sci. 68: 799-814. (Pubitemid 32168010)
50. Danielsen, C. C., H. Wiggers, and H. R. Andersen. 1998. Increased amounts of collagenase and gelatinase in porcine myocardium following ischemia and reperfusion. J. Mol. Cell. Cardiol. 30: 1431-1442. (Pubitemid 28345043)
51. Lu, L., Z. Gunja-Smith, J. F. Woessner, P. C. Ursell, T. Nissen, R. E. Galardy, Y. Xu, P. Zhu, and G. G. Schwartz. 2000. Matrix metalloproteinases and collagen ultrastructure in moderate myocardial ischemia and reperfusion in vivo. Am. J. Physiol. Heart Circ. Physiol. 279: H601-H609.
52. Li, Y. Y., A. M. Feldman, Y. Sun, and C. F. McTiernan. 1998. Differential expression of tissue inhibitors of metalloproteinases in the failing human heart. Circulation 98: 1728-1734. (Pubitemid 28492492)
53. Tyagi, S. C., S. G. Kumar, S. J. Haas, H. K. Reddy, D. J. Voelker, M. R. Hayden, T. L. Demmy, R. A. Schmaltz, and J. J. Curtis. 1996. Post-transcriptional regulation of extracellular matrix metalloproteinase in human heart end-stage failure secondary to ischemic cardiomyopathy. J. Mol. Cell. Cardiol. 28: 1415-1428. (Pubitemid 26340896)
54. Ducharme, A., S. Frantz, M. Aikawa, E. Rabkin, M. Lindsey, L. E. Rohde, F. J. Schoen, R. A. Kelly, Z. Werb, P. Libby, and R. T. Lee. 2000. Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J. Clin. Invest. 106: 55-62. (Pubitemid 30437240)
55. Tidball, J. G., and M. Wehling-Henricks. 2005. Damage and inflammation in muscular dystrophy: potential implications and relationships with autoimmune myositis. Curr. Opin. Rheumatol. 17: 707-713. (Pubitemid 41546488)
56. Engvall, E., and U. M. Wewer. 2003. The new frontier in muscular dystrophy research: booster genes. FASEB J. 17: 1579-1584. (Pubitemid 37100059)
57. Khurana, T. S., and K. E. Davies. 2003. Pharmacological strategies for muscular dystrophy. Nat. Rev. Drug Discov. 2: 379-390. (Pubitemid 37361708)
58. Spencer, M. J., and J. G. Tidball. 2001. Do immune cells promote the pathology of dystrophin-deficient myopathies? Neuromuscul. Disord. 11: 556-564. (Pubitemid 32761799)
59. Spencer, M. J., C. M. Walsh, K. A. Dorshkind, E. M. Rodriguez, and J. G. Tidball. 1997. Myonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity. J. Clin. Invest. 99: 2745-2751. (Pubitemid 27259822)
60. Spencer, M. J., E. Montecino-Rodriguez, K. Dorshkind, and J. G. Tidball. 2001. Helper (CD4(+)) and cytotoxic (CD8(+)) T cells promote the pathology of dystrophin-deficient muscle. Clin. Immunol. 98: 235-243.
61. Wehling-Henricks, M., S. Sokolow, J. J. Lee, K. H. Myung, S. A. Villalta, and J. G. Tidball. 2008. Major basic protein-1 promotes fibrosis of dystrophic muscle and attenuates the cellular immune response in muscular dystrophy. Hum. Mol. Genet. 17: 2280-2292.
62. Morrison, J., D. B. Palmer, S. Cobbold, T. Partridge, and G. Bou-Gharios. 2005. Effects of T-lymphocyte depletion on muscle fibrosis in the mdx mouse. Am. J. Pathol. 166: 1701-1710. (Pubitemid 40734393)
63. Takafuji, V., M. Forgues, E. Unsworth, P. Goldsmith, and X. W. Wang. 2007. An osteopontin fragment is essential for tumor cell invasion in hepatocellular carcinoma. Oncogene 26: 6361-6371. (Pubitemid 47494216)
64. Yu, Q., and I. Stamenkovic. 2000. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 14: 163-176. (Pubitemid 30070982)
65. Raffetto, J. D., and R. A. Khalil. 2008. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem. Pharmacol. 75: 346-359. (Pubitemid 350298459)
66. Ohtsuka, T., K. Nishimura, A. Kurata, A. Ogimoto, H. Okayama, and J. Higaki. 2007. Serum matrix metalloproteinase-3 as a novel marker for risk stratification of patients with nonischemic dilated cardiomyopathy. J. Card. Fail. 13: 752-758. (Pubitemid 350051977)
67. Dwivedi, A., S. C. Slater, and S. J. George. 2009. MMP-9 and -12 cause Ncadherin shedding and thereby beta-catenin signalling and vascular smooth muscle cell proliferation. Cardiovasc. Res. 81: 178-186.
68. Johnson, J. L., L. Devel, B. Czarny, S. J. George, C. L. Jackson, V. Rogakos, F. Beau, A. Yiotakis, A. C. Newby, and V. Dive. 2011. A selective matrix metalloproteinase-12 inhibitor retards atherosclerotic plaque development in apolipoprotein E-knockout mice. Arterioscler. Thromb. Vasc. Biol. 31: 528-535.
69. Johnson, J. L., S. J. George, A. C. Newby, and C. L. Jackson. 2005. Divergent effects of matrix metalloproteinases 3, 7, 9, and 12 on atherosclerotic plaque stability in mouse brachiocephalic arteries. Proc. Natl. Acad. Sci. USA 102: 15575-15580. (Pubitemid 41528098)
70. Dogra, C., H. Changotra, J. E. Wergedal, and A. Kumar. 2006. Regulation of phosphatidylinositol 3-kinase (PI3K)/Akt and nuclear factor-kappa B signaling pathways in dystrophin-deficient skeletal muscle in response to mechanical stretch. J. Cell. Physiol. 208: 575-585. (Pubitemid 44141882)
71. Kumar, A., N. Khandelwal, R. Malya, M. B. Reid, and A. M. Boriek. 2004. Loss of dystrophin causes aberrant mechanotransduction in skeletal muscle fibers. FASEB J. 18: 102-113. (Pubitemid 38076470)
72. Kolodziejczyk, S. M., G. S. Walsh, K. Balazsi, P. Seale, J. Sandoz, A. M. Hierlihy, M. A. Rudnicki, J. S. Chamberlain, F. D. Miller, and L. A. Megeney. 2001. Activation of JNK1 contributes to dystrophic muscle pathogenesis. Curr. Biol. 11: 1278-1282. (Pubitemid 32774085)
73. Hnia, K., J. Gayraud, G. Hugon, M. Ramonatxo, S. De La Porte, S. Matecki, and D. Mornet. 2008. L-arginine decreases inflammation and modulates the nuclear factor-kappaB/matrix metalloproteinase cascade in mdx muscle fibers. Am. J. Pathol. 172: 1509-1519. (Pubitemid 351793345)
74. Nakamura, A., K. Yoshida, S. Takeda, N. Dohi, and S. Ikeda. 2002. Progression of dystrophic features and activation of mitogen-activated protein kinases and calcineurin by physical exercise, in hearts of mdx mice. FEBS Lett. 520: 18-24. (Pubitemid 34607266)
75. Nakamura, A., G. V. Harrod, and K. E. Davies. 2001. Activation of calcineurin and stress activated protein kinase/p38-mitogen activated protein kinase in hearts of utrophin-dystrophin knockout mice. Neuromuscul. Disord. 11: 251-259. (Pubitemid 32288795)
76. Acharyya, S., S. A. Villalta, N. Bakkar, T. Bupha-Intr, P. M. Janssen, M. Carathers, Z. W. Li, A. A. Beg, S. Ghosh, Z. Sahenk, et al. 2007. Interplay of IKK/NF-kappaB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J. Clin. Invest. 117: 889-901. (Pubitemid 46556745)
77. Evans-Anderson, H. J., C. M. Alfieri, and K. E. Yutzey. 2008. Regulation of cardiomyocyte proliferation and myocardial growth during development by FOXO transcription factors. Circ. Res. 102: 686-694. (Pubitemid 351457856)
78. Kumar, M., D. Y. Makonchuk, H. Li, A. Mittal, and A. Kumar. 2009. TNF-like weak inducer of apoptosis (TWEAK) activates proinflammatory signaling pathways and gene expression through the activation of TGF-beta-activated kinase 1. J. Immunol. 182: 2439-2448.
79. Li, H., A. Mittal, P. K. Paul, M. Kumar, D. S. Srivastava, S. C. Tyagi, and A. Kumar. 2009. Tumor necrosis factor-related weak inducer of apoptosis augments matrix metalloproteinase 9 (MMP-9) production in skeletal muscle through the activation of nuclear factor-kappaB-inducing kinase and p38 mitogen-activated protein kinase: a potential role of MMP-9 in myopathy. J. Biol. Chem. 284: 4439-4450.