Mitochondrial alterations and oxidative stress in an acute transient mouse model of muscle degeneration: Implications for Muscular dystrophy and related muscle pathologies

Journal of Biological Chemistry

Volumn 289, Issue 1, 2014, Pages 485-509

  Ramadasan Nair, Renjini ^a   Gayathri, Narayanappa ^a   Mishra, Sudha ^a   Sunitha, Balaraju ^a   Mythri, Rajeswara Babu ^a   Nalini, Atchayaram ^a   Subbannayya, Yashwanth ^b   Harsha, Hindalahalli Chandregowda ^b   Kolthur Seetharam, Ullas ^c   Bharath, Muchukunte Mukunda Srinivas ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH AND NEUROSCIENCES   (India)

^b Institute of Bioinformatics   (India)

^c TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; MACHINERY; MAMMALS; MASS SPECTROMETRY; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PROTEINS;

DUCHENNE MUSCULAR DYSTROPHIES; EXPERIMENTAL MODELING; FATTY ACID METABOLISM; GLUTATHIONE REDUCED; MITOCHONDRIAL DAMAGE; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL PROTEIN; ULTRASTRUCTURAL CHANGES;

MUSCLE;

ADENOSINE TRIPHOSPHATE; CALCIUM; CARDIOTOXIN; GLUTATHIONE; MITOCHONDRIAL PROTEIN; COBROTOXIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CELL ULTRASTRUCTURE; CHILD; CITRIC ACID CYCLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DUCHENNE MUSCULAR DYSTROPHY; ENZYME ASSAY; EXPERIMENTAL MODEL; FATTY ACID METABOLISM; FEMALE; GRIP STRENGTH; HEREDITARY MOTOR SENSORY NEUROPATHY; HISTOCHEMISTRY; HUMAN; MALE; MASS SPECTROMETRY; MOUSE; MUSCLE ATROPHY; MUSCULAR DYSTROPHY; MYOSITIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SARCOLEMMA; UNINDEXED SEQUENCE; WESTERN BLOTTING; ADOLESCENT; AGED; ANIMAL; ANIMAL MUSCULAR DYSTROPHY; CELL LINE; CHEMICALLY INDUCED; CLINICAL TRIAL; GENE EXPRESSION REGULATION; INFANT; METABOLISM; MIDDLE AGED; MUSCLE MITOCHONDRION; MYOBLAST; PATHOLOGY; PRESCHOOL CHILD; TOXICITY;

ADOLESCENT; ADULT; AGED; ANIMALS; CELL LINE; CHILD; CHILD, PRESCHOOL; COBRA CARDIOTOXIN PROTEINS; GENE EXPRESSION REGULATION; HUMANS; INFANT; MICE; MIDDLE AGED; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; MYOBLASTS, SKELETAL; OXIDATIVE STRESS;

EID: 84891709202     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.493270     Document Type: Article

References (97)

1. Emery, A. E. (2002) The muscular dystrophies. Lancet 359, 687-695 (Pubitemid 34203773)
2. Hoffman, E. P. (2001) in Disorders of Voluntary Muscle (Karpati, G., Hilton-Jones, D., and Griggs, R. C., eds) 7 Ed., pp. 385-432, Cambridge University Press, Cambridge
3. Fairclough, R. J., Perkins, K. J., and Davies, K. E. (2012) Pharmacologically targeting the primary defect and downstream pathology in Duchenne muscular dystrophy. Curr. Gene Ther. 12, 206-244
4. Dimitri, D. (2009) Inflammatory myopathies. Diagnosis and classifications. Presse Med. 38, 1141-1163
5. Gissel, H. (2005) The role of Ca2+ in muscle cell damage. Ann. N. Y. Acad. Sci. 1066, 166-180
6. Jongpiputvanich, S., Sueblinvong, T., and Norapucsunton, T. (2005) Mitochondrial respiratory chain dysfunction in various neuromuscular diseases. J. Clin. Neurosci. 12, 426-428 (Pubitemid 40745228)
7. Burr, I. M., Asayama, K., and Fenichel, G. M. (1987) Superoxide dismutases, glutathione peroxidase, and catalase in neuromuscular disease. Muscle Nerve 10, 150-154 (Pubitemid 17004219)
8. Ng, R., Banks, G. B., Hall, J. K., Muir, L. A., Ramos, J. N., Wicki, J., Odom, G. L., Konieczny, P., Seto, J., Chamberlain, J. R., and Chamberlain, J. S. (2012) Animal models of muscular dystrophy. Prog. Mol. Biol. Transl. Sci. 105, 83-111
9. Kherif, S., Lafuma, C., Dehaupas, M., Lachkar, S., Fournier, J. G., Verdière-Sahuqué, M., Fardeau, M., and Alameddine, H. S. (1999) Expression of matrix metalloproteinases 2 and 9 in regenerating skeletal muscle. Astudy in experimentally injured and mdx muscles. Dev. Biol. 205, 158-170 (Pubitemid 29042665)
10. Bernardi, P. (1999) Mitochondria in muscle cell death. Ital. J. Neurol. Sci. 20, 395-400 (Pubitemid 30202016)
11. Paternostro-Sluga, T., Grim-Stieger, M., Posch, M., Schuhfried, O., Vacariu, G., Mittermaier, C., Bittner, C., and Fialka-Moser, V. (2008) Reliability and validity of the Medical Research Council (MRC) scale and a modified scale for testing muscle strength in patients with radial palsy. J. Rehabil. Med. 40, 665-671
12. Renjini, R., Gayathri, N., Nalini, A., and Srinivas Bharath, M. M. (2012) Analysis of calpain-3 protein in muscle biopsies of different muscular dystrophies from India. Indian J. Med. Res. 135, 878-886
13. Renjini, R., Gayathri, N., Nalini, A., and Srinivas Bharath, M. M. (2012) Oxidative damage in muscular dystrophy correlates with the severity of the pathology. Role of glutathione metabolism. Neurochem. Res. 37, 885-898
14. Smith, J. P., Hicks, P. S., Ortiz, L. R., Martinez, M. J., and Mandler, R. N. (1995) Quantitative measurement of muscle strength in the mouse. J. Neurosci. Methods 62, 15-19
15. Dubowitz, V., and Sewry, C. A. (2007) Muscle Biopsy. A Practical Approach, 3 Ed., pp. 293-323, Saunders Elsevier, Philadelphia, PA
16. Ardite, E., Barbera, J. A., Roca, J., and Fernández-Checa, J. C. (2004) Glutathione depletion impairs myogenic differentiation of murine skeletal muscle C2C12 cells through sustained NF-B activation. Am. J. Pathol. 165, 719-728 (Pubitemid 39129280)
17. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
18. Grynkiewicz, G., Poenie, M., and Tsien, R. Y. (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450 (Pubitemid 15114340)
19. Peng, T. I., and Greenamyre, J. T. (1998) Privileged access to mitochondria of calcium influx through N-methyl-D-aspartate receptors. Mol. Pharmacol. 53, 974-980 (Pubitemid 28280438)
20. Neri, S., Mariani, E., Meneghetti, A., Cattini, L., and Facchini, A. (2001) Calcein-acetyoxymethyl cytotoxicity assay. Standardization of a method allowing additional analyses on recovered effector cells and supernatants. Clin. Diagn Lab. Immunol. 8, 1131-1135 (Pubitemid 33035744)
21. Reers, M., Smith, T. W., and Chen, L. B. (1991) J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30, 4480-4486
22. Budd, S. L., Castilho, R. F., and Nicholls, D. G. (1997) Mitochondrial membrane potential and hydroethidine-monitored superoxide generation in cultured cerebellar granule cells. FEBS Lett. 415, 21-24 (Pubitemid 27402041)
23. López-Figueroa, M. O., Caamaño, C., Morano, M. I., Rønn, L. C., Akil, H., and Watson, S. J. (2000) Direct evidence of nitric oxide presence within mitochondria. Biochem. Biophys. Res. Commun. 272, 129-133 (Pubitemid 30444910)
24. Bhattacharya, S. K., Thakar, J. H., Johnson, P. L., and Shanklin, D. R. (1991) Isolation of skeletal muscle mitochondria from hamsters using an ionic medium containing ethylenediaminetetraacetic acid and nagarse. Anal. Biochem. 192, 344-349
25. Trounce, I. A., Kim, Y. L., Jun, A. S., and Wallace, D. C. (1996) Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol. 264, 484-509
26. Srere, P. A. (1969) [1] Citrate synthase: [EC 4.1.3.7. Citrate oxaloacetatelyase (CoA-acetylating)]. Methods Enzymol. 13, 3-11
27. Castro, L., Rodriguez, M., and Radi, R. (1994) Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J. Biol. Chem. 269, 29409-29415 (Pubitemid 24365085)
28. Jacobson, E. L., and Jacobson, M. K. (1976) Pyridine nucleotide levels as a function of growth in normal and transformed 3T3 cells. Arch. Biochem. Biophys. 175, 627-634
29. Hissin, P. J., and Hilf, R. (1976) A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 74, 214-226
30. Choi, A. O., Cho, S. J., Desbarats, J., Lovrić, J., and Maysinger, D. (2007) Quantum dot-induced cell death involves Fas up-regulation and lipid peroxidation in human neuroblastoma cells. J. Nanobiotechnology 5, 1
31. Sultana, R., and Butterfield, D. A. (2011) Identification of the oxidative stress proteome in the brain. Free Radic Biol. Med. 50, 487-494
32. Owen, J. B., Opii, W. O., Ramassamy, C., Pierce, W. M., and Butterfield, D. A. (2008) Proteomic analysis of brain protein expression levels in NF-κβ p50 -/- homozygous knockout mice. Brain Res. 1240, 22-30
33. Thongboonkerd, V., McLeish, K. R., Arthur, J. M., and Klein, J. B. (2002) Proteomic analysis of normal human urinary proteins isolated by acetone precipitation or ultracentrifugation. Kidney Int. 62, 1461-1469
34. Marimuthu, A., O'Meally, R. N., Chaerkady, R., Subbannayya, Y., Nanjappa, V., Kumar, P., Kelkar, D. S., Pinto, S. M., Sharma, R., Renuse, S., Goel, R., Christopher, R., Delanghe, B., Cole, R. N., Harsha, H. C., and Pandey, A. (2011) A comprehensive map of the human urinary proteome. J. Proteome Res. 10, 2734-2743
35. Banerjee, K. K., Ayyub, C., Sengupta, S., and Kolthur-Seetharam, U. (2012) dSir2 deficiency in the fatbody, but not muscles, affects systemic insulin signaling, fat mobilization and starvation survival in flies. Aging 4, 206-223
36. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
37. Pawar, H., Kashyap, M. K., Sahasrabuddhe, N. A., Renuse, S., Harsha, H. C., Kumar, P., Sharma, J., Kandasamy, K., Marimuthu, A., Nair, B., Rajagopalan, S., Maharudraiah, J., Premalatha, C. S., Kumar, K. V., Vijayakumar, M., Chaerkady, R., Prasad, T. S., Kumar, R. V., Kumar, R. V., and Pandey, A. (2011) Quantitative tissue proteomics of esophageal squamous cell carcinoma for novel biomarker discovery. Cancer Biol. Ther. 12, 510-522
38. Patel, H. V., Vyas, A. A., Vyas, K. A., Liu, Y. S., Chiang, C. M., Chi, L. M., and Wu, W. (1997) Heparin and heparan sulfate bind to snake cardiotoxin. Sulfated oligosaccharides as a potential target for cardiotoxin action. J. Biol. Chem. 272, 1484-1492 (Pubitemid 27043225)
39. Yan, Z., Choi, S., Liu, X., Zhang, M., Schageman, J. J., Lee, S. Y., Hart, R., Lin, L., Thurmond, F. A., and Williams, R. S. (2003) Highly coordinated gene regulation in mouse skeletal muscle regeneration. J. Biol. Chem. 278, 8826-8836 (Pubitemid 36800642)
40. Sandri, M., Minetti, C., Pedemonte, M., and Carraro, U. (1998) Apoptotic myonuclei in human Duchenne muscular dystrophy. Lab. Invest. 78, 1005-1016 (Pubitemid 28378214)
41. Chen, Y. W., Nagaraju, K., Bakay, M., McIntyre, O., Rawat, R., Shi, R., and Hoffman, E. P. (2005) Early onset of inflammation and later involvement of TGFβ in Duchenne muscular dystrophy. Neurology 65, 826-834 (Pubitemid 41362124)
42. Onofre-Oliveira, P. C., Santos, A. L., Martins, P. M., Ayub-Guerrieri, D., and Vainzof, M. (2012) Differential expression of genes involved in the degeneration and regeneration pathways in mouse models for muscular dystrophies. Neuromolecular Med. 14, 74-83
43. Parker, M. H., Loretz, C., Tyler, A. E., Snider, L., Storb, R., and Tapscott, S. J. (2012) Inhibition of CD26/DPP-IV enhances donor muscle cell engraftment and stimulates sustained donor cell proliferation. Skelet. Muscle 2, 4
44. Emery, A. E. (1977) Muscle histology and creatine kinase levels in the foetus in Duchenne muscular dystrophy. Nature 266, 472-473 (Pubitemid 8067233)
45. Sabatelli, P., Pellegrini, C., Faldini, C., and Merlini, L. (2012) Cytoskeletal and extracellular matrix alterations in limb girdle muscular dystrophy 2I muscle fibers. Neurol. India 60, 510-511
46. Turki, A., Hayot, M., Carnac, G., Pillard, F., Passerieux, E., Bommart, S., Raynaud De Mauverger, E., Hugon, G., Pincemail, J., Pietri, S., Lambert, K., Belayew, A., Vassetzky, Y., Juntas Morales, R., Mercier, J., and Laoudj-Chenivesse, D. (2012) Functional muscle impairment in facioscapulohumeral muscular dystrophy is correlated with oxidative stress and mitochondrial dysfunction. Free Radic. Biol. Med. 53, 1068-1079
47. Berlett, B. S., and Stadtman, E. R. (1997) Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272, 20313-20316 (Pubitemid 27355575)
48. Kudryashova, E., Kramerova, I., and Spencer, M. J. (2012) Satellite cell senescence underlies myopathy in a mouse model of limb-girdle muscular dystrophy 2H. J. Clin. Invest. 122, 1764-1776
49. Yugeta, N., Urasawa, N., Fujii, Y., Yoshimura, M., Yuasa, K., Wada, M. R., Nakura, M., Shimatsu, Y., Tomohiro, M., Takahashi, A., Machida, N., Wakao, Y., Nakamura, A., and Takeda, S. (2006) Cardiac involvement in Beagle-based canine X-linked muscular dystrophy in Japan (CXMDJ). Electrocardiographic, echocardiographic, and morphologic studies. BMC Cardiovasc. Disord. 6, 47
50. Tsai, P. C., Hsieh, C. Y., Chiu, C. C., Wang, C. K., Chang, L. S., and Lin, S. R. (2012) Cardiotoxin III suppresses MDA-MB-231 cell metastasis through the inhibition of EGF/EGFR-mediated signaling pathway. Toxicon 60, 734-743
51. Chien, C. M., Chang, S. Y., Lin, K. L., Chiu, C. C., Chang, L. S., and Lin, S. R. (2010) Taiwan cobra cardiotoxin III inhibits Src kinase leading to apoptosis and cell cycle arrest of oral squamous cell carcinoma Ca9-22 cells. Toxicon 56, 508-520
52. Wang, C. H., Monette, R., Lee, S. C., Morley, P., and Wu, W. G. (2005) Cobra cardiotoxin-induced cell death in fetal rat cardiomyocytes and cortical neurons. Different pathway but similar cell surface target. Toxicon 46, 430-440 (Pubitemid 41218738)
53. Wang, Y. X., and Rudnicki, M. A. (2012) Satellite cells, the engines of muscle repair. Nat. Rev. Mol. Cell Biol. 13, 127-133
54. Messina, S., Mazzeo, A., Bitto, A., Aguennouz, M., Migliorato, A., De Pasquale, M. G., Minutoli, L., Altavilla, D., Zentilin, L., Giacca, M., Squadrito, F., and Vita, G. (2007) VEGF overexpression via adeno-associated virus gene transfer promotes skeletal muscle regeneration and enhances muscle function in mdx mice. FASEB J. 21, 3737-3746 (Pubitemid 350075161)
55. Wanschitz, J. V., Dubourg, O., Lacene, E., Fischer, M. B., Höftberger, R., Budka, H., Romero, N. B., Eymard, B., Herson, S., Butler-Browne, G. S., Voit, T., and Benveniste, O. (2013) Expression of myogenic regulatory factors and myo-endothelial remodeling in sporadic inclusion body myositis. Neuromuscul. Disord. 23, 75-83
56. Marshall, J. L., Holmberg, J., Chou, E., Ocampo, A. C., Oh, J., Lee, J., Peter, A. K., Martin, P. T., and Crosbie-Watson, R. H. (2012) Sarcospan-dependent Akt activation is required for utrophin expression and muscle regeneration. J. Cell Biol. 197, 1009-1027
57. Fadic, R. (2005) Cell surface and gene expression regulation molecules in dystrophinopathy. mdx vs. Duchenne. Biol. Res. 38, 375-380
58. Paco, S., Ferrer, I., Jou, C., Cusí, V., Corbera, J., Torner, F., Gualandi, F., Sabatelli, P., Orozco, A., Gómez-Foix, A. M., Colomer, J., Nascimento, A., and Jimenez-Mallebrera, C. (2012) Muscle fiber atrophy and regeneration coexist in collagen VI-deficient human muscle. Role of calpain-3 and nuclear factor-B signaling. J. Neuropathol. Exp. Neurol. 71, 894-906
59. Sandri, M., and Carraro, U. (1999) Apoptosis of skeletal muscles during development and disease. Int. J. Biochem. Cell Biol. 31, 1373-1390
60. Spencer, M. J., Walsh, C. M., Dorshkind, K. A., Rodriguez, E. M., and Tidball, J. G. (1997) Myonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity. J. Clin. Invest. 99, 2745-2751 (Pubitemid 27259822)
61. Warren, G. L., Hulderman, T., Jensen, N., McKinstry, M., Mishra, M., Luster, M. I., and Simeonova, P. P. (2002) Physiological role of tumor necrosis factor α in traumatic muscle injury. FASEB J. 16, 1630-1632
62. Kuru, S., Inukai, A., Kato, T., Liang, Y., Kimura, S., and Sobue, G. (2003) Expression of tumor necrosis factor-α in regenerating muscle fibers in inflammatory and non-inflammatory myopathies. Acta Neuropathol. 105, 217-224 (Pubitemid 36798812)
63. Enwere, E. K., Boudreault, L., Holbrook, J., Timusk, K., Earl, N., La Casse, E., Renaud, J. M., and Korneluk, R. G. (2013) Loss of cIAP1 attenuates soleus muscle pathology and improves diaphragm function in mdx mice. Hum. Mol. Genet. 22, 867-878
64. Wang, C. H., and Wu, W. G. (2005) Amphiphilic beta-sheet cobra cardiotoxin targets mitochondria and disrupts its network. FEBS Lett. 579, 3169-3174
65. Ownby, C. L., Fletcher, J. E., and Colberg, T. R. (1993) Cardiotoxin 1 from cobra (Naja naja atra) venom causes necrosis of skeletal muscle in vivo. Toxicon 31, 697-709
66. Brown, S., and Lucy, J. A. (1997) Dystrophin. Gene, Protein and Cell Biology, pp. 79-100, Cambridge University Press, Cambridge
67. Berchtold, M. W., Brinkmeier, H., and Müntener, M. (2000) Calcium ion in skeletal muscle. Its crucial role for muscle function, plasticity, and disease. Physiol. Rev. 80, 1215-1265 (Pubitemid 30452014)
68. Turner, P. R., Fong, P. Y., Denetclaw, W. F., and Steinhardt, R. A. (1991) Increased calcium influx in dystrophic muscle. J. Cell Biol. 115, 1701-1712 (Pubitemid 21910010)
69. Robin, G., Berthier, C., and Allard, B. (2012) Sarcoplasmic reticulum Ca2+ permeation explored from the lumen side in mdx muscle fibers under voltage control. J. Gen. Physiol 139, 209-218
70. Goonasekera, S. A., Lam, C. K., Millay, D. P., Sargent, M. A., Hajjar, R. J., Kranias, E. G., and Molkentin, J. D. (2011) Mitigation of muscular dystrophy in mice by SERCA overexpression in skeletal muscle. J. Clin. Invest. 121, 1044-1052
71. Iwata, Y., Katanosaka, Y., Arai, Y., Shigekawa, M., and Wakabayashi, S. (2009) Dominant-negative inhibition of Ca2+ influx via TRPV2 ameliorates muscular dystrophy in animal models. Hum. Mol. Genet. 18, 824-834
72. Hopf, F. W., Turner, P. R., and Steinhardt, R. A. (2007) Calcium misregulation and the pathogenesis of muscular dystrophy. Subcell. Biochem. 45, 429-464
73. Fraysse, B., Liantonio, A., Cetrone, M., Burdi, R., Pierno, S., Frigeri, A., Pisoni, M., Camerino, C., and De Luca, A. (2004) The alteration of calcium homeostasis in adult dystrophic mdx muscle fibers is worsened by a chronic exercise in vivo. Neurobiol. Dis. 17, 144-154 (Pubitemid 39345770)
74. Dalle-Donne, I., Scaloni, A., Giustarini, D., Cavarra, E., Tell, G., Lungarella, G., Colombo, R., Rossi, R., and Milzani, A. (2005) Proteins as biomarkers of oxidative/nitrosative stress in diseases. The contribution of redox proteomics. Mass Spectrom. Rev. 24, 55-99 (Pubitemid 40146422)
75. Bernardi, P., Krauskopf, A., Basso, E., Petronilli, V., Blachly-Dyson, E., Blalchy-Dyson, E., Di Lisa, F., and Forte, M. A. (2006) The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J. 273, 2077-2099
76. Fraysse, B., Nagi, S. M., Boher, B., Ragot, H., Lainé, J., Salmon, A., Fiszman, M. Y., Toussaint, M., and Fromes, Y. (2010) Ca2+ overload and mitochondrial permeability transition pore activation in living α-sarcoglycan-deficient cardiomyocytes. Am. J. Physiol. Cell Physiol. 299, C706-713
77. Tews, D. S. (2002) Apoptosis and muscle fibre loss in neuromuscular disorders. Neuromuscul. Disord. 12, 613-622
78. Carberry, S., Zweyer, M., Swandulla, D., and Ohlendieck, K. (2012) Profiling of age-related changes in the tibialis anterior muscle proteome of the mdx mouse model of dystrophinopathy. J. Biomed. Biotechnol. 2012, 691641
79. Baron, D., Magot, A., Ramstein, G., Steenman, M., Fayet, G., Chevalier, C., Jourdon, P., Houlgatte, R., Savagner, F., and Pereon, Y. (2011) Immune response and mitochondrial metabolism are commonly deregulated in DMD and aging skeletal muscle. PLoS One 6, e26952
80. Menazza, S., Blaauw, B., Tiepolo, T., Toniolo, L., Braghetta, P., Spolaore, B., Reggiani, C., Di Lisa, F., Bonaldo, P., and Canton, M. (2010) Oxidative stress by monoamine oxidases is causally involved in myofiber damage in muscular dystrophy. Hum. Mol. Genet. 19, 4207-4215
81. Tews, D. S., and Goebel, H. H. (1998) Cell death and oxidative damage in inflammatory myopathies. Clin. Immunol. Immunopathol. 87, 240-247 (Pubitemid 28285439)
82. Cotgreave, I. A., Goldschmidt, L., Tonkonogi, M., and Svensson, M. (2002) Differentiation-specific alterations to glutathione synthesis in and hormonally stimulated release from human skeletal muscle cells. FASEB J. 16, 435-437
83. Degl'Innocenti, D., Rosati, F., Iantomasi, T., Vincenzini, M. T., and Ramponi, G. (1999) GSH system in relation to redox state in dystrophic skin fibroblasts. Biochimie 81, 1025-1029
84. Wagner, A. E., Ernst, I. M., Birringer, M., Sancak, O., Barella, L., and Rimbach, G. (2012) A combination of lipoic acid plus coenzyme Q10 induces PGC1α, a master switch of energy metabolism, improves stress response, and increases cellular glutathione levels in cultured C2C12 skeletal muscle cells. Oxid. Med. Cell Longev. 2012, 835970
85. Comte, B., Vincent, G., Bouchard, B., Benderdour, M., and Des Rosiers, C. (2002) Reverse flux through cardiac NADP+-isocitrate dehydrogenase under normoxia and ischemia. Am. J. Physiol. Heart Circ. Physiol. 283, H1505-1514
86. Dudley, R. W., Khairallah, M., Mohammed, S., Lands, L., Des Rosiers, C., and Petrof, B. J. (2006) Dynamic responses of the glutathione system to acute oxidative stress in dystrophic mouse (mdx) muscles. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R704-710 (Pubitemid 44352353)
87. Barreiro, E., and Hussain, S. N. (2010) Protein carbonylation in skeletal muscles. Impact on function. Antioxid. Redox Signal. 12, 417-429
88. Fitz Patrick, D. R., Germain-Lee, E., and Valle, D. (1995) Isolation and characterization of rat and human cDNAs encoding a novel putative peroxisomal enoyl-CoA hydratase. Genomics 27, 457-466
89. Kovalyov, L. I., Kovalyova, M. A., Kovalyov, P. L., Serebryakova, M. V., Moshkovskii, S. A., and Shishkin, S. S. (2006) Polymorphism of 3, 5-2, 4-dienoyl-coenzyme A isomerase (the ECH1 gene product protein) in human striated muscle tissue. Biochemistry 71, 448-453
90. Nahleh, Z., Tfayli, A., Najm, A., El Sayed, A., and Nahle, Z. (2012) Heat shock proteins in cancer. Targeting the "chaperones." Future Med. Chem. 4, 927-935
91. Yamashima, T. (2012) Hsp70.1 and related lysosomal factors for necrotic neuronal death. J. Neurochem. 120, 477-494
92. Oikawa, S., Yamada, T., Minohata, T., Kobayashi, H., Furukawa, A., Tada-Oikawa, S., Hiraku, Y., Murata, M., Kikuchi, M., and Yamashima, T. (2009) Proteomic identification of carbonylated proteins in the monkey hippocampus after ischemia-reperfusion. Free Radic. Biol. Med. 46, 1472-1477
93. Moller, I. M., and Kristensen, B. K. (2004) Protein oxidation in plant mitochondria as a stress indicator. Photochem. Photobiol. Sci. 3, 730-735 (Pubitemid 39302971)
94. Szöke, D., and Panteghini, M. (2012) Diagnostic value of transferrin. Clin. Chim. Acta 413, 1184-1189
95. Matsuda, R., Spector, D., Micou-Eastwood, J., and Strohman, R. C. (1984) There is selective accumulation of a growth factor in chicken skeletal muscle. II. Transferrin accumulation in dystrophic fast muscle. Dev. Biol. 103, 276-284
96. Ghosh, A. K., and Jacobs-Lorena, M. (2011) Surface-expressed enolases of Plasmodium and other pathogens. Mem. Inst. Oswaldo Cruz 106, 85-90
97. Lopez-Alemany, R., Suelves, M., Diaz-Ramos, A., Vidal, B., and Munoz-Canoves, P. (2005) α-Enolase plasminogen receptor in myogenesis. Front. Biosci. 10, 30-36