Attenuation of free radical production and paracrystalline inclusions by creatine supplementation in a patient with a novel cytochrome b mutation

Muscle and Nerve

Volumn 29, Issue 4, 2004, Pages 537-547

  Tarnopolsky, Mark A ^a   Simon, David K ^b   Roy, Brian D ^a   Chorneyko, Kathy ^a   Lowther, Stuart A ^a   Johns, Donald R ^b   Sandhu, Jagdeep K ^c   Li, Yan ^c   Sikorska, Marianna ^c  

^a MCMASTER UNIVERSITY MEDICAL CENTRE   (Canada)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Creatine kinase; Cybrids; Dietary supplements; Exercise; Mitochondrial myopathy

Indexed keywords

ADENOSINE TRIPHOSPHATE; CREATINE; CYTOCHROME B; FREE RADICAL; MITOCHONDRIAL DNA; PEROXYNITRITE;

ADULT; ARTICLE; CASE REPORT; CELL SURVIVAL; CELL TRANSFORMATION; DIET SUPPLEMENTATION; DNA SEQUENCE; ELECTRON MICROSCOPY; EXERCISE; HUMAN; HUMAN TISSUE; MALE; MUSCLE BIOPSY; OXIDATIVE STRESS; POINT MUTATION; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ADULT; CELL SURVIVAL; CREATINE; CYTOCHROMES B; DNA, MITOCHONDRIAL; EXERCISE TEST; FREE RADICALS; HUMANS; INCLUSION BODIES; MALE; MITOCHONDRIAL MYOPATHIES; MUSCLE, SKELETAL; MUTATION; PEROXYNITROUS ACID; PHYSICAL ENDURANCE; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPORTS;

EID: 1842425028     PISSN: 0148639X     EISSN: None     Source Type: Journal    
DOI: 10.1002/mus.20020     Document Type: Article

References (53)

1. Andreu AL, Hanna MG, Reichmann H, Bruno C, Penn AS, Tanji K, Pallotti F, Iwata S, Bonilla E, Lach B, Morgan-Hughes J, DiMauro S. Exercise intolerance due to mutations in the cytochrome b gene of mitochondrial DNA. N Engl J Med 1999;341:1037-1044.
2. Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, Howell N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet 1999;23:147.
3. Arnold DL, Taylor DJ, Radda GK. Investigation of human mitochondrial myopathies by phosphorus magnetic resonance spectroscopy. Ann Neurol 1985;18:189-196.
4. Ashton T, Young IS, Peters JR, Jones E, Jackson SK, Davies B, Rowlands CC. Electron spin resonance spectroscopy, exercise, and oxidative stress: an ascorbic acid intervention study. J Appl Physiol 1999;87:2032-2036.
5. Barbiroli B, Frassineti C, Martinelli P, Iotti S, Lodi R, Cortelli P, Montagna P. Coenzyme Q10 improves mitochondrial respiration in patients with mitochondrial cytopathies. An in vivo study on brain and skeletal muscle by phosphorous magnetic resonance spectroscopy. Cell Mol Biol 1997;43:741-749.
6. Borchert A, Wilichowski E, Hanefeld F. Supplementation with creatine monohydrate in children with mitochondrial encephalomyopathies. Muscle Nerve 1999;22:1299-1300.
7. Brown MD, Starikovskaya E, Derbeneva O, Hosseini S, Allen JC, Mikhailovskaya IE, Sukernik RI, Wallace DC. The role of mtDNA background in disease expression: a new primary LHON mutation associated with Western Eurasian haplogroup J. Hum Genet 2002;110:130-138.
8. Carter SL, Rennie CD, Hamilton SJ, Tarnopolsky MA. Changes in skeletal muscle in males and females following endurance training. Can J Physiol Pharmacol 2001;79:386-392.
9. Chomyn A. Platelet-mediated transformation of human mitochondrial DNA-less cells. Methods Enzymol 1996;264:334-339.
10. Eppenberger-Eberhardt M, Riesinger I, Messerli M, Schwarb P, Muller M, Eppenberger HM, Wallimann T. Adult rat cardiomyocytes cultured in creatine-deficient medium display large mitochondria with paracrystalline inclusions, enriched for creatine kinase. J Cell Biol 1991;113:289-302.
11. Esposito LA, Melov S, Panov A, Cottrell BA, Wallace DC. Mitochondrial disease in mouse results in increased oxidative stress. Proc Natl Acad Sci USA 1999;96:4820-4825.
12. Greenhaff PL, Bodin K, Soderlund K, Hultman E. Effect of oral creatine supplementation on skeletal muscle phosphocreatine resynthesis. Am J Physiol 1994;266:E725-E730.
13. Ha HC, Woster PM, Yager JD, Casero RA Jr. The role of polyamine catabolism in polyamine analogue-induced programmed cell death. Proc Natl Acad Sci USA 1997;94:11557-11562.
14. Heddi A, Stepien G, Benke PJ, Wallace DC. Coordinate induction of energy gene expression in tissues of mitochondrial disease patients. J Biol Chem 1999;274:22968-22976.
15. Herrnstadt C, Elson JL, Fahy E, Preston G, Turnbull DM, Anderson C, Ghosh SS, Olefsky JM, Beal MF, Davis RE, Howell N. Reduced-median-network analysis of complete mitochondrial DNA coding-region sequences for the major African, Asian, and European haplogroups. Am J Hum Genet 2002;70:1152-1171.
16. Hultman E, Soderlund K, Timmons JA, Cederblad G, Greenhaff PL. Muscle creatine loading in men. J Appl Physiol 1996;81:232-237.
17. Johns DR. Seminars in medicine of the Beth Israel Hospital, Boston. Mitochondrial DNA and disease. N Engl J Med 1995; 333:638-644.
18. Khassaf M, Child RB, McArdle A, Brodie DA, Esanu C, Jackson MJ. Time course of responses of human skeletal muscle to oxidative stress induced by nondamaging exercise. J Appl Physiol 2001;90:1031-1035.
19. Klivenyi P, Ferrante RJ, Matthews RT, Bogdanov MB, Klein AM, Andreassen OA, Mueller G, Wermer M, Kaddurah-Daouk R, Beal MF. Neuroprotective effects of creatine in a transgenic animal model of amyotrophic lateral sclerosis. Nat Med 1999;5:347-350.
20. Klopstock T, Querner V, Schmidt F, Gekeler F, Walter M, Hartard M, Henning M, Gasser T, Pongratz D, Straube A, Dieterich M, Muller-Felber W. A placebo-controlled crossover trial of creatine in mitochondrial diseases. Neurology 2000; 55:1748-1751.
21. Lawler JM, Barnes WS, Wn G, Song W, Demaree S. Direct antioxidant properties of creatine. Biochem Biophys Res Commun 2002;290:47-52.
22. Mahoney DJ, Parise G, Tarnopolsky MA. Nutritional and exercise-based therapies in the treatment of mitochondrial disease. Curr Opin Clin Nutr Metab Care 2002;5:619-629.
23. Matthews PM, Allaire C, Shoubridge EA, Karpati G, Carpenter S, Arnold DL. In vivo muscle magnetic resonance spectroscopy in the clinical investigation of mitochondrial disease. Neurology 1991;41:114-120.
24. McKenzie S, Phillips SM, Carter SL, Lowther S, Gibala MJ, Tarnopolsky MA. Endurance exercise training attenuates leucine oxidation and BCOAD activation during exercise in humans. Am J Physiol Endocrinol Metab 2000;278:E580-E587.
25. Miller SW, Trimmer PA, Parker WD Jr, Davis RE. Creation and characterization of mitochondrial DNA-depleted cell lines with "neuronal-like" properties. J Neurochem 1996;67: 1897-1907.
26. Mirabella M, Di Giovanni S, Silvestri G, Tonali P, Servidei S. Apoptosis in mitochondrial encephalomyopathies with mitochondrial DNA mutations: a potential pathogenic mechanism. Brain 2000;123:93-104.
27. Mitsui T, Kawai H, Nagasawa M, Kunishige M, Akaike M, Kimura Y, Saito S. Oxidative damage to skeletal muscle DNA from patients with mitochondrial encephalomyopathies. J Neurol Sci 1996;139:111-116.
28. O'Gorman E, Beutner G, Wallimann T, Brdiczka D. Differential effects of creatine depletion on the regulation of enzyme activities and on creatine-stimulated mitochondrial respiration in skeletal muscle, heart, and brain. Biochim Biophys Acta 1996;1276:161-170.
29. O'Gorman E, Fuchs KH, Tittmann P, Gross H, Wallimann T Crystalline mitochondrial inclusion bodies isolated from creatine depleted rat soleus muscle. J Cell Sci 1997;110:1403-1411.
30. O'Gorman E, Piendl T, Muller M, Brdiczka D, Wallimann T. Mitochondrial intermembrane inclusion bodies: the common denominator between human mitochondrial myopathies and creatine depletion, due to impairment of cellular energetics. Mol Cell Biochem 1997;174:283-289.
31. Ohkoshi N, Mizusawa H, Shiraiwa N, Shoji S, Harada K, Yoshizawa K. Superoxide dismutases of muscle in mitochondrial encephalomyopathies. Muscle Nerve 1995;18:1265-1271.
32. Passaquin AC, Renard M, Kay L, Challet C, Mokhtarian A, Wallimann T, Ruegg UT. Creatine supplementation reduces skeletal muscle degeneration and enhances mitochondrial function in mdx mice. Neuromuscul Disord 2002;12:174-182.
33. Petroski RE, Geller HM. Selective labeling of embryonic neurons cultured on astrocyte monolayers with 5(6)-carboxyfluorescein diacetate (CFDA). J Neurosci Methods 1994;52:23-32.
34. Pitkanen S, Robinson BH. Mitochondrial complex 1 deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J Clin Invest 1996;98: 345-351.
35. Rowbottom DG, Keast D, Green S, Kakulas B, Morton AR. The case history of an elite ultra-endurance cyclist who developed chronic fatigue syndrome. Med Sci Sports Exerc 1998; 30:1345-1348.
36. Rusanen H, Majamaa K, Hassinen IE. Increased activities of antioxidant enzymes and decreased ATP concentration in cultured myoblasts with the 3243A→G mutation in mitochondrial DNA. Biochim Biophys Acta 2000;1500:10-16.
37. Santos-Silva A, Rebelo MI, Castro EM, Belo L, Guerra A, Rego C, Quintanilha A. Leukocyte activation, erythrocyte damage, lipid profile and oxidative stress imposed by high competition physical exercise in adolescents. Clin Chim Acta 2001;306: 119-126.
38. Simon DK, Johns DR. Mitochondrial disorders: clinical and genetic features. Annu Rev Med 1999;50:111-127.
39. Simon DK, Pulst SM, Sutton JP, Browne SE, Beal MF, Johns DR. Familial multisystem degeneration with parkinsonism associated with the 11778 mitochondrial DNA mutation. Neurology 1999;53:1787-1793.
40. Smeitink J, Stadhouders A, Sengers R, Ruitenbeek W, Wevers R, ter Laak H, Trijbels F. Mitochondrial creatine kinase containing crystals, creatine content and mitochondrial creatine kinase activity in chronic progressive external ophthalmoplegia. Neuromuscul Disord 1992;2:35-40.
41. Stachowiak O, Dolder M, Wallimann T, Richter C. Mitochondrial creatine kinase is a prime target of peroxynitrite-induced modification and inactivation. J Biol Chem 1998;273: 16694-16699.
42. Stachowiak O, Schlattner U, Dolder M, Wallimann T. Oligomeric state and membrane binding behaviour of creatine kinase isoenzymes: implications for cellular function and mitochondrial structure. Mol Cell Biochem 1998;184:141-151.
43. Sullivan PG, Geiger JD, Mattson MP, Scheff SW. Dietary supplement creatine protects against traumatic brain injury. Ann Neurol 2000;48:723-729.
44. Taivassalo T, De Stefano N, Argov Z, Matthews PM, Chen J, Genge A, Karpati G, Arnold DL. Effects of aerobic training in patients with mitochondrial myopathies. Neurology 1998;50: 1055-1060.
45. Taivassalo T, Fu K, Johns T, Arnold D, Karpati G, Shoubridge EA. Gene shifting: a novel therapy for mitochondrial myopathy. Hum Mol Genet 1999;8:1047-1052.
46. Tarnopolsky MA, Maguire J, Myint T, Applegarth D, Robinson BH. Clinical, physiological, and histological features in a kindred with the T3271C MELAS mutation. Muscle Nerve 1998;21:25-33.
47. Tarnopolsky MA, Parise G. Direct measurement of high-energy phosphate compounds in patients with neuromuscular disease. Muscle Nerve 1999;22:1228-1233.
48. Tarnopolsky MA, Parshad A, Walzel B, Schlattner U, Wallimann T. Creatine transporter and mitochondrial creatine kinase protein content in myopathies. Muscle Nerve 2001;24: 682-688.
49. Tarnopolsky MA, Roy BD, MacDonald JR. A randomized, controlled trial of creatine monohydrate in patients with mitochondrial cytopathies. Muscle Nerve 1997;20:1502-1509.
50. Taube R, Eichner ER. Evaluation of decreased performance in a world class cyclist-Greg Lemond. Med Sci Sports Exerc 1995;27:xxi.
51. Taylor DJ, Kemp GJ, Radda GK. Bioenergetics of skeletal muscle in mitochondrial myopathy. J Neurol Sci 1994;127: 198-206.
52. Vissing J, Gansted U, Quistorff B. Exercise intolerance in mitochondrial myopathy is not related to lactic acidosis. Ann Neurol 2001;49:672-676.
53. Vives-Bauza C, Gamez J, Roig M, Briones P, Cervera C, Solano A, Montoya J, Andreu AL. Exercise intolerance resulting from a muscle-restricted mutation in the mitochondrial tRNA(Leu (CUN)) gene. Ann Med 2001;33:493-496.