Effect of thyroid hormone on mitochondrial properties and oxidative stress in cells from patients with mtDNA defects

American Journal of Physiology - Cell Physiology

Volumn 296, Issue 2, 2009, Pages

  Menzies, Keir J ^b,c   Robinson, Brian H ^d   Hood, David A ^a,b  

^a YORK UNIVERSITY   (Canada)

^b Department of Biology ^*  (Canada)

^c YORK UNIVERSITY   (Canada)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

3,3 ,5 triiodothyronine; Cytoplasmic calcium; Mitochondrial biogenesis; Mitochondrial disease; Mitochondrial dna; Reactive oxygen species

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; CYTOCHROME C OXIDASE; LIOTHYRONINE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; UNCOUPLING PROTEIN 2;

ARTICLE; BIOGENESIS; CALCIUM CELL LEVEL; CELL STRESS; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; FIBROBLAST CULTURE; GENE MUTATION; HORMONE ACTION; HUMAN; HUMAN CELL; HYPERTROPHIC CARDIOMYOPATHY; LEIGH DISEASE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CALCIUM; CARDIOMYOPATHY, HYPERTROPHIC; CASE-CONTROL STUDIES; CELL LINE, TUMOR; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX IV; FIBROBLASTS; HEAT-SHOCK PROTEINS; HUMANS; ION CHANNELS; LEIGH DISEASE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MUTATION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, TRANSFER, LEU; SUPEROXIDE DISMUTASE; THYROID HORMONE RECEPTORS ALPHA; THYROID HORMONE RECEPTORS BETA; TRANSCRIPTION FACTORS; TRIIODOTHYRONINE;

EID: 60849098436     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00415.2007     Document Type: Article

References (52)

1. 2+ accumulation in rabbit hearts exposed to hypoxia and acidification. Am J Physiol Cell Physiol 284: C1123-C1132, 2003.
2. Bakker A, Barthelemy C, Frachon P, Chateau D, Sternberg D, Mazat JP, Lombes A. Functional mitochondrial heterogeneity in heteroplasmic cells carrying the mitochondrial DNA mutation associated with the MELAS syndrome (mitochondrial encephalopathy, lactic acidosis, and strokelike episodes). Pediatr Res 48: 143-150, 2000.
3. Beyer RE. An analysis of the role of coenzyme Q in free radical generation and as an antioxidant. Biochem Cell Biol 70: 390-403, 1992.
4. Buttgereit F, Brand MD. A hierarchy of ATP-consuming processes in mammalian cells. Biochem J 312: 163-167, 1995.
5. Carrozzo R, Rizza T, Lucioli S, Pierini R, Bertini E, Santorelli FM. A mitochondrial ATPase 6 mutation is associated with Leigh syndrome in a family and affects proton flow and adenosine triphosphate output when modeled in Escherichia coli. Acta Paediatr Suppl 93: 65-67, 2004.
6. Chinnery PF, Johnson MA, Wardell TM, Singh-Kler R, Hayes C, Brown DT, Taylor RW, Bindoff LA, Turnbull DM. The epidemiology of pathogenic mitochondrial DNA mutations. Ann Neurol 48: 188-193, 2000.
7. Chol M, Lebon S, Benit P, Chretien D, de Lonlay P, Goldenberg A, Odent S, Hertz-Pannier L, Vincent-Delorme C, Cormier-Daire V, Rustin P, Rotig A, Munnich A. The mitochondrial DNA G13513A MELAS mutation in the NADH dehydrogenase 5 gene is a frequent cause of Leigh-like syndrome with isolated complex I deficiency. J Med Genet 40: 188-191, 2003.
8. Chung AB, Stepien G, Haraguchi Y, Li K, Wallace DC. Transcriptional control of nuclear genes for the mitochondrial muscle ADP/ATP translo-cator and the ATP synthase beta subunit. Multiple factors interact with the OXBOX/REBOX promoter sequences. J Biol Chem 267: 21154-21161,1992.
9. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 341: 233-249, 1999.
10. Esposito LA, Melov S, Panov A, Cottrell BA, Wallace DC. Mitochon-drial disease in mouse results in increased oxidative stress. Proc Natl Acad Sci USA 96: 4820-4825, 1999.
11. Freyssenet D, Irrcher I, Connor MK, Di Carlo M, Hood DA. Calcium-regulated changes in mitochondrial phenotype in skeletal muscle cells. Am J Physiol Cell Physiol 286: C1053-C1061, 2004.
12. Galkin A, Brandt U. Superoxide radical formation by pure complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica. J Biol Chem 280: 30129-30135, 2005.
13. Garcia JJ, Ogilvie I, Robinson BH, Capaldi RA. Structure, functioning, and assembly of the ATP synthase in cells from patients with the T8993G mitochondrial DNA mutation. Comparison with the enzyme in Rho(0) cells completely lacking mtDNA. J Biol Chem 275: 11075-11081, 2000.
14. Garstka HL, Facke M, Escribano JR, Wiesner RJ. Stoichiometry of mitochondrial transcripts and regulation of gene expression by mitochon-drial transcription factor A. Biochem Biophys Res Commun 200: 619-626,1994.
15. Goto Y, Nonaka I, Horai S. A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopa-thies. Nature 348: 651-653, 1990.
16. Irrcher I, Adhihetty PJ, Sheehan T, Joseph AM, Hood DA. PPAR-γcoactivator-1α expression during thyroid hormone- and contractile activity-induced mitochondrial adaptations. Am J Physiol Cell Physiol 284:C1669-C1677, 2003.
17. Joseph AM, Rungi AA, Robinson BH, Hood DA. Compensatory responses of protein import and transcription factor expression in mitochon-drial DNA defects. Am J Physiol Cell Physiol 286: C867-C875, 2004.
18. Kadenbach B, Arnold S, Lee I, Huttemann M. The possible role of cytochrome c oxidase in stress-induced apoptosis and degenerative diseases. Biochim Biophys Acta 1655: 400-408, 2004.
19. Keij JF, Bell-Prince C, Steinkamp JA. Staining of mitochondrial membranes with 10-nonyl acridine orange, mitofluor green, and mitotracker green is affected by mitochondrial membrane potential altering drugs.Cytometry 39: 203-210, 2000.
20. Kim KH, Rodriguez AM, Carrico PM, Melendez JA. Potential mechanisms for the inhibition of tumor cell growth by manganese superoxide dismutase. Antioxid Redox Signal 3: 361-373, 2001.
21. Kramer KA, Oglesbee D, Hartman SJ, Huey J, Anderson B, Magera MJ, Matern D, Rinaldo P, Robinson BH, Cameron JM, Hahn SH.Automated spectrophotometric analysis of mitochondrial respiratory chain complex enzyme activities in cultured skin fibroblasts. Clin Chem 51:2110-2116, 2005.
22. Krieger DA, Tate CA, McMillin-Wood J, Booth FW. Populations of rat skeletal muscle mitochondria after exercise and immobilization. J Appl Physiol 48: 23-28, 1980.
23. Kroemer G, Dallaporta B, Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 60: 619 -642,1998.
24. Larsen NB, Rasmussen M, Rasmussen LJ. Nuclear and mitochondrial DNA repair: similar pathways? Mitochondrion 5: 89-108, 2005.
25. Lenaz G, Baracca A, Carelli V, D"Aurelio M, Sgarbi G, Solaini G. Bioenergetics of mitochondrial diseases associated with mtDNA mutations. Biochim Biophys Acta 1658: 89-94, 2004.
26. Leo S, Bianchi K, Brini M, Rizzuto R. Mitochondrial calcium signalling in cell death. FEBS J 272: 4013-4022, 2005.
27. Li N, Ragheb K, Lawler G, Sturgis J, Rajwa B, Melendez JA, Robinson JP. Mitochondrial complex I inhibitor rotenone induces apop-tosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem 278: 8516-8525, 2003.
28. Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang CY, Mootha VK, Jager S, Vianna CR, Reznick RM, Cui L, Manieri M, Donovan MX, Wu Z, Cooper MP, Fan MC, Rohas LM, Zavacki AM, Cinti S, Shulman GI, Lowell BB, Krainc D, Spiegelman BM. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119: 121-135, 2004.
29. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, Haeffner A, Hirsch F, Geuskens M, Kroemer G. Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 184: 1155-1160, 1996.
30. Moudy AM, Handran SD, Goldberg MP, Ruffin N, Karl I, Kranz-Eble P, DeVivo DC, Rothman SM. Abnormal calcium homeostasis and mitochondrial polarization in a human encephalomyopathy. Proc Natl Acad Sci USA 92: 729-733, 1995.
31. Mracek T, Pecina P, Vojtiskova A, Kalous M, Sebesta O, Houstek J. Two components in pathogenic mechanism of mitochondrial ATPase deficiency: energy deprivation and ROS production. Exp Gerontol 41:683-687, 2006.
32. Nakai D, Shimizu T, Nojiri H, Uchiyama S, Koike H, Takahashi M,Hirokawa K, Shirasawa T. Coq7/clk-1 regulates mitochondrial respiration and the generation of reactive oxygen species via coenzyme Q. Aging Cell 3: 273-281, 2004.
33. Pillar TM, Seitz HJ. Thyroid hormone and gene expression in the regulation of mitochondrial respiratory function. Eur J Endocrinol 136:231-239, 1997.
34. Portman MA, Xiao Y, Qian K, Tucker RL, Parish SM, Ning XH. Thyroid hormone coordinates respiratory control maturation and adenine nucleotide translocator expression in heart in vivo. Circulation 102:1323-1329, 2000.
35. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839, 1998.
36. Pulkes T, Eunson L, Patterson V, Siddiqui A, Wood NW, Nelson IP, Morgan-Hughes JA, Hanna MG. The mitochondrial DNA G13513A transition in ND5 is associated with a LHON/MELAS overlap syndrome and may be a frequent cause of MELAS. Ann Neurol 46: 916-919, 1999.
37. Reers M, Smith TW, Chen LB. J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30: 4480-4486, 1991.
38. Richter C, Park JW, Ames BN. Normal oxidative damage to mitochon-drial and nuclear DNA is extensive. Proc Natl Acad Sci USA 85: 6465-6467, 1988.
39. Rossmanith W, Karwan RM. Impairment of tRNA processing by point mutations in mitochondrial tRNA(Leu)(UUR) associated with mitochon-drial diseases. FEBS Lett 433: 269-274, 1998.
40. Sauer H, Wartenberg M, Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 11: 173-186, 2001.
41. Sgarbi G, Baracca A, Lenaz G, Valentino LM, Carelli V, Solaini G. Inefficient coupling between proton transport and ATP synthesis may be the pathogenic mechanism for NARP/Leigh syndromes resulting from the T8993G mutation in mtDNA. Biochem J 395: 493-500, 2006.
42. Sheehan TE, Kumar PA, Hood DA. Tissue-specific regulation of cyto-chrome c oxidase subunit expression by thyroid hormone. Am J Physiol Endocrinol Metab 286: E968-E974, 2004.
43. Sudo A, Honzawa S, Nonaka I, Goto Y. Leigh syndrome caused by mitochondrial DNA G13513A mutation: frequency and clinical features in Japan. J Hum Genet 49: 92-96, 2004.
44. Thyagarajan D, Shanske S, Vazquez-Memije M, De Vivo D, DiMauro S. A novel mitochondrial ATPase 6 point mutation in familial bilateral striatal necrosis. Ann Neurol 38: 468-472, 1995.
45. van Erven PM, Cillessen JP, Eekhoff EM, Gabreels FJ, Doesburg WH, Lemmens WA, Slooff JL, Renier WO, Ruitenbeek W. Leigh syndrome, a mitochondrial encephalo(myo)pathy. A review of the literature. Clin Neurol Neurosurg 89: 217-230, 1987.
46. Virbasius JV, Scarpulla RC. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci USA 91: 1309-1313, 1994.
47. 2+ handling in human complex I deficiency. J Biol Chem 279: 40328-40336, 2004.
48. Weitzel JM, Iwen KA, Seitz HJ. Regulation of mitochondrial biogenesis by thyroid hormone. Exp Physiol 88: 121-128, 2003.
49. Weitzel JM, Radtke C, Seitz HJ. Two thyroid hormone-mediated gene expression patterns in vivo identified by cDNA expression arrays in rat. Nucleic Acids Res 29: 5148 -5155, 2001.
50. Wrutniak-Cabello C, Casas F, Cabello G. Thyroid hormone action in mitochondria. J Mol Endocrinol 26: 67-77, 2001.
51. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G. Mitochondrial control of nuclear apoptosis. J Exp Med 183: 1533-1544, 1996.
52. Zeviani M, Mariotti C, Antozzi C, Fratta GM, Rustin P, Prelle A. OXPHOS defects and mitochondrial DNA mutations in cardiomyopathy. Muscle Nerve 3: S170-S174, 1995.