Gentamicin treatment in exercised mdx mice: Identification of dystrophin-sensitive pathways and evaluation of efficacy in work-loaded dystrophic muscle

Neurobiology of Disease

Volumn 32, Issue 2, 2008, Pages 243-253

  De Luca, Annamaria ^a   Nico, Beatrice ^b   Rolland, Jean François ^a   Cozzoli, Anna ^a   Burdi, Rosa ^a   Mangieri, Domenica ^b   Giannuzzi, Viviana ^a   Liantonio, Antonella ^a   Cippone, Valentina ^a   De Bellis, Michela ^a   Nicchia, Grazia Paola ^b   Camerino, Giulia Maria ^b   Frigeri, Antonio ^b   Svelto, Maria ^b   Camerino, Diana Conte ^a  

^a Unit of Pharmacology   (Italy)

^b UNIVERSITY OF BARI   (Italy)

Author keywords

Aquaporin 4; Calcium homeostasis; Creatine kinase; Dystrophin; Electrophysiology; Exercise; Gentamicin treatment; Histology; Muscular dystrophy; Nuclear factor kB

Indexed keywords

AQUAPORIN 4; CREATINE KINASE; DYSTROPHIN; GENTAMICIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; CREATINE KINASE BLOOD LEVEL; DRUG EFFICACY; EXERCISE; FORELIMB; GASTROCNEMIUS MUSCLE; HISTOPATHOLOGY; ION CONDUCTANCE; MALE; MEMBRANE PERMEABILITY; MOUSE; MUSCLE CELL; MUSCLE FIBER MEMBRANE CONDUCTANCE; MUSCLE INJURY; MUSCLE STRENGTH; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOLEMMA; TREATMENT DURATION;

ANIMALS; AQUAPORIN 4; BODY WEIGHT; CALCIUM; DYSTROPHIN; GENTAMICINS; HOMEOSTASIS; MALE; MICE; MICE, INBRED MDX; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; PATCH-CLAMP TECHNIQUES; PHYSICAL CONDITIONING, ANIMAL; PROTEIN SYNTHESIS INHIBITORS; SARCOLEMMA; SIGNAL TRANSDUCTION;

EID: 53749088724     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2008.07.009     Document Type: Article

References (51)

1. Adams M.E., Tesch Y., Percival J.M., Albrecht D.E., Conhaim J.I., Anderson K., and Froehner S.C. Differential targeting of nNOS and AQP4 to dystrophin-deficient sarcolemma by membrane-directed {alpha}-dystrobrevin. J. Cell Sci. 121 (2008) 48-54
2. Acharyya S., Villalta S.A., Bakkar N., Bupha-Intr T., Janssen P.M., Carathers M., Li Z.W., Beg A.A., Ghosh S., Sahenk Z., Weinstein M., Gardner K.L., Rafael-Fortney J.A., Karin M., Tidball J.G., Baldwin A.S., and Guttridge D.C. Interplay of IKK/NF-kappaB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J. Clin. Invest. 117 (2007) 889-901
3. Arakawa M., Shiozuka M., Nakayama Y., Hara T., Hamada M., Kondo S., Ikeda D., Takahashi Y., Sawa R., Nonomura Y., Sheykholeslami K., Kondo K., Kaga K., Kitamura T., Suzuki-Miyagoe Y., Takeda S., and Matsuda R. Negamycin restores dystrophin expression in skeletal and cardiac muscles of mdx mice. J. Biochem. 134 (2003) 751-758
4. Alderton J.M., and Steinhardt R.A. How calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. Trends Cardiovasc. Med. 10 (2000) 268-272
5. Allen D.G., Whitehead N.P., and Yeung E.W. Mechanisms of stretch-induced muscle damage in normal and dystrophic muscle: role of ionic changes. J. Physiol. 567 (2005) 723-735
6. Andreetta F., Bernasconi P., Baggi F., Ferro P., Oliva L., Arnoldi E., Cornelio F., Mantegazza R., and Confalonieri P. Immunomodulation of TGF-beta1 in mdx mouse inhibits connective tissue proliferation in diaphragm but increases inflammatory response: implications for antifibrotic therapy. J. Neuroimmunol. 175 (2006) 77-86
7. Barton-Davis E.R., Cordierm L., Shoturma D.I., Leland S.E., and Sweeney H.L. Aminoglycoside antibiotics restore dystrophin function to skeletal muscles of mdx mice. J. Clin. Invest. 104 (1999) 375-381
8. Bidou L., Hatin I., Perez N., Allamand V., Panthier J.J., and Rousset J.P. Premature stop codons involved in muscular dystrophies show a broad spectrum of readthrough efficiencies in response to gentamicin treatment. Gene Ther. 11 (2004) 619-627
9. Burdi R., Didonna M.P., Pignol B., Nico B., Mangieri D., Rolland J.F., Camerino C., Zallone A., Ferro P., Andreetta F., Confalonieri P., and De Luca A. First evaluation of the potential effectiveness in muscular dystrophy of a novel chimeric compound, BN 82270, acting as calpain-inhibitor and anti-oxidant. Neuromuscul. Disord. 16 (2006) 237-248
10. Bushby K., Griggs R., and MSG/ENMC FOR DMD Trial Study Group. 145th ENMC International Workshop: planning for an International Trial of Steroid Dosage Regimes in DMD (FOR DMD), 22-24th October 2006, Naarden, The Netherlands. Neuromuscul. Disord. 17 (2007) 423-428
11. Chen Y.W., Nagaraju K., Bakay M., McIntyre O., Rawat R., Shi R., and Hoffman E.P. Early onset of inflammation and later involvement of TGFbeta in Duchenne muscular dystrophy. Neurology 65 (2005) 826-834
12. Crosbie R.H., Dovico S.A., Flanagan J.D., Chamberlain J.S., Ownby C.L., and Campbell K.P. Characterization of aquaporin-4 in muscle and muscular dystrophy. FASEB J. 16 (2002) 943-949
13. De Luca A., Pierno S., and Conte Camerino D. Electrical properties of diaphragm and EDL muscles during the life of dystrophic mice. Am. J. Physiol. 272 (1997) C333-C340
14. De Luca A., Pierno S., Liantonio A., Cetrone M., Camerino C., Fraysse B., Mirabella M., Servidei S., Ruegg U.T., and Conte Camerino D. Enhanced dystrophic progression in mdx mice by exercise and beneficial effects of taurine and insulin-like growth factor-1. J. Pharmacol. Exp. Ther. 304 (2003) 453-463
15. De Luca A., Nico B., Liantonio A., Didonna M.P., Fraysse B., Pierno S., Burdi R., Mangieri D., Rolland J.F., Camerino C., Zallone A., Confalonieri P., Andreetta F., Arnoldi E., Courdier-Fruh I., Magyar J.P., Frigeri A., Pisoni M., Svelto M., and Conte Camerino D. A multidisciplinary evaluation of the effectiveness of cyclosporine A in dystrophic mdx mice. Am. J. Pathol. 166 (2005) 477-489
16. Dudley R.W., Danialou G., Govindaraju K., Lands L., Eidelman D.E., and Petrof B.J. Sarcolemmal damage in dystrophin deficiency is modulated by synergistic interactions between mechanical and oxidative/nitrosative stresses. Am. J. Pathol. 168 (2006) 1276-1287
17. Fraysse B., Liantonio A., Cetrone M., Burdi R., Pierno S., Frigeri A., Pisoni M., Camerino C., and De Luca A. The alteration of calcium homeostasis in adult dystrophic mdx muscle fibers is worsened by a chronic exercise in vivo. Neurobiol. Dis. 17 (2004) 144-154
18. Frigeri A., Nicchia G.P., Verbavatz J.M., Valenti G., and Svelto M. Expression of aquaporin-4 in fast-twitch fibers of mammalian skeletal muscle. J. Clin. Invest. 102 (1998) 695-703
19. Frigeri A., Nicchia G.P., Repetto S., Bado M., Minetti C., and Svelto M. Altered aquaporin-4 expression in human muscular dystrophies: a common feature?. FASEB J. 16 (2002) 1120-1122
20. Frigeri A., Nicchia G.P., Balena R., Nico B., and Svelto M. Aquaporins in skeletal muscle: reassessment of the functional role of aquaporin-4. FASEB J. 18 (2004) 905-907
21. Gailly P., De Backer F., Van Schoor M., and Gillis J.M. In situ measurements of calpain activity in isolated muscle fibres from normal and dystrophin-lacking mdx mice. J. Physiol. 582 (2007) 1261-1275
22. Gosselin L.E., Williams J.E., Personius K., and Farkas G.A. A comparison of factors associated with collagen metabolism in different skeletal muscles from dystrophic (mdx) mice: impact of pirfenidone. Muscle Nerve 35 (2007) 208-216
23. Granchelli J.A., Pollina C., and Hudecki M.S. Pre-clinical screening of drugs using the mdx mouse. Neuromuscul. Disord. 10 (2000) 235-239
24. Grounds M.D., Radley H.G., Lynch G.S., Nagaraju K., and De Luca A. Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol. Dis. 31 (2008) 1-19
25. Hirawat S., Welch E.M., Elfring G.L., Northcutt V.J., Paushkin S., Hwang S., Leonard E.M., Almstead N.G., Ju W., Peltz S.W., and Miller L.L. Safety, tolerability, and pharmacokinetics of PTC124, a nonaminoglycoside nonsense mutation suppressor, following single- and multiple-dose administration to healthy male and female adult volunteers. J. Clin. Pharmacol. 47 (2007) 430-444
26. Hoffman E.P., and Dressman D. Molecular pathophysiology and targeted therapeutics for muscular dystrophy. Trends Pharmacol. Sci. 22 (2001) 465-470
27. Kapsa R., Kornberg A.J., and Byrne E. Novel therapies for Duchenne muscular dystrophy. Lancet Neurol. 2 (2003) 299-310
28. Kimura S., Ito K., Miyagi T., Hiranuma T., Yoshioka K., Ozasa S., Matsukura M., Ikezawa M., Matsuo M., Takeshima Y., and Miike T. A novel approach to identify Duchenne muscular dystrophy patients for aminoglycoside antibiotics therapy. Brain Dev. 27 (2005) 400-405
29. 2+-permeable growth factor-regulated channel. J. Cell Biol. 5 (2003) 957-967
30. Loufrani L., Dubroca C., You D., Li Z., Levy B., Paulin D., and 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. 24 (2004) 671-676
31. Menke A., and Jockusch H. Decreased osmotic stability of dystrophin-less muscle cells from the mdx mouse. Nature 349 (1991) 69-71
32. Messina S., Altavilla D., Aguennouz M., Seminara P., Minutoli L., Monici M.C., Bitto A., Mazzeo A., Marini H., Squadrito F., and Vita G. Lipid peroxidation inhibition blunts nuclear factor-kappaB activation, reduces skeletal muscle degeneration, and enhances muscle function in mdx mice. Am. J. Pathol. 168 (2006) 918-926
33. Myrdal S.E., and Steyger P.S. TRPV1 regulators mediate gentamicin penetration of cultured kidney cells. Hear. Res. 204 (2005) 170-182
34. Neri M., Torelli S., Brown S., Ugo I., Sabatelli P., Merlini L., Spitali P., Rimessi P., Gualandi F., Sewry C., Ferlini A., and Muntoni F. Dystrophin levels as low as 30% are sufficient to avoid muscular dystrophy in the human. Neuromuscul. Disord. 17 (2007) 913-918
35. Nicchia G.P., Srinivas M., Li W., Brosnan C.F., Frigeri A., and Spray D.C. New possible roles for aquaporin-4 in astrocytes: cell cytoskeleton and functional relationship with connexin43. FASEB J. 19 (2005) 1674-1676
36. Petrof B.J. Molecular pathophysiology of myofiber injury in deficiencies of the dystrophin-glycoprotein complex. Am. J. Phys. Med. Rehabil. 81 (2002) S162-S174
37. Pierno S., Nico B., Burdi R., Liantonio A., Didonna M.P., Cippone V., Fraysse B., Rolland J.F., Mangieri D., Confalonieri P., Andreetta F., Ferro P., Camerino C., Zallone A., and De Luca A. Role of TNF-a, but not of COX-2 derived eicosanoids, on functional and morphological indices of dystrophic progression in mdx mice: a pharmacological approach. Neuropathol. Appl. Neurobiol. 33 (2007) 344-359
38. Porter J.D., Khanna S., Kaminski H.J., Rao J.S., Merriam A.P., Richmonds C.R., Leahy P., Li J., Guo W., and Andrade F.H. A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum. Mol. Genet. 11 (2002) 263-272
39. Radley H.G., and Grounds M.D. Cromolyn administration (to block mast cell degranulation) reduces necrosis of dystrophic muscle in mdx mice. Neurobiol. Dis. 23 (2006) 387-397
40. Rando T.A. Role of nitric oxide in the pathogenesis of muscular dystrophies: a "two hit" hypothesis of the cause of muscle necrosis. Microsc. Res. Tech. 55 (2001) 223-235
41. Robert V., Massimino M.L., Tosello V., Marsault R., Cantini M., Sorrentino V., and Pozzan T. Alteration in calcium handling at the subcellular level in mdx myotubes. J. Biol. Chem. 276 (2001) 4647-4651
42. Rolland J.F., De Luca A., Burdi R., Andreetta F., Confalonieri P., and Conte Camerino D. Overactivity of exercise-sensitive cation channels and their impaired modulation by IGF-1 in mdx native muscle fibers: beneficial effect of pentoxifylline. Neurobiol. Dis. 24 (2006) 466-474
43. Sicinski P., Geng Y., Ryder-Cook A.S., Barnard E.A., Darlison M.G., and Barnard P.J. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244 (1989) 1578-1580
44. Squire S., Raymackers J.M., Vandebrouck C., Potter A., Tinsley J., Fisher R., Gillis J.M., and Davies K.E. Prevention of pathology in mdx mice by expression of utrophin: analysis using an inducible transgenic expression system. Hum. Mol. Genet. 11 (2002) 3333-3344
45. 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. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352 (1991) 536-539
46. Vandebrouck C., Martin D., Colson-Van Schoor M., Debaix H., and Gailly P. Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J. Cell Biol, 6 (2002) 1089-1096
47. Wagner K.R., Hamed S., Hadley D.W., Gropman A.L., Burstein A.H., Escolar D.M., Hoffman E.P., and Fischbeck K.H. Gentamicin treatment of Duchenne and Becker muscular dystrophy due to nonsense mutations. Ann. Neurol. 49 (2001) 706-711
48. Welch E.M., Barton E.R., Zhuo J., Tomizawa Y., Friesen W.J., Trifillis P., Paushkin S., Patel M., Trotta C.R., Hwang S., Wilde R.G., Karp G., Takasugi J., Chen G., Jones S., Ren H., Moon Y.C., Corson D., Turpoff A.A., Campbell J.A., Conn M.M., Khan A., Almstead N.G., Hedrick J., Mollin A., Risher N., Weetal M., Yeh S., Branstrom A.A., Colacino J.M., Babiak J., Ju W.D., Hirawat S., Northcutt V.J., Miller L.L., Spatrick P., He F., Kawana M., Feng H., Jacobson A., Peltz S.W., and Sweeney H.L. PTC124 targets genetic disorders caused by nonsense mutations. Nature 447 (2007) 87-91
49. Whitehead N.P., Streamer M., Lusambili L.I., Sachs F., and Allen D.G. Streptomycin reduces stretch-induced membrane permeability in muscles from mdx mice. Neuromuscul. Disord. 16 (2006) 845-854
50. Wilton S. PTC124, non sense mutations and Duchenne muscular dystrophy. Neuromuscul. Disord. 17 (2007) 719
51. Yeung E.W., Whitehead N.P., Suchyna T.M., Gottlieb P.A., Sachs F., and Allen D.G. Effects of stretch-activated channel blockers on [Ca2+]i and muscle damage in the mdx mouse. J. Physiol. 562 (2005) 367-380