Evaluation of potential synergistic action of a combined treatment with alpha-methyl-prednisolone and taurine on the mdx mouse model of Duchenne muscular dystrophy

Neuropathology and Applied Neurobiology

Volumn 37, Issue 3, 2011, Pages 243-256

  Cozzoli, A ^a   Rolland, J F ^a   Capogrosso, R F ^a   Sblendorio, V T ^a   Longo, V ^b   Simonetti, S ^c   Nico, B ^b   De Luca, A ^a  

^a Faculty of Pharmacy   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c Paediatric Hospital Giovanni XXIII   (Italy)

Author keywords

Animal model; Duchenne muscular dystrophy; Markers of disease; Preclinical tests; Prednisolone and taurine; Synergistic drugs association

Indexed keywords

ALPHA METHYLPREDNISOLONE; AMINO ACID; CALCIUM; CREATINE KINASE; GLUCOCORTICOID; LACTATE DEHYDROGENASE; TAURINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CALCIUM HOMEOSTASIS; CLINICAL EVALUATION; CONTROLLED STUDY; CREATINE KINASE BLOOD LEVEL; DRUG EFFICACY; DRUG POTENTIATION; DUCHENNE MUSCULAR DYSTROPHY; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; EX VIVO STUDY; EXTENSOR DIGITORUM LONGUS MUSCLE; FAST MUSCLE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTOPATHOLOGY; IN VIVO STUDY; LACTATE DEHYDROGENASE BLOOD LEVEL; LIMB; MALE; MECHANICAL STIMULATION; MONOTHERAPY; MOUSE; MUSCLE; MUSCLE STRENGTH; NONHUMAN; PRIORITY JOURNAL; TREADMILL EXERCISE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CREATINE KINASE; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; GLUCOCORTICOIDS; L-LACTATE DEHYDROGENASE; MALE; METHYLPREDNISOLONE; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; PATCH-CLAMP TECHNIQUES; TAURINE;

EID: 79951793290     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2010.01106.x     Document Type: Article

References (50)

1. Hoffman EP, Dressman D. Molecular pathophysiology and targeted therapeutics for muscular dystrophy. Trends Pharmacol Sci 2001; 22: 465-70
2. Grounds MD, Radley HG, Lynch GS, Nagaraju K, De Luca A. Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol Dis 2008; 31: 1-19
3. Alderton JM, Steinhardt RA. How calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. Trends Cardiovasc Med 2000; 10: 268-72
4. Vandebrouck C, Martin D, Colson-Van Schoor M, Debaix H, Gailly P. Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J Cell Biol 2002; 158: 1089-96
5. 2+-permeable growth factor-regulated channel. J Cell Biol 2003; 161: 957-67
6. 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: 144-54
7. Rolland JF, De Luca A, Burdi R, Andreetta F, Confalonieri P, 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 2006; 24: 466-74
8. De Luca A, Pierno S, Liantonio A, Cetrone M, Camerino C, Fraysse B, Mirabella M, Servidei S, Ruegg UT, 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 2003; 304: 453-63
9. Basset O, Boittin FX, Cognard C, Constantin B, Ruegg UT. BCL-2 overexpression prevents calcium overload and subsequent apoptosis in dystrophic myotubes. Biochem J 2006; 395: 267-76
10. Burdi R, Didonna MP, Pignol B, Nico B, Mangieri D, Rolland JF, Camerino C, Zallone A, Ferro P, Andreetta F, Confalonieri P, 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 2006; 16: 237-48
11. Gailly P, De Backer F, Van Schoor M, Gillis JM. In situ measurements of calpain activity in isolated muscle fibres from normal and dystrophin-lacking mdx mice. J Physiol 2007; 582: 1261-75
12. Chen YW, Nagaraju K, Bakay M, McIntyre O, Rawat R, Shi R, Hoffman EP. Early onset of inflammation and later involvement of TGFbeta in Duchenne muscular dystrophy. Neurology 2005; 65: 826-34
13. Grounds MD, Torrisi J. Anti-TNFalpha (Remicade) therapy protects dystrophic skeletal muscle from necrosis. FASEB J 2004; 18: 676-82
14. Messina S, Altavilla D, Aguennouz M, Seminara P, Minutoli L, Monici MC, Bitto A, Mazzeo A, Marini H, Squadrito F, Vita G. Lipid peroxidation inhibition blunts nuclear factor-kappaB activation, reduces skeletal muscle degeneration, and enhances muscle function in mdx mice. Am J Pathol 2006; 168: 918-26
15. Pierno S, Nico B, Burdi R, Liantonio A, Didonna MP, Cippone V, Fraysse B, Rolland JF, Mangieri D, Andreetta F, Ferro P, Camerino C, Zallone A, Confalonieri P, De Luca A. Role of tumour necrosis factor alpha, but not of cyclo-oxygenase-2-derived eicosanoids, on functional and morphological indices of dystrophic progression in mdx mice: a pharmacological approach. Neuropathol Appl Neurobiol 2007; 33: 344-59
16. Villalta SA, Nguyen HX, Deng B, Gotoh T, Tidball JG. Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum Mol Genet 2009; 18: 482-96
17. Aartsma-Rus A, Fokkema I, Verschuuren J, Ginjaar I, van Deutekom J, van Ommen GJ, den Dunnen JT. Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Hum Mutat 2009; 30: 293-9
18. Cossu G, Sampaolesi M. New therapies for Duchenne muscular dystrophy: challenges, prospects and clinical trials. Trends Mol Med 2007; 13: 520-6
19. Muir LA, Chamberlain JS. Emerging strategies for cell and gene therapy of the muscular dystrophies. Expert Rev Mol Med 2009; 11: e18
20. St-Pierre SJ, Chakkalakal JV, Kolodziejczyk SM, Knudson JC, Jasmin BJ, Megeney LA. Glucocorticoid treatment alleviates dystrophic myofiber pathology by activation of the calcineurin/NF-AT pathway. FASEB J 2004; 18: 1937-9
21. Miura P, Andrews M, Holcik M, Jasmin BJ. IRES-mediated translation of utrophin A is enhanced by glucocorticoid treatment in skeletal muscle cells. PloS ONE 2008; 3: e2309
22. Baban D, Davies KE. Microarray analysis of mdx mice expressing high levels of utrophin: therapeutic implications for dystrophin deficiency. Neuromuscul Disord 2008; 18: 239-47
23. Bauer R, Straub V, Blain A, Bushby K, MacGowan GA. Contrasting effects of steroids and angiotensin-converting-enzyme inhibitors in a mouse model of dystrophin-deficient cardiomyopathy. Eur J Heart Fail 2009; 11: 463-71
24. Vandenburgh H, Shansky J, Benesch-Lee F, Skelly K, Spinazzola JM, Saponjian Y, Tseng BS. Automated drug screening with contractile muscle tissue engineered from dystrophic myoblasts. FASEB J 2009; 23: 3325-34
25. Archer JD, Vargas CC, Anderson JE. Persistent and improved functional gain in mdx dystrophic mice after treatment with L-arginine and deflazacort. FASEB J 2006; 20: 738-40
26. Conte Camerino D, Tricarico D, Pierno S, Desaphy JF, Liantonio A, Pusch M, Burdi R, Camerino C, Fraysse B, De Luca A. Taurine and skeletal muscle disorders. Neurochem Res 2004; 29: 135-42
27. Shao A, Hathcock JN. Risk assessment for the amino acids taurine, L-glutamine and L-arginine. Regul Toxicol Pharmacol 2008; 50: 376-99
28. McIntosh L, Granberg KE, Brière KM, Anderson JE. Nuclear magnetic resonance spectroscopy study of muscle growth, mdx dystrophy and glucocorticoid treatments: correlation with repair. NMR Biomed 1998; 11: 1-10
29. De Luca A, Pierno S, Liantonio A, Cetrone M, Camerino C, Simonetti S, Papadia F, Conte Camerino D. Alteration of excitation-contraction coupling mechanism in extensor digitorum longus muscle fibres of dystrophic mdx mouse and potential efficacy of taurine. Br J Pharmacol 2001; 132: 1047-54
30. Gulston MK, Rubtsov DV, Atherton HJ, Clarke K, Davies KE, Lilley KS, Griffin JL. A combined metabolomic and proteomic investigation of the effects of a failure to express dystrophin in the mouse heart. J Proteome Res 2008; 7: 2069-77
31. Schuller-Levis GB, Park E. Taurine: new implications for an old amino acid. FEMS Microbiol Lett 2003; 226: 195-202
32. Nagaraju K, Willmann R, TREAT-NMD Network and the Wellstone Muscular Dystrophy Cooperative Research Network. Developing standard procedures for murine and canine efficacy studies of DMD therapeutics: report of two expert workshops on 'Pre-clinical testing for Duchenne dystrophy': Washington DC, October 27th-28th 2007 and Zürich, June 30th-July 1st 2008. Neuromuscul Disord 2009; 19: 502-6
33. De Luca A, Nico B, Liantonio A, Didonna MP, Fraysse B, Pierno S, Burdi R, Mangieri D, Rolland JF, Camerino C, Zallone A, Confalonieri P, Andreetta F, Arnoldi E, Courdier-Fruh I, Magyar JP, Frigeri A, Pisoni M, Svelto M, Conte Camerino D. A multidisciplinary evaluation of the effectiveness of cyclosporine a in dystrophic mdx mice. Am J Pathol 2005; 166: 477-89
34. Burdi R, Rolland JF, Fraysse B, Litvinova K, Cozzoli A, Giannuzzi V, Liantonio A, Camerino GM, Sblendorio V, Capogrosso RF, Palmieri B, Andreetta F, Confalonieri P, De Benedictis L, Montagnani M, De Luca A. Multiple pathological events in exercised dystrophic mdx mice are targeted by pentoxifylline: outcome of a large array of in vivo and ex vivo tests. J Appl Physiol 2009; 106: 1311-24
35. De Luca A, Nico B, Rolland JF, Cozzoli A, Burdi R, Mangieri D, Giannuzzi V, Liantonio A, Cippone V, De Bellis M, Nicchia GP, Camerino GM, Frigeri A, Svelto M, Conte Camerino D. Gentamicin treatment in exercised mdx mice: identification of dystrophin-sensitive pathways and evaluation of efficacy in work-loaded dystrophic muscle. Neurobiol Dis 2008; 32: 243-53
36. Whitehead NP, Streamer M, Lusambili LI, Sachs F, Allen DG. Streptomycin reduces stretch-induced membrane permeability in muscles from mdx mice. Neuromuscul Disord 2006; 16: 845-54
37. Zanou N, Iwata Y, Schakman O, Lebacq J, Wakabayashi S, Gailly P. Essential role of TRPV2 ion channel in the sensitivity of dystrophic muscle to eccentric contractions. FEBS Lett 2009; 583: 3600-4
38. Iwata H, Obara T, Kim BK, Baba A. Regulation of taurine transport in rat skeletal muscle. J Neurochem 1986; 47: 158-63
39. Ito T, Kimura Y, Uozumi Y, Takai M, Muraoka S, Matsuda T, Ueki K, Yoshiyama M, Ikawa M, Okabe M, Schaffer SW, Fujio Y, Azuma J. Taurine depletion caused by knocking out the taurine transporter gene leads to cardiomyopathy with cardiac atrophy. J Mol Cell Cardiol 2008; 44: 927-37
40. Huxtable RJ. Physiological actions of taurine. Physiol Rev 1992; 72: 101-63
41. Dirksen RT. Checking your SOCCs and feet: the molecular mechanisms of Ca2+ entry in skeletal muscle. J Physiol 2009; 587: 3139-47
42. Bakker AJ, Berg HM. Effect of taurine on sarcoplasmic reticulum function and force in skinned fast-twitch skeletal muscle fibres of the rat. J Physiol 2002; 538: 185-94
43. De Luca A, Pierno S, Camerino DC. Effect of taurine depletion on excitation-contraction coupling and Cl- conductance of rat skeletal muscle. Eur J Pharmacol 1996; 296: 215-22
44. Pierno S, De Luca A, Camerino C, Huxtable RJ, Camerino DC. Chronic administration of taurine to aged rats improves the electrical and contractile properties of skeletal muscle fibers. J Pharmacol Exp Ther 1998; 286: 1183-90
45. Dawson R Jr, Biasetti M, Messina S, Dominy J. The cytoprotective role of taurine in exercise-induced muscle injury. Amino Acids 2002; 22: 309-24
46. Hamilton EJ, Berg HM, Easton CJ, Bakker AJ. The effect of taurine depletion on the contractile properties and fatigue in fast-twitch skeletal muscle of the mouse. Amino Acids 2006; 31: 273-8
47. Shiny KS, Kumar SH, Farvin KH, Anandan R, Devadasan K. Protective effect of taurine on myocardial antioxidant status in isoprenaline-induced myocardial infarction in rats. J Pharm Pharmacol 2005; 57: 1313-17
48. Varis T, Kaukonen KM, Kivistö KT, Neuvonen PJ. Plasma concentrations and effects of oral methylprednisolone are considerably increased by itraconazole. Clin Pharmacol Ther 1998; 64: 363-8
49. Usui T, Saitoh Y, Komada F. Induction of CYP3As in HepG2 cells by several drugs. Association between induction of CYP3A4 and expression of glucocorticoid receptor. Biol Pharm Bull 2003; 26: 510-17
50. Matsuda H, Kinoshita K, Sumida A, Takahashi K, Fukuen S, Fukuda T, Takahashi K, Yamamoto I, Azuma J. Taurine modulates induction of cytochrome P450 3A4 mRNA by rifampicin in the HepG2 cell line. Biochim Biophys Acta 2002; 1593: 93-8