Nitric oxide and muscle repair: Multiple actions converging on therapeutic efficacy

European Journal of Pharmacology

Volumn 730, Issue 1, 2014, Pages 181-185

  Rovere Querini, Patrizia ^a   Clementi, Emilio ^b,c   Brunelli, Silvia ^a,d  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b SCIENTIFIC INSTITUTE   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Keywords; Macrophages; Muscle dystrophy; Nitric oxide; Satellite cells

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; ISOSORBIDE DINITRATE; MOLSIDOMINE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE;

ACUTE DISEASE; CHRONIC DISEASE; DRUG ACTIVITY; DRUG EFFICACY; DRUG MECHANISM; HUMAN; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MUSCLE CHARACTERISTICS AND FUNCTIONS; MUSCLE FUNCTION; MUSCLE INJURY; MUSCLE REPAIR; MUSCULAR DYSTROPHY; NITRIC OXIDE DONATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SATELLITE CELL; SIGNAL TRANSDUCTION; ANIMAL; METABOLISM; MUSCLE; MUSCULAR DYSTROPHIES; PATHOLOGY; PATHOPHYSIOLOGY; SKELETAL MUSCLE SATELLITE CELL;

ANIMALS; HUMANS; MUSCLES; MUSCULAR DYSTROPHIES; NITRIC OXIDE; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84898789429     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.11.006     Document Type: Article

References (56)

1. S. Acharyya, S.A. Villalta, N. Bakkar, T. Bupha-Intr, P.M.L. Janssen, M. Carathers, Z.-W. Li, A.A. Beg, S. Ghosh, Z. Sahenk, M. Weinstein, K.L. Gardner, J.A. Rafael-Fortney, M. Karin, J.G. Tidball, A.S. Baldwin, and D.C. Guttridge Interplay of IKK/NF-kappaB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy J. Clin. Invest. 117 2007 889 901 (Pubitemid 46556745)
2. C.M. Adamo, D.F. Dai, J.M. Percival, E. Minami, M.S. Willis, E. Patrucco, S.C. Froehner, and J.A. Beavo Sildenafil reverses cardiac dysfunction in the mdx mouse model of Duchenne muscular dystrophy Proc. Nat. Acad. Sci. U.S.A. 107 2010 19079 19083
3. J.D. Archer, C.C. Vargas, and J.E. Anderson Persistent and improved functional gain in mdx dystrophic mice after treatment with l-arginine and deflazacort FASEB J. 20 2006 738 740 (Pubitemid 46671199)
4. S.J. Bailey, J. Fulford, A. Vanhatalo, P.G. Winyard, J.R. Blackwell, F.J. DiMenna, D.P. Wilkerson, N. Benjamin, and A.M. Jones Dietary nitrate supplementation enhances muscle contractile efficiency during knee-extensor exercise in humans J. Appl. Physiol. 109 2010 135 148
5. F. Benabdellah, H. Yu, A. Brunelle, O. Laprevote, and S. De La Porte MALDI reveals membrane lipid profile reversion in MDX mice Neurobiol. Dis. 36 2009 252 258
6. D.E. Bowles, S.W. McPhee, C. Li, S.J. Gray, J.J. Samulski, A.S. Camp, J. Li, B. Wang, P.E. Monahan, J.E. Rabinowitz, J.C. Grieger, L. Govindasamy, M. Agbandje-McKenna, X. Xiao, and R.J. Samulski Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector Mol. Ther. 20 2012 443 455
7. J.E. Brenman, D.S. Chao, H. Xia, K. Aldape, and D.S. Bredt Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy Cell 82 1995 743 752
8. S. Brunelli, and P. Rovere-Querini The immune system and the repair of skeletal muscle Pharmacol. Res. 58 2008 117 121
9. S. Brunelli, C. Sciorati, G. D'Antona, A. Innocenzi, D. Covarello, B.G. Galvez, C. Perrotta, A. Monopoli, F. Sanvito, R. Bottinelli, E. Ongini, G. Cossu, and E. Clementi Nitric oxide release combined with nonsteroidal antiinflammatory activity prevents muscular dystrophy pathology and enhances stem cell therapy Proc. Nat. Acad. Sci. U.S.A. 104 2007 264 269 (Pubitemid 46068020)
10. R. Buono, C. Vantaggiato, V. Pisa, E. Azzoni, M.T. Bassi, S. Brunelli, C. Sciorati, and E. Clementi Nitric oxide sustains long-term skeletal muscle regeneration by regulating fate of satellite cells via signaling pathways requiring Vangl2 and cyclic GMP Stem Cells 30 2012 197 209
11. D. Cacchiarelli, J. Martone, E. Girardi, M. Cesana, T. Incitti, M. Morlando, C. Nicoletti, T. Santini, O. Sthandier, L. Barberi, A. Auricchio, A. Musaro, and I. Bozzoni MicroRNAs involved in molecular circuitries relevant for the Duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway Cell Metab. 12 2010 341 351
12. W.J. Chang, S.T. Iannaccone, K.S. Lau, B.S. Masters, T.J. McCabe, K. McMillan, R.C. Padre, M.J. Spencer, J.G. Tidball, and J.T. Stull Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy Proc. Nat. Acad. Sci. U.S.A. 93 1996 9142 9147 (Pubitemid 26282032)
13. S. Cirak, L. Feng, K. Anthony, V. Arechavala-Gomeza, S. Torelli, C. Sewry, J.E. Morgan, and F. Muntoni Restoration of the dystrophin-associated glycoprotein complex after exon skipping therapy in Duchenne muscular dystrophy Mol. Ther. 20 2012 462 467
14. C. Colussi, C. Mozzetta, A. Gurtner, B. Illi, J. Rosati, S. Straino, G. Ragone, M. Pescatori, G. Zaccagnini, A. Antonini, G. Minetti, F. Martelli, G. Piaggio, P. Gallinari, C. Steinkuhler, E. Clementi, C. Dell'Aversana, L. Altucci, A. Mai, M.C. Capogrossi, P.L. Puri, and C. Gaetano HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment Proc. Nat. Acad. Sci. U.S.A. 105 2008 19183 19187
15. M.G. D'Angelo, S. Gandossini, F.M. Boneschi, C. Sciorati, S. Bonato, E. Brighina, G.P. Comi, A.C. Turconi, F. Magri, G. Stefanoni, S. Brunelli, N. Bresolin, D. Cattaneo, and E. Clementi Nitric oxide donor and non steroidal anti inflammatory drugs as a therapy for muscular dystrophies: evidence from a safety study with pilot efficacy measures in adult dystrophic patients Pharmacol. Res. 2012
16. C. De Palma, and E. Clementi Nitric oxide in myogenesis and therapeutic muscle repair Mol. Neurobiol. 46 2012 682 692
17. C. De Palma, S. Falcone, S. Pisoni, S. Cipolat, C. Panzeri, S. Pambianco, A. Pisconti, R. Allevi, M.T. Bassi, G. Cossu, T. Pozzan, S. Moncada, L. Scorrano, S. Brunelli, and E. Clementi Nitric oxide inhibition of Drp1-mediated mitochondrial fission is critical for myogenic differentiation Cell Death Differ. 17 2010 1684 1696
18. V. Dubowitz Prednisone for Duchenne muscular dystrophy Lancet Neurol. 4 2005 264 (Pubitemid 40545032)
19. A.E. Emery The muscular dystrophies Lancet 359 2002 687 695 (Pubitemid 34203773)
20. M. Feelisch, J. Ostrowski, and E. Noack On the mechanism of NO release from sydnonimines J. Cardiovasc. Pharmacol. 14 Suppl. 11 1989 S13 22
21. T. Fulmer The DMD Landscape 2013 BioCentury. BioCentury Publications, Inc.
22. N.M. Goemans, M. Tulinius, J.T. van den Akker, B.E. Burm, P.F. Ekhart, N. Heuvelmans, T. Holling, A.A. Janson, G.J. Platenburg, J.A. Sipkens, J.M. Sitsen, A. Aartsma-Rus, G.J. van Ommen, G. Buyse, N. Darin, J.J. Verschuuren, G.V. Campion, S.J. de Kimpe, and J.C. van Deutekom Systemic administration of PRO051 in Duchenne's muscular dystrophy N. Engl. J. Med. 364 2011 1513 1522
23. R.C. Griggs, B.E. Herr, A. Reha, G. Elfring, L. Atkinson, V. Cwik, E. McColl, R. Tawil, S. Pandya, M.P. McDermott, and K. Bushby Corticosteroids in Duchenne muscular dystrophy: major variations in practice Muscle Nerve 48 2013 27 31
24. A.D. Guerron, R. Rawat, A. Sali, C.F. Spurney, E. Pistilli, H.J. Cha, G.S. Pandey, R. Gernapudi, D. Francia, V. Farajian, D.M. Escolar, L. Bossi, M. Becker, P. Zerr, S. de la Porte, H. Gordish-Dressman, T. Partridge, E.P. Hoffman, and K. Nagaraju Functional and molecular effects of arginine butyrate and prednisone on muscle and heart in the mdx mouse model of Duchenne muscular dystrophy PLoS One 5 2010 e11220
25. M.J. Hickey Role of inducible nitric oxide synthase in the regulation of leucocyte recruitment Clin. Sci. (London) 100 2001 1 12 (Pubitemid 32057801)
26. F.J. Larsen, T.A. Schiffer, S. Borniquel, K. Sahlin, B. Ekblom, J.O. Lundberg, and E. Weitzberg Dietary inorganic nitrate improves mitochondrial efficiency in humans Cell Metab. 13 2011 149 159
27. C. Lepper, T.A. Partridge, and C.M. Fan An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration Development (Cambridge, England) 138 2011 3639 3646
28. D.G. Leung, and K.R. Wagner Therapeutic advances in muscular dystrophy Ann. Neurol. 2013
29. D.M. McCafferty, J.S. Mudgett, M.G. Swain, and P. Kubes Inducible nitric oxide synthase plays a critical role in resolving intestinal inflammation Gastroenterology 112 1997 1022 1027 (Pubitemid 27113830)
30. G.C. Minetti, C. Colussi, R. Adami, C. Serra, C. Mozzetta, V. Parente, S. Fortuni, S. Straino, M. Sampaolesi, M. Di Padova, B. Illi, P. Gallinari, C. Steinkuhler, M.C. Capogrossi, V. Sartorelli, R. Bottinelli, C. Gaetano, and P.L. Puri Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors Nat. Med. 12 2006 1147 1150 (Pubitemid 44527349)
31. J.M. Percival, N.P. Whitehead, M.E. Adams, C.M. Adamo, J.A. Beavo, and S.C. Froehner Sildenafil reduces respiratory muscle weakness and fibrosis in the mdx mouse model of Duchenne muscular dystrophy J. Pathol. 228 2012 77 87
32. C. Pichavant, A. Aartsma-Rus, P.R. Clemens, K.E. Davies, G. Dickson, S. Takeda, S.D. Wilton, J.A. Wolff, C.I. Wooddell, X. Xiao, and J.P. Tremblay Current status of pharmaceutical and genetic therapeutic approaches to treat DMD Mol. Ther. 19 2011 830 840
33. F. Relaix, and P.S. Zammit Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage Development (Cambridge, England) 139 2012 2845 2856
34. E. Rigamonti, T. Touvier, E. Clementi, A.A. Manfredi, S. Brunelli, and P. Rovere-Querini Requirement of inducible nitric oxide synthase for skeletal muscle regeneration after acute damage J. Immunol. 190 2013 1767 1777
35. U.T. Ruegg Pharmacological prospects in the treatment of Duchenne muscular dystrophy Curr. Opin. Neurol. 26 2013 577 584
36. R. Sambasivan, R. Yao, A. Kissenpfennig, L. Van Wittenberghe, A. Paldi, B. Gayraud-Morel, H. Guenou, B. Malissen, S. Tajbakhsh, and A. Galy Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration Development (Cambridge, England) 138 2011 (4333-4333)
37. J. Scharner, and P.S. Zammit The muscle satellite cell at 50: the formative years Skeletal Muscle 1 2011 28
38. W. Schgoer, M. Theurl, J. Jeschke, A.G. Beer, K. Albrecht, R. Gander, S. Rong, D. Vasiljevic, M. Egger, A.M. Wolf, S. Frauscher, B. Koller, I. Tancevski, J.R. Patsch, P. Schratzberger, H. Piza-Katzer, A. Ritsch, F.H. Bahlmann, R. Fischer-Colbrie, D. Wolf, and R. Kirchmair Gene therapy with the angiogenic cytokine secretoneurin induces therapeutic angiogenesis by a nitric oxide-dependent mechanism Circ. Res. 105 2009 994 1002
39. C. Sciorati, R. Buono, E. Azzoni, S. Casati, P. Ciuffreda, G. D'Angelo, D. Cattaneo, S. Brunelli, and E. Clementi Co-administration of ibuprofen and nitric oxide is an effective experimental therapy for muscular dystrophy, with immediate applicability to humans Br. J. Pharmacol. 160 2010 1550 1560
40. C. Sciorati, B.G. Galvez, S. Brunelli, E. Tagliafico, S. Ferrari, G. Cossu, and E. Clementi Ex vivo treatment with nitric oxide increases mesoangioblast therapeutic efficacy in muscular dystrophy J. Cell Sci. 119 2006 5114 5123 (Pubitemid 46085190)
41. C. Sciorati, D. Miglietta, R. Buono, V. Pisa, D. Cattaneo, E. Azzoni, S. Brunelli, and E. Clementi A dual acting compound releasing nitric oxide (NO) and ibuprofen, NCX 320, shows significant therapeutic effects in a mouse model of muscular dystrophy Pharmacol. Res. 64 2011 210 217
42. C. Sciorati, L. Staszewsky, V. Zambelli, I. Russo, M. Salio, D. Novelli, G. Di Grigoli, R.M. Moresco, E. Clementi, and R. Latini Ibuprofen plus isosorbide dinitrate treatment in the mdx mice ameliorates dystrophic heart structure Pharmacol. Res. 73 2013 35 43
43. J.S. Stamler, and G. Meissner Physiology of nitric oxide in skeletal muscle Physiol. Rev. 81 2001 209 237 (Pubitemid 32096176)
44. K. Strle, R.H. McCusker, R.W. Johnson, S.M. Zunich, R. Dantzer, and K.W. Kelley Prototypical anti-inflammatory cytokine IL-10 prevents loss of IGF-I-induced myogenin protein expression caused by IL-1beta Am. J. Physiol. Endocrinol. Metab. 294 2008 E709 718
45. K. Strle, R.H. McCusker, L. Tran, A. King, R.W. Johnson, G.G. Freund, R. Dantzer, and K.W. Kelley Novel activity of an anti-inflammatory cytokine: IL-10 prevents TNFalpha-induced resistance to IGF-I in myoblasts J. Neuroimmunol. 188 2007 48 55 (Pubitemid 47103216)
46. J.G. Tidball, and S.A. Villalta Regulatory interactions between muscle and the immune system during muscle regeneration Am. J. Physiol. Regul. Integr. Comp. Physiol. 298 2010 R1173 1187
47. P. Tripathi, L. Kashyap, and V. Singh The role of nitric oxide in inflammatory reactions FEMS Immunol. Med. Microbiol. 51 2007 443 452 (Pubitemid 350076162)
48. B. Vidal, A.L. Serrano, M. Tjwa, M. Suelves, E. Ardite, R. De Mori, B. Baeza-Raja, M. Martinez de Lagran, P. Lafuste, V. Ruiz-Bonilla, M. Jardi, R. Gherardi, C. Christov, M. Dierssen, P. Carmeliet, J.L. Degen, M. Dewerchin, and P. Munoz-Canoves Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway Genes Dev. 22 2008 1747 1752 (Pubitemid 351915499)
49. S.A. Villalta, B. Deng, C. Rinaldi, M. Wehling-Henricks, and J.G. Tidball IFN-gamma promotes muscle damage in the mdx mouse model of Duchenne muscular dystrophy by suppressing M2 macrophage activation and inhibiting muscle cell proliferation J. Immunol. 187 2011 5419 5428
50. V. Voisin, C. Sebrie, S. Matecki, H. Yu, B. Gillet, M. Ramonatxo, M. Israel, and S. De la Porte l-arginine improves dystrophic phenotype in mdx mice Neurobiol. Dis. 20 2005 123 130 (Pubitemid 41219209)
51. S.M. Wahl, N. McCartney-Francis, J. Chan, R. Dionne, L. Ta, and J.M. Orenstein Nitric oxide in experimental joint inflammation. Benefit or detriment? Cells Tissues Organs 174 2003 26 33 (Pubitemid 36677091)
52. J.L. Wallace, S. Viappiani, and M. Bolla Cyclooxygenase-inhibiting nitric oxide donators for osteoarthritis Trends Pharmacol. Sci. 30 2009 112 117
53. G. Wang, and Q. Lu A nitrate ester of sedative alkyl alcohol improves muscle function and structure in a murine model of Duchenne muscular dystrophy Mol. Pharm. 2013 (130827140244008)
54. M. Wehling, M.J. Spencer, and J.G. Tidball A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice J. Cell Biol. 155 2001 123 131 (Pubitemid 34286213)
55. M. Wehling-Henricks, M.C. Jordan, T. Gotoh, W.W. Grody, K.P. Roos, and J.G. Tidball Arginine metabolism by macrophages promotes cardiac and muscle fibrosis in mdx muscular dystrophy PLoS One 5 2010 e10763
56. P. Zordan, C. Sciorati, L. Campana, L. Cottone, E. Clementi, P.-R. Querini, and S. Brunelli The nitric oxide-donor molsidomine modulates the innate inflammatory response in a mouse model of muscular dystrophy Eur. J. Pharmacol. 715 2013 296 303