Revisiting the dystrophin-ATP connection: How half a century of research still implicates mitochondrial dysfunction in Duchenne Muscular Dystrophy aetiology

Medical Hypotheses

Volumn 85, Issue 6, 2015, Pages 1021-1033

  Timpani, Cara A ^a   Hayes, Alan ^a,b   Rybalka, Emma ^a,b  

^a VICTORIA UNIVERSITY   (Australia)

^b WESTERN HEALTH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; DYSTROPHIN; GLUCOSE TRANSPORTER 4; NEURONAL NITRIC OXIDE SYNTHASE; OXOGLUTARATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE; CALCIUM; LIPID; OXYGEN;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CELL STRESS; CITRIC ACID CYCLE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DUCHENNE MUSCULAR DYSTROPHY; DYSTROPHIN GENE; ENZYME ACTIVATION; ENZYME LOCALIZATION; GLYCOLYSIS; HUMAN; INTRACELLULAR SIGNALING; LIPID STORAGE; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; MOLECULAR PATHOLOGY; MUSCLE ATROPHY; NEUROPATHOLOGY; NONHUMAN; OXYGEN CONSUMPTION; POINT MUTATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; CHEMISTRY; DISEASE MODEL; HISTORY; HOMEOSTASIS; MEDICAL RESEARCH; METABOLISM; MITOCHONDRION; MOUSE; MUSCULAR DYSTROPHY, DUCHENNE; PATHOPHYSIOLOGY; PHENOTYPE; SKELETAL MUSCLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; BIOMEDICAL RESEARCH; CALCIUM; DISEASE MODELS, ANIMAL; DYSTROPHIN; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HOMEOSTASIS; HUMANS; LIPIDS; MICE; MITOCHONDRIA; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MUSCULAR DYSTROPHY, DUCHENNE; OXYGEN; PHENOTYPE;

EID: 84947486243     PISSN: 03069877     EISSN: 15322777     Source Type: Journal    
DOI: 10.1016/j.mehy.2015.08.015     Document Type: Article

References (212)

1. Emery A. Population frequencies of inherited neuromuscular diseases - a world survey. Neuromuscul Disord 1991, 1:19.
2. P.A. Romitti, Y. Zhu, S. Puzhankara, et al., Prevalence of Duchenne and Becker muscular dystrophies in the United States, pediatrics, 2015.
3. Brooke M., Griggs R., Mendell J., Fenichel G., Shumate J. The natural history of Duchenne muscular dystrophy: a caveat for therapeutic trials. Trans Am Neurol Assoc 1981, 106:195.
4. Brooke M., Fenichel G., Griggs R., et al. Duchenne muscular dystrophy patterns of clinical progression and effects of supportive therapy. Neurology 1989, 39. 475-475.
5. Duchenne G.B. De la paralysie musculaire pseudo-hypertrophique ou paralysie myo-sclérosique 1868, P. Asselin.
6. Hoffman E.P., Brown R.H., Kunkel L.M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987, 51:919-928.
7. Koenig M., Monaco A.P., Kunkel L.M. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 1988, 53:219-228.
8. Ohlendieck K., Campbell K.P. Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J Cell Biol 1991, 115:1685-1694.
9. Wells D.J., Wells K.E., Asante E.A., et al. Expression of human full-length and minidystrophin in transgenic mdx mice: implications for gene therapy of Duchenne muscular dystrophy. Hum Mol Genet 1995, 4:1245-1250.
10. Clemens P., Kochanek S., Sunada Y., et al. In vivo muscle gene transfer of full-length dystrophin with an adenoviral vector that lacks all viral genes. Gene Ther 1996, 3:965-972.
11. Sakamoto M., Yuasa K., Yoshimura M., et al. Micro-dystrophin cDNA ameliorates dystrophic phenotypes when introduced into mdx mice as a transgene. Biochem Biophys Res Commun 2002, 293:1265-1272.
12. Willmann R., Possekel S., Dubach-Powell J., Meier T., Ruegg M.A. Mammalian animal models for Duchenne muscular dystrophy. Neuromuscul Disord 2009, 19:241-249.
13. Matsumura C.Y., Pertille A., Albuquerque T.C., Santo Neto H., Marques M.J. Diltiazem and verapamil protect dystrophin-deficient muscle fibers of MDX mice from degeneration: a potential role in calcium buffering and sarcolemmal stability. Muscle Nerve 2009, 39:167-176.
14. Fairclough R.J., Wood M.J., Davies K.E. Therapy for Duchenne muscular dystrophy: renewed optimism from genetic approaches. Nat Rev Genet 2013, 14:373-378.
15. Cossu G., Sampaolesi M. New therapies for Duchenne muscular dystrophy: challenges, prospects and clinical trials. Trends Mol Med 2007, 13:520-526.
16. Moxley R., Ashwal S., Pandya S., et al. 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 2005, 64:13-20.
17. Dreyfus J.-C., Schapira Georges, Schapira Fanny Biochemical study of muscle in progressive muscular dystrophy. J Clin Invest 1954, 33:794-797.
18. Di Mauro S., Angelini Corrado, Catani Claudia Enzymes of the glycogen cycle and glycolysis in various human neuromuscular disorders. J Neurol Neurosurg Psychiatry 1967, 30:411-415.
19. Hess J. Phosphorylase activity and glycogen, glucose-6-phosphate, and lactic acid content of human skeletal muscle in various myopathies. J Lab Clin Med 1965, 66:452-463.
20. Chi M.M.Y., Hintz C.S., McKee D., et al. Effect of Duchenne muscular dystrophy on enzymes of energy metabolism in individual muscle fibers. Metabolism 1987, 36:761-767.
21. Chinet A., Even P., Decrouy A. Dystrophin-dependent efficiency of metabolic pathways in mouse skeletal muscles. Cell Mol Life Sci 1994, 50:602-605.
22. van Bennekom C., Oerlemans F.T., Kulakowski S., De Bruyn C.H. Enzymes of purine metabolism in muscle specimens from patients with Duchenne-type muscular dystrophy. Adv Exp Med Biol 1984, 165:447-450.
23. Ge Y., Molloy M.P., Chamberlain J.S., Andrews P.C. Proteomic analysis of mdx skeletal muscle: great reduction of adenylate kinase 1 expression and enzymatic activity. Proteomics 2003, 3:1895-1903.
24. Bonsett C., Rudman A. Duchenne's muscular dystrophy: a tissue culture perspective. Indiana Med J Indiana State Med Assoc 1984, 77:446.
25. Glesby M.J., Rosenmann E., Nylen E.G., Wrogemann K., Serum C.K. Calcium, magnesium, and oxidative phosphorylation in mdx mouse muscular dystrophy. Muscle Nerve 1988, 11:852-856.
26. Kuznetsov A.V., Winkler K., Wiedemann F., von Bossanyi P., Dietzmann K., Kunz W.S. Impaired mitochondrial oxidative phosphorylation in skeletal muscle of the dystrophin-deficient mdx mouse. Mol Cell Biochem 1998, 183:87-96.
27. Rybalka E., Timpani C.A., Cooke M.B., Williams A.D., Hayes A. Defects in mitochondrial ATP synthesis in dystrophin-deficient Mdx skeletal muscles may be caused by complex I insufficiency. PLoS ONE 2014, 9:e115763.
28. Ronzoni E., Wald S., Berg L., Ramsey R. Distribution of high energy phosphate in normal and dystrophic muscle. Neurology 1958, 8:359-368.
29. Vignos P., Warner J. Glycogen, creatine and high energy phosphate in human muscle disease. J Lab Clin Med 1963, 62:579.
30. Tamari H., Ohtani Y., Higashi A., Miyoshino S., Matsuda I. Xanthine oxidase inhibitor in Duchenne muscular dystrophy. Brain Dev 1982, 4:137-143.
31. Cole M., Rafael J., Taylor D., Lodi R., Davies K., Styles P. A quantitative study of bioenergetics in skeletal muscle lacking utrophin and dystrophin. Neuromuscul Disord 2002, 12:247-257.
32. Shuttlewood R., Griffiths J. The purine nucleotide profile in mouse, chicken and human dystrophic muscle: an abnormal ratio of inosine plus adenine nucleotides to guanine nucleotides. Clin Sci 1982, 62:113-115.
33. Onopiuk M., Brutkowski W., Wierzbicka K., et al. Mutation in dystrophin-encoding gene affects energy metabolism in mouse myoblasts. Biochem Biophys Res Commun 2009, 386:463-466.
34. Howland J.L., Challberg M.D. Altered respiration and proton permeability in liver mitochondria from genetically dystrophic mice. Biochem Biophys Res Commun 1973, 50:574-580.
35. +. Metabolism 1978, 27:761-769.
36. Zhang W., Ten Hove M., Schneider J.E., et al. Abnormal cardiac morphology, function and energy metabolism in the dystrophic mdx mouse: an MRI and MRS study. J Mol Cell Cardiol 2008, 45:754-760.
37. Lewis C., Jockusch H., Ohlendieck K. Proteomic profiling of the dystrophin-deficient MDX heart reveals drastically altered levels of key metabolic and contractile proteins. J Biomed Biotechnol 2010, 2010.
38. Bresolin N., Castelli E., Comi G., et al. Cognitive impairment in Duchenne muscular dystrophy. Neuromuscul Disord 1994, 4:359-369.
39. Tracey I., Scott R.B., Thompson C.H., et al. Brain abnormalities in Duchenne muscular dystrophy: phosphorus-31 magnetic resonance spectroscopy and neuropsychological study. Lancet 1995, 345:1260-1264.
40. Tracey I., Dunn J., Parkes H., Radda G. An in vivo and in vitro 1 H-magnetic resonance spectroscopy study of mdx mouse brain: abnormal development or neural necrosis?. J Neurol Sci 1996, 141:13-18.
41. Tracey I., Dunn J.F., Radda G.K. Brain metabolism is abnormal in the mdx model of Duchenne muscular dystrophy. Brain 1996, 119:1039-1044.
42. Tuon L., Comim C.M., Fraga D.B., et al. Mitochondrial respiratory chain and creatine kinase activities in mdx mouse brain. Muscle Nerve 2010, 41:257-260.
43. Bonsett C., Rudman A. The dystrophin connection-ATP?. Med Hypotheses 1992, 38:139-154.
44. Meryon E. On granular and fatty degeneration of the voluntary muscles. Med Chir Trans 1852, 35:73.
45. Duchenne G.-B. De l'électrisation localisée et de son application à la pathologie 1861, Baillière.
46. Bonsett C., Rudman A., Elliott A.Y. Intracellular lipid in pseudohypertrophic muscular dystrophy tissue culture. J. Indiana State Med Assoc 1979, 72:184-187.
47. Bonsett C., Rudman A. 'Oil globules' in Duchenne muscular dystrophy-History, demonstration, and metabolic significance. Med Hypotheses 1994, 43:327-338.
48. Harriman D., Reed R. The incidence of lipid droplets in human skeletal muscle in neuromuscular disorders: a histochemical, electron-microscopic and freeze-etch study. J Pathol 1972, 106:1-24.
49. Pearce G. Electron microscopy in the study of muscular dystrophy. Ann N Y Acad Sci 1966, 138:138-150.
50. Watt M.J., Hoy A.J. Lipid metabolism in skeletal muscle: generation of adaptive and maladaptive intracellular signals for cellular function. Am J Physiol Endocrinol Metab 2012, 302:E1315-E1328.
51. He J., Watkins S., Kelley D.E. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 2001, 50:817-823.
52. Goodpaster B.H., Theriault R., Watkins S.C., Kelley D.E. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 2000, 49:467-472.
53. Sinha R., Dufour S., Petersen K.F., et al. Assessment of skeletal muscle triglyceride content by 1H nuclear magnetic resonance spectroscopy in lean and obese adolescents relationships to insulin sensitivity, total body fat, and central adiposity. Diabetes 2002, 51:1022-1027.
54. Hilton T.N., Tuttle L.J., Bohnert K.L., Mueller M.J., Sinacore D.R. Excessive adipose tissue infiltration in skeletal muscle in individuals with obesity, diabetes mellitus, and peripheral neuropathy: association with performance and function. Phys Ther 2008, 88:1336-1344.
55. Delmonico M.J., Harris T.B., Visser M., et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 2009, 90:1579-1585.
56. Timmons J.A., Larsson O., Jansson E., et al. Human muscle gene expression responses to endurance training provide a novel perspective on Duchenne muscular dystrophy. FASEB J. 2005, 19:750-760.
57. Allen D.G., Lamb G., Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 2008, 88:287-332.
58. 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, 82:743-752.
59. Chang W.-J., Iannaccone S.T., Lau K.S., et al. Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci 1996, 93:9142-9147.
60. Kameya S., Miyagoe Y., Nonaka I., et al. Α1-syntrophin gene disruption results in the absence of neuronal-type nitric-oxide synthase at the sarcolemma but does not induce muscle degeneration. J Biol Chem 1999, 274:2193-2200.
61. Li D., Yue Y., Lai Y., Hakim C.H., Duan D. Nitrosative stress elicited by nNOSμ delocalization inhibits muscle force in dystrophin-null mice. J Pathol 2011, 223:88-98.
62. Leary S.C., Battersby B.J., Hansford R.G., Moyes C.D. Interactions between bioenergetics and mitochondrial biogenesis. Biochim Biophys Acta (BBA) Bioenerg 1998, 1365:522-530.
63. Thomas G.D., Sander M., Lau K.S., Huang P.L., Stull J.T., Victor R.G. Impaired metabolic modulation of α-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc Natl Acad Sci 1998, 95:15090-15095.
64. Vaghy P.L., Fang J., Wu W., Vaghy L.P. Increased caveolin-3 levels in mdx mouse muscles. FEBS Lett 1998, 431:125-127.
65. Judge L.M., Haraguchiln M., Chamberlain J.S. Dissecting the signaling and mechanical functions of the dystrophin-glycoprotein complex. J Cell Sci 2006, 119:1537-1546.
66. Arning L., Jagiello P., Schara U., et al. Transcriptional profiles from patients with dystrophinopathies and limb girdle muscular dystrophies as determined by qRT-PCR. J Neurol 2004, 251:72-78.
67. Crosbie R.H., Straub V., Yun H.-Y., et al. Mdx muscle pathology is independent of nNOS perturbation. Hum Mol Genet 1998, 7:823-829.
68. Gücüyener K., Ergenekon E., Erbas D., Pinarli G., Serdaroğlu A. The serum nitric oxide levels in patients with Duchenne muscular dystrophy. Brain Dev 2000, 22:181-183.
69. Kasai T., Abeyama K., Hashiguchi T., Fukunaga H., Osame M., Maruyama K. Decreased total nitric oxide production in patients with Duchenne muscular dystrophy. J Biomed Sci 2004, 11:534-537.
70. Barton E.R., Morris L., Kawana M., Bish L.T., Toursel T. Systemic administration of L-arginine benefits mdx skeletal muscle function. Muscle Nerve 2005, 32:751-760.
71. Balon T.W., Nadler J.L. Evidence that nitric oxide increases glucose transport in skeletal muscle. J Appl Physiol 1997, 82:359-363.
72. Bradley S.J., Kingwell B.A., McConell G.K. Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans. Diabetes 1999, 48:1815-1821.
73. Maclennan P.A., McArdle A., Edwards R. Acute effects of phorbol esters on the protein-synthetic rate and carbohydrate metabolism of normal and mdx mouse muscles. Biochem J 1991, 275:477.
74. Even P., Decrouy A., Chinet A. Defective regulation of energy metabolism in mdx-mouse skeletal muscles. Biochem J 1994, 304:649.
75. Olichon-Berthe C., Gautier N., Van Obberghen E., Le Marchand-Brustel Y. Expression of the glucose transporter GLUT4 in the muscular dystrophic mdx mouse. Biochem J 1993, 291:257.
76. Raith M., Valencia R.G., Fischer I., et al. Linking cytoarchitecture to metabolism: sarcolemma-associated plectin affects glucose uptake by destabilizing microtubule networks in mdx myofibers. Skeletal Muscle 2013, 3:14.
77. Stedman H.H., Sweeney H.L., Shrager J.B., et al. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 1991, 352:536-539.
78. Wehling-Henricks M., Oltmann M., Rinaldi C., Myung K.H., Tidball J.G. Loss of positive allosteric interactions between neuronal nitric oxide synthase and phosphofructokinase contributes to defects in glycolysis and increased fatigability in muscular dystrophy. Hum Mol Genet 2009, 18:3439-3451.
79. Lilling G., Beitner R. Altered allosteric properties of cytoskeleton-bound phosphofructokinase in muscle from mice with X chromosome-linked muscular dystrophy (mdx). Biochem Med Metab Biol 1991, 45:319-325.
80. Kotelnikova E., Shkrob M.A., Pyatnitskiy M.A., Ferlini A., Daraselia N. Novel approach to meta-analysis of microarray datasets reveals muscle remodeling-related drug targets and biomarkers in Duchenne muscular dystrophy. PLoS Comput Biol 2012, 8:e1002365.
81. Wegener G., Krause U. Different modes of activating phosphofructokinase, a key regulatory enzyme of glycolysis, in working vertebrate muscle. Biochem Soc Trans 2002, 30:264-269.
82. Wehling M., Spencer M.J., Tidball J.G. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 2001, 155:123-132.
83. Galluzzi L., Kepp O., Kroemer G. Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol 2012, 13:780-788.
84. Davis B., Nagy B., Samaha F.J. Duchenne muscular dystrophy: adenosine triphosphate and creatine phosphate content in muscle. Neurology 1981, 31:916-919.
85. Newman R.J., Bore P.J., Chan L., et al. Nuclear magnetic resonance studies of forearm muscle in duchenne dystrophy. Br Med J (Clin Res Ed) 1982, 284:1072-1074.
86. Camiña F., Novo-Rodriguez M.I., Rodriguez-Segade S., Castro-Gago M. Purine and carnitine metabolism in muscle of patients with Duchenne muscular dystrophy. Clin Chim Acta 1995, 243:151-164.
87. Dunn J., Frostick S., Brown G., Radda G. Energy status of cells lacking dystrophin: an in vivo/in vitro study of mdx mouse skeletal muscle. Biochim Biophys Acta (BBA) Mol Basis Dis 1991, 1096:115-120.
88. Percival J.M., Siegel M.P., Knowels G., Marcinek D.J. Defects in mitochondrial localization and ATP synthesis in the mdx mouse model of Duchenne muscular dystrophy are not alleviated by PDE5 inhibition. Hum Mol Genet 2013, 22:153-167.
89. Bertorini T.E., Palmieri G.M.A., Griffin J., et al. Chronic allopurinol and adenine therapy in Duchenne muscular dystrophy: effects on muscle function, nucleotide degradation, and muscle ATP and ADP content. Neurology 1985, 35:61.
90. Liang R.C.R. Studies on mitochondria from dystrophic skeletal muscle of mice. Biochem Med Metab Biol 1986, 36:172-178.
91. Martens M., Jankulovska L., Neymark M., Lee C. Impaired substrate utilization in mitochondria from strain 129 dystrophic mice. Biochim Biophys Acta (BBA) Bioenerg 1980, 589:190-200.
92. Bhattacharya S.K., Johnson P.L., Thakar J.H. Reversal of impaired oxidative phosphorylation and calcium overloading in the in vitro cardiac mitochondria of CHF-146 dystrophic hamsters with hereditary muscular dystrophy. J Neurol Sci 1993, 120:180-186.
93. Faist V., König J., Höger H., Elmadfa I. Decreased mitochondrial oxygen consumption and antioxidant enzyme activities in skeletal muscle of dystrophic mice after low-intensity exercise. Ann Nutr Metab 2001, 45:58-66.
94. Olson E., Vignos P., Woodlock J., Perry T. Oxidative phosphorylation of skeletal muscle in human muscular dystrophy. J Lab Clin Med 1968, 71:23l.
95. Shumate J.B., Carroll J.E., Brooke M.H., Choksi R.M. Palmitate oxidation in human muscle: comparison to CPT and carnitine. Muscle Nerve 1982, 5:226-231.
96. Griffin J., Williams H., Sang E., Clarke K., Rae C., Nicholson J. Metabolic profiling of genetic disorders: a multitissue 1 H nuclear magnetic resonance spectroscopic and pattern recognition study into dystrophic tissue. Anal Biochem 2001, 293:16-21.
97. Nylen E.G., Wrogemann K. Mitochondrial calcium content and oxidative phosphorylation in heart and skeletal muscle of dystrophic mice. Exp Neurol 1983, 80:69-80.
98. Ionăşescu V., Luca N., Vuia O. Respiratory control and oxidative phosphorylation in the dystrophic muscle. Acta Neurol Scand 1967, 43:564-572.
99. Chen Y.W., Zhao P., Borup R., Hoffman E.P. Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology. J Cell Biol 2000, 151:1321-1336.
100. Dudley R.W., Khairallah M., Mohammed S., Lands L., Des Rosiers C., Petrof B.J. Dynamic responses of the glutathione system to acute oxidative stress in dystrophic mouse (mdx) muscles. Am J Physiol-Regul Integr Comp Physiol 2006, 291:R704-R710.
101. Carberry S., Brinkmeier H., Zhang Y., Winkler C.K., Ohlendieck K. Comparative proteomic profiling of soleus, extensor digitorum longus, flexor digitorum brevis and interosseus muscles from the mdx mouse model of Duchenne muscular dystrophy. Int J Mol Med 2013, 32(3):544-556.
102. Matsumura C.Y., de Oliveira B.M., Durbeej M., Marques M.J. Isobaric tagging-based quantification for proteomic analysis: a comparative study of spared and affected muscles from mdx mice at the early phase of dystrophy. PLoS ONE 2013, 8:e65831.
103. Cao A., Macciotta A., Fiorelli G., Mannucci P., Idéo G. Chromatographic and electrophoretic pattern of lactate and malate dehydrogenase in normal human adult and foetal muscle and in muscle of patients affected by Duchenne muscular dystrophy. Enzymol Biol Clin 1965, 7:156-166.
104. Gellerich F.N., Gizatullina Z., Trumbeckaite S., et al. The regulation of OXPHOS by extra mitochondrial calcium. Biochim Biophys Acta (BBA) Bioenerg 2010, 1797:1018-1027.
105. P.R. Turner, T. Westwood, C.M. Regen, R.A. Steinhardt, Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice, 1988.
106. MAcLennan P.A., McArdle A., Edwards R. Effects of calcium on protein turnover of incubated muscles from mdx mice. Am J Physiol Endocrinol Metab 1991, 260:594-598.
107. Kämper A., Rodemann H. Alterations of protein degradation and 2-D protein pattern in muscle cells of MDX and DMD origin. Biochem Biophys Res Commun 1992, 189:1484-1490.
108. Hopf F., Turner P., Denetclaw W., Reddy P., Steinhardt R. A critical evaluation of resting intracellular free calcium regulation in dystrophic mdx muscle. Am J Physiol Cell Physiol 1996, 271:C1325-C1339.
109. Bakker A., Head S., Williams D., Stephenson D. Ca2+ levels in myotubes grown from the skeletal muscle of dystrophic (mdx) and normal mice. J Physiol 1993, 460:1-13.
110. Pauly M., Daussin F., Burelle Y., et al. AMPK activation stimulates autophagy and ameliorates muscular dystrophy in the mdx mouse diaphragm. Am J Pathol 2012, 181:583-592.
111. Schuh R.A., Jackson K.C., Khairallah R.J., Ward C.W., Spangenburg E.E. Measuring mitochondrial respiration in intact single muscle fibers. Am J Physiol Regul Integr Comp Physiol 2012, 302:R712-R719.
112. Passaquin A.C., Renard M., Kay L., et al. Creatine supplementation reduces skeletal muscle degeneration and enhances mitochondrial function in mdx mice. Neuromuscul Disord 2002, 12:174-182.
113. Wrogemann K., Jacobson B., Blanchaer M. On the mechanism of a calcium-associated defect of oxidative phosphorylation in progressive muscular dystrophy. Arch Biochem Biophys 1973, 159:267.
114. Godin R., Daussin F., Matecki S., Li T., Petrof B.J., Burelle Y. PGC1α gene transfer restores mitochondrial biomass and improves mitochondrial calcium handling in post-necrotic mdx MOUSE skeletal muscle. J Physiol 2012, 590(21):5487-5502.
115. Jahnke V.E., Van Der Meulen J.H., Johnston H.K., et al. Metabolic remodeling agents show beneficial effects in the dystrophin-deficient mdx mouse model. Skeletal Muscle 2012, 2:16.
116. Jato-Rodriguez J., Hudson A., Strickland K. Activities of enzymes of the citric acid cycle and electron transport chain in the skeletal muscle of normal and dystrophic mice (strain 129). Enzyme 1972, 13:286.
117. Kemp G., Taylor D., Dunn J., Frostick S., Radda G. Cellular energetics of dystrophic muscle. J Neurol Sci 1993, 116:201-206.
118. Kadenbach B. Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim Biophys Acta (BBA) Bioenerg 2003, 1604:77-94.
119. Stein L.R., Imai S.-I. The dynamic regulation of NAD metabolism in mitochondria. Trends Endocrinol Metab 2012, 23:420-428.
120. Hood D.A. Invited review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 2001, 90:1137-1157.
121. Watkins S.C., Cullen M.J. A qualitative and quantitative study of the ultrastructure of regenerating muscle fibres in Duchenne muscular dystrophy and polymyositis. J Neurol Sci 1987, 82:181-192.
122. Mastaglia F., Papadimitriou J., Kakulas B. Regeneration of muscle in Duchenne muscular dystrophy: an electron microscope study. J Neurol Sci 1970, 11:425-444.
123. Cullen M., Fulthorpe J. Stages in fibre breakdown in Duchenne muscular dystrophy: an electron-microscopic study. J Neurol Sci 1975, 24:179-200.
124. Cullen M., Jaros E. Ultrastructure of the skeletal muscle in the X chromosome-linked dystrophic (mdx) mouse. Acta Neuropathol 1988, 77:69-81.
125. Tidball J.G., Albrecht D.E., Lokensgard B.E., Spencer M.J. Apoptosis precedes necrosis of dystrophin-deficient muscle. J Cell Sci 1995, 108:2197-2204.
126. Afifi A.K., Bergman R.A., Zellweger H. A possible role for electron microscopy in detection of carriers of Duchenne type muscular dystrophy. J Neurol Neurosurg Psychiatry 1973, 36:643-650.
127. Cogliati S., Frezza C., Soriano Maria E., et al. Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell 2013, 155:160-171.
128. Viollet B., Andreelli F., Jorgensen S.B., et al. Physiological role of AMP-activated protein kinase (AMPK): insights from knockout mouse models. Biochem Soc Trans 2003, 31:216-219.
129. Wang Y., Liang Y., Vanhoutte P.M. SIRT1 and AMPK in regulating mammalian senescence: a critical review and a working model. FEBS Lett 2011, 585:986-994.
130. Winder W., Holmes B., Rubink D., Jensen E., Chen M., Holloszy J. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J Appl Physiol 2000, 88:2219-2226.
131. Webster C., Silberstein L., Hays A.P., Blau H.M. Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 1988, 52:503-513.
132. Ljubicic V., Jasmin B.J. AMP-activated protein kinase at the nexus of therapeutic skeletal muscle plasticity in Duchenne muscular dystrophy. Trends Mol Med 2013, 19(10):614-662.
133. Chakkalakal J.V., Stocksley M.A., Harrison M.-A., et al. Expression of utrophin A mRNA correlates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signaling. Proc Natl Acad Sci 2003, 100:7791-7796.
134. Chakkalakal J.V., Harrison M.-A., Carbonetto S., Chin E., Michel R.N., Jasmin B.J. Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice. Hum Mol Genet 2004, 13:379-388.
135. Angus L.M., Chakkalakal J.V., Méjat A., et al. Calcineurin-NFAT signaling, together with GABP and peroxisome PGC-1α, drives utrophin gene expression at the neuromuscular junction. Am J Physiol Cell Physiol 2005, 289:C908-C917.
136. Chakkalakal J.V., Michel S.A., Chin E.R., Michel R.N., Jasmin B.J. Targeted inhibition of Ca2+/calmodulin signaling exacerbates the dystrophic phenotype in mdx mouse muscle. Hum Mol Genet 2006, 15:1423-1435.
137. Karpati G., Carpenter S., Prescott S. Small-caliber skeletal muscle fibers do not suffer necrosis in mdx mouse dystrophy. Muscle Nerve 1988, 11:795-803.
138. Ljubicic V., Miura P., Burt M., et al. Chronic AMPK activation evokes the slow, oxidative myogenic program and triggers beneficial adaptations in mdx mouse skeletal muscle. Hum Mol Genet 2011, 20(17):ddr265.
139. Ljubicic V., Khogali S., Renaud J.-M., Jasmin B.J. Chronic AMPK stimulation attenuates adaptive signaling in dystrophic skeletal muscle. Am J Physiol Cell Physiol 2012, 302:C110-C121.
140. Al-Rewashdy H., Ljubicic V., Lin W., Renaud J.-M., Jasmin B.J. Utrophin A is essential in mediating the functional adaptations of mdx mouse muscle following chronic AMPK activation. Hum Mol Genet 2014, 24(5):1243-1255.
141. Bueno Júnior C.R., Pantaleão L.C., Voltarelli V.A., Bozi L.H.M., Brum P.C., Zatz M. Combined effect of AMPK/PPAR agonists and exercise training in mdx mice functional performance. PLoS ONE 2012, 7:45699.
142. Handschin C., Kobayashi Y.M., Chin S., Seale P., Campbell K.P., Spiegelman B.M. PGC-1α regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev 2007, 21:770-783.
143. Selsby J.T., Morine K.J., Pendrak K., Barton E.R., Sweeney H.L. Rescue of dystrophic skeletal muscle by PGC-1α involves a fast to slow fiber type shift in the mdx mouse. PLoS ONE 2012, 7:e30063.
144. Sandri M. Autophagy in skeletal muscle. FEBS Lett 2010, 584:1411-1416.
145. De Palma C., Perrotta C., Pellegrino P., Clementi E., Cervia D. Skeletal muscle homeostasis in Duchenne muscular dystrophy: modulating autophagy as a promising therapeutic strategy. Front Aging Neurosci 2014, 6.
146. Lucas-Heron B. Muscular degeneration in Duchenne's dystrophy may be caused by a mitochondrial defect. Med Hypotheses 1995, 44:298-300.
147. Kelly-Worden M., Thomas E. Mitochondrial dysfunction in duchenne muscular dystrophy. Open J Endocr Metab Dis 2014, 2014.
148. Wallace D.C. Mitochondrial diseases in man and mouse. Science 1999, 283:1482-1488.
149. Yakes F.M., Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci 1997, 94:514-519.
150. Lin P.-H., Lee S.-H., Su C.-P., Wei Y.-H. Oxidative damage to mitochondrial DNA in atrial muscle of patients with atrial fibrillation. Free Radical Biol Med 2003, 35:1310-1318.
151. DiMauro S., Davidzon G. Mitochondrial DNA and disease. Ann Med 2005, 37:222-232.
152. Bonilla E., Schmidt B., Samitt C.E., et al. Normal and dystrophin-deficient muscle fibers in carriers of the gene for Duchenne muscular dystrophy. Am J Pathol 1988, 133:440.
153. Barbiroli B., Funicello R., Ferlini A., Montagna P., Zaniol P. Muscle energy metabolism in female DMD/BMD carriers: a 31P-MR spectroscopy study. Muscle Nerve 1992, 15:344-348.
154. Barbiroli B., Funicello R., Iotti S., Montagna P., Ferlini A., Zaniol P. 31P-NMR spectroscopy of skeletal muscle in Becker dystrophy and DMD/BMD carriers: altered rate of phosphate transport. J Neurol Sci 1992, 109:188-195.
155. Stephens J., Lewin E. Serum enzyme variations and histological abnormalities in the carrier state in Duchenne dystrophy. J Neurol Neurosurg Psychiatry 1965, 28:104.
156. Thomson W. The biochemical identification of the carrier state in X-linked recessive (Duchenne) muscular dystrophy. Clin Chim Acta Int J Clin Chem 1969, 26:207.
157. Wong L.J.C., Wladyka C., Mardach-Verdon R. A mitochondrial DNA mutation in a patient with an extensive family history of Duchenne muscular dystrophy. Muscle Nerve 2004, 30:118-122.
158. Hiona A., Leeuwenburgh C. The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging. Exp Gerontol 2008, 43:24-33.
159. Dirks A.J., Hofer T., Marzetti E., Pahor M., Leeuwenburgh C. Mitochondrial DNA mutations, energy metabolism and apoptosis in aging muscle. Ageing Res Rev 2006, 5:179-195.
160. Desler C., Hansen T.L., Frederiksen J.B., Marcker M.L., Singh K.K., Juel Rasmussen L. Is there a link between mitochondrial reserve respiratory capacity and aging?. J Aging Res 2012, 2012.
161. Baron D., Magot A., Ramstein G., et al. Immune response and mitochondrial metabolism are commonly deregulated in DMD and aging skeletal muscle. PLoS ONE 2011, 6:e26952.
162. Klamut H., Zubrzycka-Gaarn E., Bulman D., et al. Myogenic regulation of dystrophin gene expression. Br Med Bull 1989, 45:681-702.
163. Romero N.B., De Lonlay P., Llense S., et al. Pseudo-metabolic presentation in a Duchenne muscular dystrophy symptomatic carrier with 'de novo'duplication of dystrophin gene. Neuromuscul Disord 2001, 11:494-498.
164. Veerapandiyan A., Shashi V., Jiang Y.H., Gallentine W.B., Schoch K., Smith E.C. Pseudometabolic presentation of dystrophinopathy due to a missense mutation. Muscle Nerve 2010, 42:975-979.
165. Lam C., Lau C., Williams J., Chan Y., Wong L. Mitochondrial myopathy, encephalopathy, lactic acidosis and stroke-like episodes (MELAS) triggered by valproate therapy. Eur J Pediatr 1997, 156:562-564.
166. Wong L.C., Perng C., Hsu C., et al. Compensatory amplification of mtDNA in a patient with a novel deletion/duplication and high mutant load. J Med Genet 2003, 40. e125-e125.
167. Aartsma-Rus A., Van Deutekom J.C., Fokkema I.F., Van Ommen G.J.B., Den Dunnen J.T. Entries in the Leiden Duchenne muscular dystrophy mutation database: an overview of mutation types and paradoxical cases that confirm the reading-frame rule. Muscle Nerve 2006, 34:135-144.
168. Zucconi E., Valadares M.C., Vieira N.M., et al. Ringo: discordance between the molecular and clinical manifestation in a golden retriever muscular dystrophy dog. Neuromuscul Disord 2010, 20:64-70.
169. Zatz M., Vieira N.M., Zucconi E., et al. A normal life without muscle dystrophin. Neuromuscul Disord 2015, 25(5):371-374.
170. Vieira N.M., Guo L.T., Estrela E., Kunkel L.M., Zatz M., Shelton G.D. Muscular dystrophy in a family of labrador retrievers with no muscle dystrophin and a mild phenotype. Neuromuscul Disord 2015, 25(5):363-370.
171. Zatz M., Pavanello R., Lazar M., et al. Milder course in Duchenne patients with nonsense mutations and no muscle dystrophin. Neuromuscul Disord 2014, 24:986-989.
172. Dubowitz V. Enigmatic conflict of clinical and molecular diagnosis in Duchenne/Becker muscular dystrophy. Neuromuscul Disord 2006, 16:865-866.
173. M. Castro-Gago, Milder course in Duchenne patients with nonsense mutations and no, 2015.
174. Thomson W.H.S., Smith I. X-linked recessive (Duchenne) muscular dystrophy (DMD) and purine metabolism: effects of oral allopurinol and adenylate. Metabolism 1978, 27:151-163.
175. Castro-Gago M., Lojo S., Novo I., Del Río R., Peña J., Rodriguez-Segade S. Effects of chronic allopurinol therapy on purine metabolism in Duchenne muscular dystrophy. Biochem Biophys Res Commun 1987, 147:152-157.
176. Thomson W., Smith I. Allopurinol in Duchenne's muscular dystrophy. N Engl J Med 1978, 299:101.
177. Kulakowski S., Renoirte P., de Bruyn C. Dynamometric and biochemical observations in Duchenne patients receiving allopurinol. Neuropediatrics 1981, 12:92.
178. Felber S., Skladal D., Wyss M., Kremser C., Koller A., Sperl W. Oral creatine supplementation in Duchenne muscular dystrophy: a clinical and 31P magnetic resonance spectroscopy study. Neurol Res 2000, 22:145.
179. Tarnopolsky M., Martin J. Creatine monohydrate increases strength in patients with neuromuscular disease. Neurology 1999, 52. 854-854.
180. Tarnopolsky M., Mahoney D., Vajsar J., et al. Creatine monohydrate enhances strength and body composition in Duchenne muscular dystrophy. Neurology 2004, 62:1771-1777.
181. 31P MRS study. Magn Reson Imaging 2010, 28:698-707.
182. Bonsett C.A. Studies of Pseudohypertrophic Muscular Dystrophy 1969, Thomas, Springfield, Ill.
183. Sharma U., Atri S., Sharma M., Sarkar C., Jagannathan N. Skeletal muscle metabolism in Duchenne muscular dystrophy (DMD): An in-vitro proton NMR spectroscopy study. Magn Reson Imaging 2003, 21:145-153.
184. Nishio H., Wada H., Matsuo T., Horikawa H., Takahashi K., Nakajima T., et al. Glucose, free fatty acid and ketone body metabolism in Duchenne muscular dystrophy. Brain Dev 1990, 12:390-402.
185. Hankard R.G., Hammond D., Haymond M.W., Darmaun D. Oral glutamine slows down whole body protein breakdown in Duchenne muscular dystrophy. Pediatr Res 1998, 43:222-226.
186. Hankard R. Duchenne muscular dystrophy: A model for studying the contribution of muscle to energy and protein metabolism. Reprod Nutr Dev 1998, 38:181-186.
187. Ellis D.S., Strickland J.M. Differences in the metabolism of glucose between normal and dystrophic human muscle. Biochem J 1972, 130:17-18.
188. Thomson W.H.S., Leyburn P., Walton J.N. Serum enzyme activity in muscular dystrophy. Brit Med J 1960, 1276-1281.
189. Zatz M., Rapaport D., Vainzof M., Passos-Bueno M.R., Bortolini E.R., Pavanello R.C.M., et al. Serum creatine-kinase (CK) and pyruvate-kinase (PK) activities in Duchenne (DMD) as compared with Becker (BMD) muscular dystrophy. J Neurol Sci 1991, 102:190-196.
190. Ellis D. Intermediary metabolism of muscle in Duchenne muscular dystrophy. Brit Med Bull 1980, 36:165-172.
191. Stapleton D.I., Lau X., Flores M., Trieu J., Gehrig S.M., Chee A., et al. Dysfunctional muscle and liver glycogen metabolism in mdx dystrophic mice. PLoS ONE 2014, 9:e91514.
192. Mastaglia F., Kakulas B. Regeneration in Duchenne muscular dystrophy: A histological and histochemical study. Brain 1969, 92:809-818.
193. Engel A. Duchenne dystrophy. Myology 1986, 1185-1240. New York, McGraw-Hill. A. Engel, B.Q. Banker (Eds.).
194. Ronzoni E., Berg L., Landau W. Enzyme studies in progressive muscular dystrophy. Res. Publ. Ass. Nerv. Ment. Dis. 1960, 38:721-729.
195. Petell J.K., Marshall N.A., Lebherz H.G. Content and synthesis of several abundant glycolytic enzymes in skeletal muscles of normal and dystrophic mice. Int J Biochem 1984, 16:61-67.
196. Lin C.H., Hudson A.J., Strickland K.P. Fatty acid oxidation by skeletal muscle mitochondria in Duchenne muscular dystrophy. Life Sci II 1972, 11:355-362.
197. Carroll J.E., Norris B.J., Brooke M.H. Defective [U-14 C] palmitic acid oxidation in Duchenne muscular dystrophy. Neurology 1985, 35:96-97.
198. Scholte H., Luyt-Houwen I., Busch H., Jennekens F. Muscle mitochondria from patients with Duchenne muscular dystrophy have a normal beta oxidation, but an impaired oxidative phosphorylation. Neurology 1985, 35:1396-1397.
199. Borum P.R., Broquist H.P., Roelofs R.I. Muscle carnitine levels in neuromuscular disease. J Neurol Sci 1977, 34:279-286.
200. Carrier H.N., Berthillier G. Carnitine levels in normal children and adults and in patients with diseased muscle. Muscle Nerve 1980, 3:326-334.
201. Carroll J.E., Villadiego A., Brooke M.H. Increased long chain acyl CoA in Duchenne muscular dystrophy. Neurology 1983, 33:1507-1510.
202. Le Borgne F., Guyot S., Logerot M., Beney L., Gervais P., Demarquoy J. Exploration of lipid metabolism in relation with plasma membrane properties of Duchenne muscular dystrophy cells: Influence of L-carnitine. PLoS ONE 2012, 7:e49346.
203. Griffiths R.D., Cady E.B., Edwards R.H.T., Wilkie D.R. Muscle energy metabolism in Duchenne dystrophy studied by 31P-NMR: Controlled trials show no effect of allopurinol or ribose. Muscle Nerve 1985, 8:760-767.
204. 2+ handling and survival in mdx skeletal muscle cells. FEBS Lett 1998, 439:357-362.
205. Fitch CD, Rahmanian M. Creatine entry into skeletal muscle of normal and of dystrophic mice. In: Proceedings of the society for experimental biology and medicine. Society for experimental biology and medicine (New York, NY). Royal Society of Medicine; 1969. p. 236-9.
206. Martins-Bach A.B., Bloise A.C., Vainzof M., Rahnamaye Rabbani S. Metabolic profile of dystrophic mdx mouse muscles analyzed with in vitro magnetic resonance spectroscopy (MRS). Magn Reson Imaging 2012, 30:1167-1176.
207. Louis M., Raymackers J.M., Debaix H., Lebacq J., Francaux M. Effect of creatine supplementation on skeletal muscle of mdx mice. Muscle Nerve 2004, 29:687-692.
208. Ionasescu R., Kaeding L., Feld R., Witte D., Cancilla P., Stern L.Z. Alterations in creatine kinase in fresh muscle and cell cultures in Duchenne dystrophy. Ann Neurol 1981, 9:394-399.
209. Younkin D.P., Berman P., Sladky J., Chee C., Bank W., Chance B. 31P NMR studies in Duchenne muscular dystrophy. Neurology 1987, 37:165.
210. Benedict J.D., Kalinsky H.J., Scarrone L.A., Wertheim A.R., Stetten D. The origin of urinary creatine in progressive muscular dystrophy. J Clin Invest 1955, 34:141.
211. Bertorini T.E., Palmieri G.M.A., Airozo D., Edwards N.L., Fox I.H. Increased adenine nucleotide turnover in Duchenne muscular dystrophy. Pediatr Res 1981, 15:1478-1482.
212. de Bruyn C., Kulakowski S., van Bennekom C., Renoirte P., Müller M. Purine metabolism in Duchenne muscular dystrophy. Adv Exp Med Biol 1980, 122:177.