A nitrate ester of sedative alkyl alcohol improves muscle function and structure in a murine model of duchenne muscular dystrophy

Molecular Pharmaceutics

Volumn 10, Issue 10, 2013, Pages 3862-3870

  Wang, Guqi ^a   Lu, Qilong ^a  

^a CAROLINAS MEDICAL CENTER   (United States)

Author keywords

Duchenne muscular dystrophy; Muscle relaxant; Myogenin; Myostatin; Nitric oxide; Skeletal muscle

Indexed keywords

2 METHYL 2 [(NITROOXY)METHYL]PENTYL NITRATE; 2 METHYL 2 N PROPYL 1,3 PROPANEDIOL; ALKANOL; CREATINE KINASE; MEPROBAMATE; MUSCLE RELAXANT AGENT; NITRIC ACID DERIVATIVE; NITRIC OXIDE; PROPANEDIOL DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CALCIUM CELL LEVEL; CONTROLLED STUDY; CREATINE KINASE BLOOD LEVEL; DRUG EFFECT; DRUG SYNTHESIS; DUCHENNE MUSCULAR DYSTROPHY; ENDURANCE TRAINING; HUMAN; HUMAN CELL; MALE; MOUSE; MUSCLE FUNCTION; MUSCLE RELAXATION; NONHUMAN; PATHOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; MALE; MICE; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; MYOSTATIN; NEUROMUSCULAR AGENTS; NITRIC OXIDE;

EID: 84888311830     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp400310r     Document Type: Article

References (57)

1. Hoffman, E. P.; Brown, R. H., Jr.; Kunkel, L. M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987, 51 (6), 919-28.
2. Ervasti, J. M.; Ohlendieck, K.; Kahl, S. D.; Gaver, M. G.; Campbell, K. P. Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 1990, 345 (6273), 315-9.
3. Sander, M.; Chavoshan, B.; Harris, S. A.; Iannaccone, S. T.; Stull, J. T.; Thomas, G. D.; Victor, R. G. Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (25), 13818-23.
4. Kobayashi, Y. M.; Rader, E. P.; Crawford, R. W.; Iyengar, N. K.; Thedens, D. R.; Faulkner, J. A.; Parikh, S. V.; Weiss, R. M.; Chamberlain, J. S.; Moore, S. A.; Campbell, K. P. Sarcolemmalocalized nNOS is required to maintain activity after mild exercise. Nature 2008, 456, 511-5.
5. Kasai, T.; Abeyama, K.; Hashiguchi, T.; Fukunaga, H.; Osame, M.; Maruyama, I. Decreased total nitric oxide production in patients with duchenne muscular dystrophy. J. Biomed. Sci. 2004, 11 (4), 534-7.
6. Brenman, J. E.; Chao, D. S.; Xia, H.; Aldape, K.; Bredt, D. S. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 1995, 82 (5), 743-52.
7. 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.; Stull, J. T. Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc. Natl. Acad. Sci. U.S.A. 1996, 93 (17), 9142-7.
8. Crosbie, R. H.; Barresi, R.; Campbell, K. P. Loss of sarcolemma nNOS in sarcoglycan-deficient muscle. FASEB J. 2002, 16 (13), 1786-91.
9. Finanger Hedderick, E. L.; Simmers, J. L.; Soleimani, A.; Andres-Mateos, E.; Marx, R.; Files, D. C.; King, L.; Crawford, T. O.; Corse, A. M.; Cohn, R. D. Loss of sarcolemmal nNOS is common in acquired and inherited neuromuscular disorders. Neurology 2011, 76 (11), 960-7.
10. Wehling, M.; Spencer, M. J.; Tidball, J. G. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J. Cell Biol. 2001, 155 (1), 123-31.
11. Thomas, G. D.; Sander, M.; Lau, K. S.; Huang, P. L.; Stull, J. T.; Victor, R. G. Impaired metabolic modulation of alpha-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 1998, 95 (25), 15090-5.
12. Dudley, R. W.; Danialou, G.; Govindaraju, K.; Lands, L.; Eidelman, D. E.; Petrof, B. J. Sarcolemmal damage in dystrophin deficiency is modulated by synergistic interactions between mechanical and oxidative/nitrosative stresses. Am. J. Pathol. 2006, 168 (4), 1276-87 quiz 1404-5.
13. Anderson, J. E. A role for nitric oxide in muscle repair: nitric oxide-mediated activation of muscle satellite cells. Mol. Biol. Cell 2000, 11 (5), 1859-74.
14. Collins, C. A.; Olsen, I.; Zammit, P. S.; Heslop, L.; Petrie, A.; Partridge, T. A.; Morgan, J. E. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 2005, 122 (2), 289-301.
15. Tidball, J. G.; Wehling-Henricks, M. Evolving therapeutic strategies for Duchenne muscular dystrophy: targeting downstream events. Pediatr. Res. 2004, 56 (6), 831-41.
16. Wehling-Henricks, M.; Jordan, M. C.; Roos, K. P.; Deng, B.; Tidball, J. G. Cardiomyopathy in dystrophin-deficient hearts is prevented by expression of a neuronal nitric oxide synthase transgene in the myocardium. Hum. Mol. Genet. 2005, 14 (14), 1921-33.
17. Wang, G.; Burczynski, F. J.; Hasinoff, B. B.; Zhang, K.; Lu, Q.; Anderson, J. E. Development of a Nitric Oxide-Releasing Analogue of the Muscle Relaxant Guaifenesin for Skeletal Muscle Satellite Cell Myogenesis. Mol. Pharmaceutics 2009, 6 (3), 895-904.
18. Tidball, J. G.; Wehling-Henricks, M. Expression of a NOS transgene in dystrophin-deficient muscle reduces muscle membrane damage without increasing the expression of membrane-associated cytoskeletal proteins. Mol. Genet. Metab. 2004, 82 (4), 312-20.
19. Brunelli, S.; Sciorati, C.; D'Antona, G.; Innocenzi, A.; Covarello, D.; Galvez, B. G.; Perrotta, C.; Monopoli, A.; Sanvito, F.; Bottinelli, R.; Ongini, E.; Cossu, G.; Clementi, E. Nitric oxide release combined with nonsteroidal antiinflammatory activity prevents muscular dystrophy pathology and enhances stem cell therapy. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (1), 264-9.
20. Khairallah, M.; Khairallah, R. J.; Young, M. E.; Allen, B. G.; Gillis, M. A.; Danialou, G.; Deschepper, C. F.; Petrof, B. J.; Des Rosiers, C. Sildenafil and cardiomyocyte-specific cGMP signaling prevent cardiomyopathic changes associated with dystrophin deficiency. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (19), 7028-33.
21. Carre-Pierrat, M.; Mariol, M. C.; Chambonnier, L.; Laugraud, A.; Heskia, F.; Giacomotto, J.; Segalat, L. Blocking of striated muscle degeneration by serotonin in C. elegans. J. Muscle Res. Cell Motil. 2006, 27 (3-4), 253-8.
22. Mariol, M. C.; Martin, E.; Chambonnier, L.; Segalat, L. Dystrophin-dependent muscle degeneration requires a fully functional contractile machinery to occur in C. elegans. Neuromusc. Disorders 2007, 17 (1), 56-60.
23. Ikemoto, T.; Hosoya, T.; Aoyama, H.; Kihara, Y.; Suzuki, M.; Endo, M. Effects of dantrolene and its derivatives on Ca(2+) release from the sarcoplasmic reticulum of mouse skeletal muscle fibres. Br. J. Pharmacol. 2001, 134 (4), 729-36.
24. Bertorini, T. E.; Palmieri, G. M.; Griffin, J.; Igarashi, M.; Hinton, A.; Karas, J. G. Effect of dantrolene in Duchenne muscular dystrophy. Muscle Nerve 1991, 14 (6), 503-7.
25. Quinlan, J. G.; Johnson, S. R.; Samaha, F. J. Dantrolene normalizes serum creatine kinase in MDX mice. Muscle Nerve 1990, 13 (3), 268-9.
26. Amelink, G. J.; Van der Kallen, C. J.; Wokke, J. H.; Bar, P. R. Dantrolene sodium diminishes exercise-induced muscle damage in the rat. Eur. J. Pharmacol. 1990, 179 (1-2), 187-92.
27. Jacobs, G. D. Clinical applications of the relaxation response and mind-body interventions. J. Alt. Complem. Med. 2001, 7 (Suppl 1), S93-101.
28. Jacobs, G. D. The physiology of mind-body interactions: the stress response and the relaxation response. J. Alt. Complem. Med. 2001, 7 (Suppl 1), S83-92.
29. Wink, D. A.; Hines, H. B.; Cheng, R. Y.; Switzer, C. H.; Flores-Santana, W.; Vitek, M. P.; Ridnour, L. A.; Colton, C. A. Nitric oxide and redox mechanisms in the immune response. J. Leukocyte Biol. 2011, 89 (6), 873-91.
30. Murad, F. Discovery of some of the biological effects of nitric oxide and its role in cell signaling. Biosci. Rep. 1999, 19 (3), 133-54.
31. Lee, S. J. Quadrupling muscle mass in mice by targeting TGFbeta signaling pathways. PLoS One 2007, 2 (8), e789.
32. Brazeau, G. A.; Mathew, M.; Entrikin, R. K. Serum and organ indices of the mdx dystrophic mouse. Res. Commun. Chem. Pathol. Pharmacol. 1992, 77 (2), 179-89.
33. Zammit, P. S.; Partridge, T. A.; Yablonka-Reuveni, Z. The skeletal muscle satellite cell: the stem cell that came in from the cold. J. Histochem. Cytochem. 2006, 54 (11), 1177-91.
34. Tinsley, J. M.; Potter, A. C.; Phelps, S. R.; Fisher, R.; Trickett, J. I.; Davies, K. E. Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 1996, 384 (6607), 349-53.
35. Chaubourt, E.; Voisin, V.; Fossier, P.; Baux, G.; Israel, M.; De La Porte, S. Muscular nitric oxide synthase (muNOS) and utrophin. J. Physiol. Paris 2002, 96 (1-2), 43-52.
36. Waheed, I.; Gilbert, R.; Nalbantoglu, J.; Guibinga, G. H.; Petrof, B. J.; Karpati, G. Factors associated with induced chronic inflammation in mdx skeletal muscle cause posttranslational stabilization and augmentation of extrasynaptic sarcolemmal utrophin. Hum. Gene Ther. 2005, 16 (4), 489-501.
37. Mallouk, N.; Jacquemond, V.; Allard, B. Elevated subsarcolemmal Ca2+ in mdx mouse skeletal muscle fibers detected with Ca2+-activated K+ channels. Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (9), 4950-5.
38. Bodensteiner, J. B.; Engel, A. G. Intracellular calcium accumulation in Duchenne dystrophy and other myopathies: a study of 567, 000 muscle fibers in 114 biopsies. Neurology 1978, 28 (5), 439-46.
39. Iwata, Y.; Katanosaka, Y.; Shijun, Z.; Kobayashi, Y.; Hanada, H.; Shigekawa, M.; Wakabayashi, S. Protective effects of Ca2+ handling drugs against abnormal Ca2+ homeostasis and cell damage in myopathic skeletal muscle cells. Biochem. Pharmacol. 2005, 70 (5), 740-51.
40. Loufrani, L.; Levy, B. I.; Henrion, D. Defect in microvascular adaptation to chronic changes in blood flow in mice lacking the gene encoding for dystrophin. Circ. Res. 2002, 91 (12), 1183-9.
41. Tidball, J. G.; Villalta, S. A. NO may prompt calcium leakage in dystrophic muscle. Nat. Med. 2009, 15 (3), 243-4.
42. Millay, D. P.; Goonasekera, S. A.; Sargent, M. A.; Maillet, M.; Aronow, B. J.; Molkentin, J. D. Calcium influx is sufficient to induce muscular dystrophy through a TRPC-dependent mechanism. Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (45), 19023-8.
43. Fraysse, B.; Liantonio, A.; Cetrone, M.; Burdi, R.; Pierno, S.; Frigeri, A.; Pisoni, M.; Camerino, C.; De Luca, A. The alteration of calcium homeostasis in adult dystrophic mdx muscle fibers is worsened by a chronic exercise in vivo. Neurobiol. Dis. 2004, 17 (2), 144-54.
44. Cofan, M.; Nicolas, J. M.; Fernandez-Sola, J.; Robert, J.; Tobias, E.; Sacanella, E.; Estruch, R.; Urbano-Marquez, A. Acute ethanol treatment decreases intracellular calcium-ion transients in mouse single skeletal muscle fibres in vitro. Alcohol Alcoholism 2000, 35 (2), 134-8.
45. Urbano-Marquez, A.; Estruch, R.; Navarro-Lopez, F.; Grau, J. M.; Mont, L.; Rubin, E. The effects of alcoholism on skeletal and cardiac muscle. N. Engl. J. Med. 1989, 320 (7), 409-15.
46. Berger, F. M. Anticonvulsant action of 2-substituted-1, 3-propanediols. Proc. Soc. Exp. Biol. Med. 1949, 71 (2), 270.
47. Harry, L.; Yale, E. J. P.; Braker, W.; Bernstein, J.; Lott, W. A. Muscle-Relaxing Compounds Similar to 3-(o-Toloxy)-1, 2-propanediol. II. Substituted Alkanediols. J. Am. Chem. Soc. 1950, 72 (8), 3.
48. Swash, M. Nitric oxide and muscle weakness. Neurology 2011, 76 (11), 940-1.
49. Kumar, A.; Boriek, A. M. Mechanical stress activates the nuclear factor-kappaB pathway in skeletal muscle fibers: a possible role in Duchenne muscular dystrophy. FASEB J. 2003, 17 (3), 386-96.
50. Marques, M. J.; Luz, M. A.; Minatel, E.; Neto, H. S. Muscle regeneration in dystrophic mdx mice is enhanced by isosorbide dinitrate. Neurosci. Lett. 2005, 382 (3), 342-5.
51. Mizunoya, W.; Upadhaya, R.; Burczynski, F. J.; Wang, G.; Anderson, J. E. Nitric oxide donors improve prednisone effects on muscular dystrophy in the mdx mouse diaphragm. Am. J. Physiol. Cell Physiol. 2011, 300 (5), C1065-77.
52. Adamo, C. M.; Dai, D. F.; Percival, J. M.; Minami, E.; Willis, M. S.; Patrucco, E.; Froehner, S. C.; Beavo, J. A. Sildenafil reverses cardiac dysfunction in the mdx mouse model of Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (44), 19079-83.
53. Wehling-Henricks, M.; Jordan, M. C.; Gotoh, T.; Grody, W. W.; Roos, K. P.; Tidball, J. G. Arginine metabolism by macrophages promotes cardiac and muscle fibrosis in mdx muscular dystrophy. PLoS One 2010, 5 (5), e10763.
54. Li, Z. F.; Shelton, G. D.; Engvall, E. Elimination of myostatin does not combat muscular dystrophy in dy mice but increases postnatal lethality. Am. J. Pathol. 2005, 166 (2), 491-7.
55. Sumner, C. J.; Wee, C. D.; Warsing, L. C.; Choe, D. W.; Ng, A. S.; Lutz, C.; Wagner, K. R. Inhibition of myostatin does not ameliorate disease features of severe spinal muscular atrophy mice. Hum. Mol. Genet. 2009, 18 (17), 3145-52.
56. Loufrani, L.; Dubroca, C.; You, D.; Li, Z.; Levy, B.; Paulin, D.; Henrion, D. Absence of dystrophin in mice reduces NO-dependent vascular function and vascular density: total recovery after a treatment with the aminoglycoside gentamicin. Arterioscler. Thromb. Vasc. Biol. 2004, 24 (4), 671-6.
57. Amsterdam, E. A. Rationale for intermittent nitrate therapy. Am. J. Cardiol. 1992, 70 (17), 55G-59G discussion 59G-60G.