Muscle biopsies from human muscle diseases with myopathic pathology reveal common alterations in mitochondrial function

Journal of Neurochemistry

Volumn , Issue , 2016, Pages 174-191

  Sunitha, Balaraju ^a   Gayathri, Narayanappa ^a   Kumar, Manish ^b   Keshava Prasad, Thottethodi Subrahmanya ^a,b,c   Nalini, Atchayaram ^a   Padmanabhan, Balasundaram ^a   Srinivas Bharath, Muchukunte Mukunda ^a  

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

^b Institute of Bioinformatics   (India)

^c YENEPOYA UNIVERSITY   (India)

Author keywords

human; mitochondria; muscle; myopathy; proteomics; tryptophan oxidation

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ASPARTATE AMINOTRANSFERASE; CARDIOTOXIN; CITRATE SYNTHASE; MALATE DEHYDROGENASE; MITOCHONDRIAL PROTEIN; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE CYTOCHROME OXIDASE; SUPEROXIDE DISMUTASE; TRYPTOPHAN; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGED; ARTICLE; BIOCHEMICAL ANALYSIS; CHILD; CITRIC ACID CYCLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DISTAL MYOPATHY; DISTAL MYOPATHY WITH RIMMED VACUOLE; DOWN REGULATION; DYSFERLINOPATHY; ELECTRON MICROSCOPY; ENZYME HISTOCHEMISTRY; HUMAN; HUMAN TISSUE; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MITOCHONDRIAL MYOPATHY; MOLECULAR MODEL; MUSCLE BIOPSY; MUSCLE MITOCHONDRION; OXIDATION; POLYMYOSITIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEOMICS; RESPIRATORY CHAIN; TANDEM MASS SPECTROMETRY;

EID: 84976487626     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13626     Document Type: Article

References (74)

1. Bagnyukova T. V., Storey K. B. and Lushchak V. I. (2003) Induction of oxidative stress in Rana ridibunda during recovery from winter hibernation. J. Therm. Biol. 28, 21–28.
2. Baron D., Magot A., Ramstein G. et al. (2011) Immune response and mitochondrial metabolism are commonly deregulated in DMD and aging skeletal muscle. PLoS ONE 6, e26952.
3. Barreiro E. and Hussain S. N. (2010) Protein carbonylation in skeletal muscles: impact on function. Antioxid. Redox Signal. 12, 417–429.
4. Bashir R., Britton S., Strachan T. et al. (1998) A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Nat. Genet. 20, 37–42.
5. Berlett B. S. and Stadtman E. R. (1997) Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272, 20313–20316.
6. Bernardi P. and Bonaldo P. (2013) Mitochondrial dysfunction and defective autophagy in the pathogenesis of collagen VI muscular dystrophies. Cold Spring Harb. Perspect. Biol. 5, a011387.
7. 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.
8. Bourke S. C. and Gibson G. J. (2002) Sleep and breathing in neuromuscular disease. J. Eur. Respir. 19, 1194–1201.
9. 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.
10. Burr I. M., Asayama K. and Fenichel G. M. (1987) Superoxide dismutases, glutathione peroxidase, and catalase in neuromuscular disease. Muscle Nerve 10, 150–154.
11. Campos Y., Arenas J., Cabello A. and Gomez-Reino J. J. (1995) Respiratory chain enzyme defects in patients with idiopathic inflammatory myopathy. Ann. Rheum. Dis. 54, 491–493.
12. Cea G., Bendahan D., Manners D., Hilton-Jones D., Lodi R., Styles P. and Taylor D. J. (2002) Reduced oxidative phosphorylation and proton efflux suggest reduced capillary blood supply in skeletal muscle of patients with dermatomyositis and polymyositis: a quantitative 31P-magnetic resonance spectroscopy and MRI study. Brain 125, 1635–1645.
13. 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–H1514.
14. Corrado A., Cantatore F. P., Serlenga L., Amati A., Petruzzella V. and Lapadula G. (2002) Mitochondrial disease mimicking polymyositis: a case report. Clin. Rheumatol. 21, 411–414.
15. 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.
16. Cymerman I. A., Chung I., Beckmann B. M., Bujnicki J. M. and Meiss G. (2008) EXOG, a novel paralog of Endonuclease G in higher eukaryotes. Nucleic Acids Res. 36, 1369–1379.
17. 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.
18. Dimitri D. (2009) Inflammatory myopathies: diagnosis and classifications. Presse Med. 38, 1141–1163.
19. Dubowitz V. and Sewry C. A. (2007) Muscle Biopsy – A Practical Approach, pp. 293–323. Saunders Elsevier, Philadelphia.
20. 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–R710.
21. Duguay B. A. and Smiley J. R. (2013) Mitochondrial nucleases ENDOG and EXOG participate in mitochondrial DNA depletion initiated by herpes simplex virus 1 UL12.5. J. Virol. 87, 11787–11797.
22. Eisenberg I., Novershtern N., Itzhaki Z., Becker-Cohen M., Sadeh M., Willems P. H., Friedman N., Koopman W. J. and Mitrani-Rosenbaum S. (2008) Mitochondrial processes are impaired in hereditary inclusion body myopathy. Hum. Mol. Genet. 17, 3663–3674.
23. Emery A. E. (2002) The muscular dystrophies. Lancet 359, 687–695.
24. Emsley P., Lohkamp B., Scott W. G. and Cowtan K. (2010) Features and development of coot. Acta Crystallogr. D Biol Crystallogr, 66, 486–501.
25. FitzPatrick 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.
26. Fraysse B., Nagi S. M., Boher B., Ragot H., Laine J., Salmon A., Fiszman M. Y., Toussaint M. and Fromes Y. (2010) Ca2 + overload and mitochondrial permeability transition pore activation in living delta-sarcoglycan-deficient cardiomyocytes. Am. J. Physiol. Cell Physiol. 299, C706–C713.
27. Gao J., Schatton D., Martinelli P. et al. (2014) CLUH regulates mitochondrial biogenesis by binding mRNAs of nuclear-encoded mitochondrial proteins. J. Cell Biol. 207, 213–223.
28. Ghirardello A., Bassi N., Palma L., Borella E., Domeneghetti M., Punzi L. and Doria A. (2013) Autoantibodies in polymyositis and dermatomyositis. Curr. Rheumatol. Rep. 15, 335.
29. Gissel H. (2005) The role of Ca2 + in muscle cell damage. Ann. N. Y. Acad. Sci. 1066, 166–180.
30. Hicks D., Lampe A. K., Laval S. H. et al. (2009) Cyclosporine A treatment for Ullrich congenital muscular dystrophy: a cellular study of mitochondrial dysfunction and its rescue. Brain 132, 147–155.
31. Hoffman E. P. (2001) Dystrophinopathies, in Disorders of Voluntary Muscle, (Karpati G., Hilton-Jones D. and Griggs R. C., eds.), pp. 385–432. Cambridge University Press, Cambridge.
32. Honda A., Abe S., Hiroki E., Honda H., Iwanuma O., Yanagisawa N. and Ide Y. (2007) Activation of caspase 3, 9, 12, and Bax in masseter muscle of mdx mice during necrosis. J. Muscle Res. Cell Motil. 28, 243–247.
33. Jongpiputvanich S., Sueblinvong T. and Norapucsunton T. (2005) Mitochondrial respiratory chain dysfunction in various neuromuscular diseases. J. Clin. Neurosci. 12, 426–428.
34. Kang C. and Ji L. L. (2016) PGC-1alpha overexpression via local transfection attenuates mitophagy pathway in muscle disuse atrophy. Free Radic. Biol. Med. 93, 32–40.
35. Katsetos C. D., Koutzaki S. and Melvin J. J. (2013) Mitochondrial dysfunction in neuromuscular disorders. Semin. Pediatr. Neurol. 20, 202–215.
36. Kitto G. B. and Lewis R. G. (1967) Purification and properties of tuna supernatant and mitochondrial malate dehydrogenases. Biochimica et Biophysica Acta (BBA) - Enzymology, 139, 1–15.
37. Kramerova I., Kudryashova E., Wu B., Germain S., Vandenborne K., Romain N., Haller R. G., Verity M. A. and Spencer M. J. (2009) Mitochondrial abnormalities, energy deficit and oxidative stress are features of calpain 3 deficiency in skeletal muscle. Hum. Mol. Genet. 18, 3194–3205.
38. Liu J., Aoki M., Illa I. et al. (1998) Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat. Genet. 20, 31–36.
39. Liu F., Lou J., Zhao D., Li W., Zhao Y., Sun X. and Yan C. (2015) Dysferlinopathy: mitochondrial abnormalities in human skeletal muscle. Int. J. Neurosci. 126, 499–509.
40. Lodi R., Taylor D. J., Tabrizi S. J., Hilton-Jones D., Squier M. V., Seller A., Styles P. and Schapira A. H. (1998) Normal in vivo skeletal muscle oxidative metabolism in sporadic inclusion body myositis assessed by 31P-magnetic resonance spectroscopy. Brain 121(Pt 11), 2119–2126.
41. 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.
42. Lu X., Peng Q. and Wang G. (2015) Discovery of new biomarkers of idiopathic inflammatory myopathy. Clin. Chim. Acta 444, 117–125.
43. Matsuyama S. and Reed J. C. (2000) Mitochondria-dependent apoptosis and cellular pH regulation. Cell Death Differ. 7, 1155–1165.
44. Mehta S. (2006) Neuromuscular disease causing acute respiratory failure. Respir. Care 51, 1016–1021.
45. Menazza S., Blaauw B., Tiepolo T. et al. (2010) Oxidative stress by monoamine oxidases is causally involved in myofiber damage in muscular dystrophy. Hum. Mol. Genet. 19, 4207–4215.
46. Merlini L., Angelin A., Tiepolo T. et al. (2008) Cyclosporin A corrects mitochondrial dysfunction and muscle apoptosis in patients with collagen VI myopathies. Proc. Natl Acad. Sci. USA 105, 5225–5229.
47. Millay D. P., Sargent M. A., Osinska H., Baines C. P., Barton E. R., Vuagniaux G., Sweeney H. L., Robbins J. and Molkentin J. D. (2008) Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat. Med. 14, 442–447.
48. Nalini A., Gayathri N., Nishino I. and Hayashi Y. K. (2013) GNE Myopathy in India. Neurol. India 61, 371–374.
49. Ng R., Banks G. B., Hall J. K. et al. (2012) Animal models of muscular dystrophy. Prog. Mol. Biol. Transl. Sci. 105, 83–111.
50. Oldfors A., Moslemi A. R., Jonasson L., Ohlsson M., Kollberg G. and Lindberg C. (2006) Mitochondrial abnormalities in inclusion-body myositis. Neurology 66, S49–S55.
51. 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.
52. Pawar H., Kashyap M. K., Sahasrabuddhe N. A. et al. (2011) Quantitative tissue proteomics of esophageal squamous cell carcinoma for novel biomarker discovery. Cancer Biol. Ther. 12, 510–522.
53. Percival J. M., Siegel M. P., Knowels G. and Marcinek D. J. (2013) 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. 22, 153–167.
54. Ramadasan-Nair R., Gayathri N., Mishra S. et al. (2014) Mitochondrial alterations and oxidative stress in an acute transient mouse model of muscle degeneration: implications for muscular dystrophy and related muscle pathologies. J. Biol. Chem. 289, 485–509.
55. Renjini R., Gayathri N., Nalini A. and Srinivas Bharath M. M. (2012a) Analysis of calpain-3 protein in muscle biopsies of different muscular dystrophies from India. Indian J. Med. Res. 135, 878–886.
56. Renjini R., Gayathri N., Nalini A. and Srinivas Bharath M. M. (2012b) Oxidative damage in muscular dystrophy correlates with the severity of the pathology: role of glutathione metabolism. Neurochem. Res. 37, 885–898.
57. Romanello V. and Sandri M. (2015) Mitochondrial quality control and muscle mass maintenance. Front. Physiol. 6, 422.
58. Rusconi F., Mancinelli E., Colombo G., Cardani R., Da Riva L., Bongarzone I., Meola G. and Zippel R. (2010) Proteome profile in Myotonic Dystrophy type 2 myotubes reveals dysfunction in protein processing and mitochondrial pathways. Neurobiol. Dis. 38, 273–280.
59. Ryan B. J., Nissim A. and Winyard P. G. (2014) Oxidative post-translational modifications and their involvement in the pathogenesis of autoimmune diseases. Redox. Biol. 2, 715–724.
60. Rybalka E., Timpani C. A., Cooke M. B., Williams A. D. and Hayes A. (2014) Defects in mitochondrial ATP synthesis in dystrophin-deficient mdx skeletal muscles may be caused by complex I insufficiency. PLoS ONE 9, e115763.
61. Schuh R. A., Jackson K. C., Khairallah R. J., Ward C. W. and Spangenburg E. E. (2012) Measuring mitochondrial respiration in intact single muscle fibers. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302, R712–R719.
62. Siepmann T., Tesch M., Krause F., Illigens B. M. and Stoltenburg-Didinger G. (2013) Polymyositis with cytochrome C oxidase negative fibers–a pathological and clinical challenge. Ann. Diagn. Pathol. 17, 183–186.
63. Srere P. A. (1969) [1] Citrate synthase: [EC 4.1.3.7. Citrate oxaloacetate-lyase (CoA-acetylating)], in Methods in Enzymology (John M. L. ed), Vol. 13, pp. 3–11. Academic Press, New York and London.
64. Tagliavini F., Sardone F., Squarzoni S., Maraldi N. M., Merlini L., Faldini C. and Sabatelli P. (2013) Ultrastructural changes in muscle cells of patients with collagen VI-related myopathies. Muscles Ligaments Tendons J. 3, 281–286.
65. Taylor C. F., Paton N. W., Garwood K. L. et al. (2003a) A systematic approach to modeling, capturing, and disseminating proteomics experimental data. Nat. Biotechnol. 21, 247–254.
66. Taylor S. W., Fahy E., Murray J., Capaldi R. A. and Ghosh S. S. (2003b) Oxidative post-translational modification of tryptophan residues in cardiac mitochondrial proteins. J. Biol. Chem. 278, 19587–19590.
67. Tews D. S. (2002) Apoptosis and muscle fibre loss in neuromuscular disorders. Neuromuscul. Disord. 12, 613–622.
68. Tews D. S. and Goebel H. H. (1998) Cell death and oxidative damage in inflammatory myopathies. Clin. Immunol. Immunopathol. 87, 240–247.
69. Tondera D., Czauderna F., Paulick K., Schwarzer R., Kaufmann J. and Santel A. (2005) The mitochondrial protein MTP18 contributes to mitochondrial fission in mammalian cells. J. Cell Sci. 118, 3049–3059.
70. 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.
71. Turki A., Hayot M., Carnac G. et al. (2012) Functional muscle impairment in facioscapulohumeral muscular dystrophy is correlated with oxidative stress and mitochondrial dysfunction. Free Radic. Biol. Med. 53, 1068–1079.
72. Vizcaino J. A., Deutsch E. W., Wang R. et al. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32, 223–226.
73. Winter L., Kuznetsov A. V., Grimm M., Zeold A., Fischer I. and Wiche G. (2015) Plectin isoform P1b and P1d deficiencies differentially affect mitochondrial morphology and function in skeletal muscle. Hum. Mol. Genet. 24, 4530–4544.
74. Zulian A., Tagliavini F., Rizzo E. et al. (2014) Melanocytes from patients affected by ullrich congenital muscular dystrophy and bethlem myopathy have dysfunctional mitochondria that can be rescued with cyclophilin inhibitors. Front. Aging Neurosci. 6, 324.