Long-term treatment with naproxcinod significantly improves skeletal and cardiac disease phenotype in the mdx mouse model of dystrophy

Human Molecular Genetics

Volumn 23, Issue 12, 2014, Pages 3239-3249

  Uaesoontrachoon, Kitipong ^a   Quinn, James L ^a   Tatem, Kathleen S ^a   Van Der Meulen, Jack H ^a   Yu, Qing ^a   Phadke, Aditi ^a   Miller, Brittany K ^a   Gordish Dressman, Heather ^a,b   Ongini, Ennio ^c   Miglietta, Daniela ^c   Nagaraju, Kanneboyina ^a,b  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c Nicox Research Institute   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

NAPROXCINOD; PREDNISOLONE; ANTIINFLAMMATORY AGENT; NAPROXEN; NAPROXEN-N-BUTYL NITRATE; NITRIC OXIDE DONOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MONITOR; BONE DISEASE; CONTROLLED STUDY; DOSE RESPONSE; DUCHENNE MUSCULAR DYSTROPHY; ECHOCARDIOGRAPHY; ECHOGRAPH; FLUORESCENCE IMAGING; FOOD; FORELIMB; FUNCTIONAL STATUS; GRIP STRENGTH; HEART DISEASE; HEART EJECTION FRACTION; HEART FUNCTION; HINDLIMB; IMAGING SOFTWARE; IN VITRO STUDY; LOCOMOTION; LONG TERM CARE; MALE; MOUSE; MOUSE MODEL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SYSTOLIC BLOOD PRESSURE; TREADMILL EXERCISE; WILD TYPE; ANALOGS AND DERIVATIVES; ANIMAL; BODY WEIGHT; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; HEART FUNCTION TEST; MUSCULAR DYSTROPHY, DUCHENNE; PATHOLOGY; PATHOPHYSIOLOGY; SKELETAL MUSCLE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BODY WEIGHT; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HEART FUNCTION TESTS; HINDLIMB; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; NAPROXEN; NITRIC OXIDE DONORS; PREDNISOLONE;

EID: 84901323501     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu033     Document Type: Article

References (64)

1. Roses, A.D., Herbstreith, M.H. and Appel, S.H. (1975) Membrane protein kinase alteration in Duchenne muscular dystrophy. Nature, 254, 350-351.
2. Hoffman, E.P. and Schwartz, L. (1991) Dystrophin and disease. Mol Aspects Med, 12, 175-194.
3. Hoffman, E.P., Brown, R.H. Jr and Kunkel, L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell, 51, 919-928.
4. Ervasti, J.M., Ohlendieck, K., Kahl, S.D., Gaver, M.G. and Campbell, K.P. (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature, 345, 315-319.
5. Ohlendieck, K. and Campbell, K.P. (1991) Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J Cell Biol, 115, 1685-1694.
6. Hutter, O.F., Burton, F.L. and Bovell, D.L. (1991) Mechanical properties of normal and mdx mouse sarcolemma: bearing on function of dystrophin. J Muscle Res Cell Motil, 12, 585-589.
7. Menke, A. and Jockusch, H. (1991) Decreased osmotic stability of dystrophin-less muscle cells from the mdx mouse. Nature, 349, 69-71.
8. Menke, A. and Jockusch, H. (1995) Extent of shock-induced membrane leakage in human and mouse myotubes depends on dystrophin. J Cell Sci, 108 (Pt 2), 727-733.
9. Pasternak, C., Wong, S. and Elson, E.L. (1995) Mechanical function of dystrophin in muscle cells. J Cell Biol, 128, 355-361.
10. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A.M. and Sweeney, H.L. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA, 90, 3710-3714.
11. Deconinck, N. and Dan, B. (2007) Pathophysiology of Duchenne muscular dystrophy: current hypotheses. Pediatr Neurol, 36, 1-7.
12. Emery, A.E. and Burt, D. (1980) Intracellular calcium and pathogenesis and antenatal diagnosis of Duchenne muscular dystrophy. Br Med J, 280, 355-357.
13. Fong, P.Y., Turner, P.R., Denetclaw, W.F. and Steinhardt, R.A. (1990) Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science, 250, 673-676.
14. Turner, P.R., Westwood, T., Regen, C.M. and Steinhardt, R.A. (1988) Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature, 335, 735-738.
15. McArdle, A., Edwards, R.H. and Jackson, M.J. (1994) Time course of changes in plasma membrane permeability in the dystrophin-deficient mdx mouse. Muscle Nerve, 17, 1378-1384.
16. Emery, A.E. (2002) The muscular dystrophies. Lancet, 359, 687-695.
17. Matsuda,R.,Nishikawa,A. and Tanaka,H. (1995)Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle. J Biochem, 118, 959-964.
18. Brenman, J.E., Chao, D.S., Xia, H., Aldape, K. and Bredt, D.S. (1995) Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell, 82, 743-752.
19. Chang, W.J., Iannaccone, S.T., Lau, K.S., Masters, B.S., McCabe, T.J., McMillan, K., Padre, R.C., Spencer, M.J., Tidball, J.G. and Stull, J.T. (1996) Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci USA, 93, 9142-9147.
20. Stamler, J.S. and Meissner, G. (2001) Physiology of nitric oxide in skeletal muscle. Physiol Rev, 81, 209-237.
21. De Palma, C. and Clementi, E. (2012) Nitric oxide in myogenesis and therapeutic muscle repair. Mol Neurobiol, 46, 682-692.
22. Lai, Y., Thomas, G.D., Yue, Y., Yang, H.T., Li, D., Long, C., Judge, L., Bostick, B., Chamberlain, J.S., Terjung, R.L. et al. (2009) Dystrophins carrying spectrin-like repeats 16 and 17 anchornNOSto the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J Clin Invest, 119, 624-635.
23. Sander, M., Chavoshan, B., Harris, S.A., Iannaccone, S.T., Stull, J.T., Thomas, G.D. and Victor, R.G. (2000) Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc Natl Acad Sci USA, 97, 13818-13823.
24. Thomas, G.D., Sander, M., Lau, K.S., Huang, P.L., Stull, J.T. and Victor, R.G. (1998) Impaired metabolic modulation of alpha-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc Natl Acad Sci USA, 95, 15090-15095.
25. Li, D., Yue, Y., Lai, Y., Hakim, C.H. and Duan, D. (2011) Nitrosative stress elicited by nNOSmicro delocalization inhibits muscle force in dystrophin-null mice. J Pathol, 223, 88-98.
26. Lai, Y., Zhao, J., Yue, Y. and Duan, D. (2013) alpha2 and alpha3 helices of dystrophinR16andR17frame amicrodomain inthe alpha1helixofdystrophin R17 for neuronal NOS binding. Proc Natl Acad Sci USA, 110, 525-530.
27. Schnitzer, T.J., Kivitz, A.J., Lipetz, R.S., Sanders, N. and Hee, A. (2005) Comparison of the COX-inhibiting nitric oxide donator AZD3582 and rofecoxib in treating the signs and symptoms of osteoarthritis of the knee. Arthritis Rheum, 53, 827-837.
28. Wallace, J.L., Viappiani, S. and Bolla, M. (2009) Cyclooxygenase-inhibiting nitric oxide donators for osteoarthritis. Trends Pharmacol Sci, 30, 112-117.
29. White, W.B., Schnitzer, T.J., Fleming, R., Duquesroix, B. and Beekman, M. (2009) Effects of the cyclooxygenase inhibiting nitric oxide donator naproxcinod versus naproxen on systemic blood pressure in patients with osteoarthritis. Am J Cardiol, 104, 840-845.
30. Karlsson, J., Pivodic, A., Aguirre, D. and Schnitzer, T.J. (2009) Efficacy, safety, and tolerability of the cyclooxygenase-inhibiting nitric oxide donator naproxcinod in treating osteoarthritis of the hip or knee. J Rheumatol, 36, 1290-1297.
31. 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.
32. Thomas, G.D., Ye, J., De Nardi, C., Monopoli, A., , E. and Victor, R.G. (2012) Treatment with a nitric oxide-donating NSAID alleviates functional muscle ischemia in the mousemodelof Duchenne muscular dystrophy.PLoS One, 7, e49350.
33. Sciorati, C., Miglietta, D., Buono, R., Pisa, V., Cattaneo, D., Azzoni, E., Brunelli, S. and Clementi, E. (2011)Adual acting compound releasing nitric oxide (NO) and ibuprofen,NCX320, shows significant therapeutic effects in a mouse model of muscular dystrophy. Pharmacol Res, 64, 210-217.
34. Manzur, A.Y., Kinali,M.and Muntoni, F. (2008) Update on the management of Duchenne muscular dystrophy. Arch Dis Child, 93, 986-990.
35. Collins, C.A. and Morgan, J.E. (2003) Duchenne's muscular dystrophy: animal models used to investigate pathogenesis and develop therapeutic strategies. Int J Exp Pathol, 84, 165-172.
36. Fisher, I., Abraham, D., Bouri, K., Hoffman, E.P., Muntoni, F. and Morgan, J. (2005) Prednisolone-induced changes in dystrophic skeletal muscle. FASEB J, 19, 834-836.
37. Griggs, R.C., Moxley, R.T. 3rd, Mendell, J.R., Fenichel, G.M., Brooke, M.H., Pestronk, A., Miller, J.P., Cwik, V.A., Pandya, S., Robison, J. et al. (1993) Duchenne dystrophy: randomized, controlled trial of prednisone (18 months) and azathioprine (12 months). Neurology, 43, 520-527.
38. Moxley, R.T. 3rd, Ashwal, S., Pandya, S., Connolly, A., Florence, J., Mathews, K., Baumbach, L., McDonald, C., Sussman, M., Wade, C. et al. (2005) Practice parameter: corticosteroid treatment of Duchenne dystrophy: report of the Quality Standards Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society. Neurology, 64, 13-20.
39. Drachman, D.B., Toyka, K.V. and Myer, E. (1974) Prednisone in Duchenne muscular dystrophy. Lancet, 2, 1409-1412.
40. Sali, A., Guerron, A.D., Gordish-Dressman, H., Spurney, C.F., Iantorno, M., Hoffman, E.P. and Nagaraju, K. (2012) Glucocorticoid-treated mice are an inappropriate positive control for long-term preclinical studies in the mdx mouse. PLoS One, 7, e34204.
41. Huynh, T., Uaesoontrachoon, K., Quinn, J.L., Tatem, K.S., Heier, C.R., Van Der Meulen, J.H., Yu, Q., Harris, M., Nolan, C.J., Haegeman, G. et al. (2013) Selective modulation through the glucocorticoid receptor ameliorates muscle pathology in mdx mice. J Pathol, 231, 223-235.
42. Bodine, S.C., Latres, E., Baumhueter, S., Lai, V.K., Nunez, L., Clarke, B.A., Poueymirou, W.T., Panaro, F.J., Na, E., Dharmarajan, K. et al. (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science, 294, 1704-1708.
43. Shin, Y.S., Fink, H., Khiroya, R., Ibebunjo, C. and Martyn, J. (2000) Prednisolone-induced muscle dysfunction is caused more by atrophy than by altered acetylcholine receptor expression. Anesth Analg, 91, 322-328.
44. Keeling, R.M., Golumbek, P.T., Streif, E.M. and Connolly, A.M. (2007) Weekly oral prednisolone improves survival and strength in male mdx mice. Muscle Nerve, 35, 43-48.
45. Granchelli, J.A., Pollina, C. and Hudecki, M.S. (2000) Pre-clinical screening of drugs using the mdx mouse. Neuromuscul Disord, 10, 235-239.
46. Huynh, T., Uaesoontrachoon, K., Quinn, J.L., Tatem, K.S., Heier, C.R., Van Der Meulen, J.H., Yu, Q., Harris, M., Nolan, C.J., Haegeman, G. et al. (2013) Selective modulation through the glucocorticoid receptor ameliorates muscle pathology in mdx mice. J Pathol, 231, 223-235.
47. Schakman, O., Kalista, S., Barbe, C., Loumaye, A. and Thissen, J.P. (2013) Glucocorticoid-induced skeletal muscle atrophy. Int J Biochem Cell Biol, 45, 2163-2172.
48. McNally, E.M. (2007) New approaches in the therapy of cardiomyopathy in muscular dystrophy. Annu Rev Med, 58, 75-88.
49. Rumyantsev, P.P. (1977) Interrelations of the proliferation and differentiation processes during cardiac myogenesis and regeneration. Int Rev Cytol, 51, 186-273.
50. Van Erp, C., Irwin, N.G. and Hoey, A.J. (2006) Long-term administration of pirfenidone improves cardiac functioninmdxmice.MuscleNerve,34,327-334.
51. Bostick, B., Yue, Y., Long, C., Marschalk, N., Fine, D.M., Chen, J. and Duan, D. (2009) Cardiac expression of a mini-dystrophin that normalizes skeletal muscle force only partially restores heart function in aged Mdx mice. Mol Ther, 17, 253-261.
52. Wu, B.,Moulton,H.M., Iversen, P.L., Jiang, J., Li, J., Spurney, C.F., Sali,A.,Guerron,A.D.,Nagaraju,K., Doran, T. et al. (2008) Effective rescue of dystrophin improves cardiac function in dystrophin-deficient mice by amodified morpholino oligomer. Proc Natl Acad Sci USA, 105, 14814-14819.
53. Guerron, A.D., Rawat, R., Sali, A., Spurney, C.F., Pistilli, E., Cha, H.J., Pandey, G.S., Gernapudi, R., Francia, D., Farajian, V. et al. (2010) Functional and molecular effects of arginine butyrate and prednisone on muscle and heart in themdxmousemodel of Duchenne Muscular Dystrophy. PLoS One, 5, e11220.
54. Gilroy, J., Cahalan, J.L., Berman, R. and Newman, M. (1963) Cardiac and pulmonary complications in Duchenne's progressive muscular dystrophy. Circulation, 27, 484-493.
55. Melacini, P., Vianello, A., Villanova, C., Fanin, M., Miorin, M., Angelini, C. and Dalla Volta, S. (1996) Cardiac and respiratory involvement in advanced stage Duchenne muscular dystrophy. Neuromuscul Disord, 6, 367-376.
56. Tidball, J.G. (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol, 288, R345-R353.
57. Lynch, G.S., Hinkle, R.T., Chamberlain, J.S., Brooks, S.V. and Faulkner, J.A. (2001) Force and power output of fast and slow skeletal muscles from mdx mice 6-28 months old. J Physiol, 535, 591-600.
58. Van der Meulen, J.H., Kuipers, H. and Drukker, J. (1991) Relationship between exercise-induced muscle damage and enzyme release in rats. J Appl Physiol, 71, 999-1004.
59. Komulainen, J. and Vihko, V. (1994) Exercise-induced necrotic muscle damage and enzyme release in the four days following prolonged submaximal running in rats. Pflugers Arch, 428, 346-351.
60. Friden, J. and Lieber, R.L. (2001) Serum creatine kinase level is a poor predictor ofmusclefunctionafter injury. ScandJMedSciSports,11, 126-127.
61. Dahlqvist, J.R., Voss, L.G., Lauridsen, T., Krag, T.O. and Vissing, J. (2013) A pilot study of muscle plasma protein changes following exercise. Muscle Nerve, 49, 261-266.
62. Spurney, C.F., Gordish-Dressman, H., Guerron, A.D., Sali, A., Pandey, G.S., Rawat, R., Van Der Meulen, J.H., Cha, H.J., Pistilli, E.E., Partridge, T.A. et al. (2009) Preclinical drug trials in the mdx mouse: assessment of reliable and sensitive outcome measures. Muscle Nerve, 39, 591-602.
63. Spurney, C.F., Knoblach, S., Pistilli, E.E., Nagaraju, K., Martin, G.R. and Hoffman, E.P. (2008) Dystrophin-deficient cardiomyopathy in mouse: expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart. Neuromuscul Disord, 18, 371-381.
64. Baudy, A.R., Sali, A., Jordan, S., Kesari, A., Johnston, H.K., Hoffman, E.P. and Nagaraju, K. (2011) Non-invasive optical imaging of muscle pathology inmdxmice using cathepsin caged near-infrared imaging.MolImaging Biol, 13, 462-470.