OXPHOS gene expression and control in mitochondrial disorders

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1792, Issue 12, 2009, Pages 1113-1121

  Reinecke, Fimmie ^a   Smeitink, Jan A M ^b   van der Westhuizen, Francois H ^a  

^a NORTH WEST UNIVERSITY   (South Africa)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Gene expression; Mitochondria; Mitochondria nucleus communication; Mitochondrial disorders; OXPHOS; Signalling

Indexed keywords

CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; MYOCYTE ENHANCER FACTOR 2; OXOGLUTARATE DEHYDROGENASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN BNIP3; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE; UBIQUINOL CYTOCHROME C REDUCTASE;

CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; COMPLEX I DEFICIENCY; COMPLEX II DEFICIENCY; COMPLEX III DEFICIENCY; CYTOCHROME C OXIDASE DEFICIENCY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DNA REPAIR; DNA TRANSCRIPTION; GENE EXPRESSION REGULATION; GENE MUTATION; HUMAN; KEARNS SAYRE SYNDROME; LEBER HEREDITARY OPTIC NEUROPATHY; MELAS SYNDROME; MERRF SYNDROME; MITOCHONDRIAL DNA DEPLETION SYNDROME; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL GENETICS; MITOCHONDRIAL MYOPATHY; NARP SYNDROME; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; REVIEW;

GENE EXPRESSION; GENES, MITOCHONDRIAL; HUMANS; MITOCHONDRIAL DISEASES; OXIDATIVE PHOSPHORYLATION;

EID: 71849092835     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2009.04.003     Document Type: Review

References (80)

1. Anderson S., Bankier A.T., Barrell B.G., de Bruijn M.H., Coulson A.R., Drouin J., Eperon I.C., Nierlich D.P., Roe B.A., Sanger F., Schreier P.H., Smith A.J., Staden R., and Young I.G. Sequence and organization of the human mitochondrial genome. Nature 290 (1981) 457-465
2. Cannino G., Di Liegro C.M., and Rinaldi A.M. Nuclear-mitochondrial interaction. Mitochondrion 7 (2007) 359-366
3. Spinazzola A., and Zeviani M. Disorders of nuclear-mitochondrial intergenomic signaling. Gene 354 (2005) 162-168
4. Smeitink J., van den Heuvel L., and DiMauro S. The genetics and pathology of oxidative phosphorylation. Nat. Rev., Genet. 2 (2001) 342-352
5. Turrens J.F., and Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem. J. 191 (1980) 421-427
6. 1 complex. Biochem. J. 283 (2008) 21649-21654
7. Smeitink J.A., Zeviani M., Turnbull D.M., and Jacobs H.T. Mitochondrial medicine: a metabolic perspective on the pathology of oxidative phosphorylation disorders. Cell. Metab. 3 (2006) 9-13
8. Starkov A.A., Fiskum G., Chinopoulos C., Lorenzo B.J., Browne S.E., Patel M.S., and Beal M.F. Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J. Neurosci. 24 (2004) 7779-7788
9. Guzy R.D., Sharma B., Bell E., Chandel N.S., and Schumacker P.T. Loss of the SdhB, but not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol. Cell. Biol. 28 (2008) 718-731
10. Koopman W.J., Visch H.-J., Verkaart S., and Willems P.H. Cell biological consequences of OXPHOS disorders. In: Smeitink J., Sengers R.C.A., and Trijbels F.J.M. (Eds). Oxidative Phosphorylation in Health and Disease (2004), Landes Bioscience, Georgetown, Texas 130-166
11. Reinecke F., Levanets O., Olivier Y., Louw R., Semete B., Grobler A., Hidalgo J., Smeitink J., Olckers A., and van der Westhuizen F.H. Metallothionein isoform 2A expression is inducible and protects against ROS-mediated cell death in rotenone-treated HeLa cells. Biochem. J. 395 (2006) 405-415
12. Dröge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82 (2002) 47-95
13. Jones D.P. Radical-free biology of oxidative stress. Am. J. Physiol., Cell Physiol. 295 (2008) C849-C868
14. Zhang D.X., and Gutterman D.D. Mitochondrial reactive oxygen species-mediated signaling in endothelial cells. Am. J. Physiol., Heart Circ. Physiol. 292 (2007) H2023-H2031
15. Genestra M. Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Cell. Signal. 19 (2007) 1807-1819
16. Echtay K.S., Roussel D., St-Pierre J., Jekabsons M.B., Cadenas S., Stuart J.A., Harper J.A., Roebuck S.J., Morrison A., Pickering S., Clapham J.C., and Brand M.D. Superoxide activates mitochondrial uncoupling proteins. Nature 415 (2002) 96-99
17. Vives-Bauza C., Gonzalo R., Manfredi G., Garcia-Arumi E., and Andreu A.L. Enhanced ROS production and antioxidant defenses in cybrids harbouring mutations in mtDNA. Neurosci. Lett. 391 (2006) 136-141
18. Verkaart S., Koopman W.J., Cheek J., van Emst-de Vries S.E., van den Heuvel L.P., Smeitink J.A., and Willems P.H. Mitochondrial and cytosolic thiol redox state are not detectably altered in isolated human NADH:ubiquinone oxidoreductase deficiency. Biochim. Biophys. Acta 1772 (2007) 1041-1051
19. Koopman W.J., Verkaart S., Visch H.J., van Emst-de Vries S., Nijtmans L.G., Smeitink J.A.M., and Willems P.H.G.M. Human NADH:ubiquinone oxidoreductase deficiency: radical changes in mitochondrial morphology. Am. J. Physiol., Cell Physiol. 293 (2007) C22-C29
20. Iuso A., Scacco S., Piccoli C., Bellomo F., Petruzella V., Trentadue R., Minuto M., Ripoli M., Capitanio N., Zeviani M., and Papa S. Dysfunctions of cellular oxidative metabolism in patients with mutations in the NDUFS1 and NDUFS4 genes of complex I. J. Biol. Chem 281 (2006) 10374-10380
21. Schauen M., Spitkovsky D., Schubert J., Fischer J.H., Hayashi J., and Wiesner R.J. Respiratory chain deficiency slows down cell-cycle progression via reduced ROS generation and is associated with a reduction of p21CIP1/WAF1. J. Cell. Physiol. 209 (2006) 103-112
22. Verkaart S., Koopman W.J., van Emst-de Vries S.E., Nijtmans L.G., van den Heuvel L.P., Smeitink J.A., and Willems P.H. Superoxide production is inversely related to complex I activity in inherited complex I deficiency. Biochim. Biophys. Acta 1772 (2007) 373-381
23. Dassa E.P., Paupe V., Gonçalves S., and Rustin P. The mtDNA NARP mutation activates the actin-Nrf2 signaling of antioxidant defenses. Biochem. Biophys. Res. Commun. 368 (2008) 620-624
24. Quinzii C.M., Lopez L.C., Von-Moltke J., Naini A., Krishna S., Schuelke M., Salviati L., Navas P., DiMauro S., and Hirano M. Respiratory chain dysfunction and oxidative stress correlate with severity of primary CoQ10 deficiency. FASEB J. 22 (2008) 1874-1885
25. Munnich A., and Rustin P. Clinical spectrum and diagnosis of mitochondrial disorders. Am. J. Med. Genet. 106 (2001) 4-17
26. Ying W. NADNADH and NADPNADPH in cellular functions and cell death regulation and biological consequences. Antioxid. Redox Signal. 10 (2008) 179-206
27. Ermak G., and Davies K.J. Calcium and oxidative stress: from cell signaling to cell death. Mol. Immunol. 38 (2002) 713-721
28. Jacobson J., and Duchen M.R. 'What nourishes me, destroys me': towards a new mitochondrial biology. Cell Death Differ. 8 (2001) 963-966
29. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., and Sheu S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol., Cell Physiol. 287 (2004) C817-C833
30. + homeostasis in human NADH:ubiquinone oxidoreductase deficiency. Cell Calcium 44 (2008) 123-133
31. Shutt T.E., and Shadel G.S. Expanding the mitochondrial interactome. Genome Biol. 8 (2007) 203
32. Heddi A., Lestienne P., Wallace D.C., and Stepien G. Mitochondrial DNA expression in mitochondrial myopathies and coordinated expression of nuclear genes involved in ATP production. J. Biol. Chem. 268 (1993) 12156-12163
33. Heddi A., Stepien G., Benke P.J., and Wallace D.C. Coordinate induction of energy gene expression in tissues of mitochondrial disease patients. J. Biol. Chem. 274 (1999) 22968-22976
34. Collombet J.M., Faure-Vigny H., Mandon G., Dumoulin R., Boissier S., Bernard A., Mousson B., and Stepien G. Expression of oxidative phosphorylation genes in muscle cell cultures from patients with mitochondrial myopathies. Mol. Cell. Biochem. 168 (1997) 73-85
35. Bonod-Bidaud C., Giraud S., Mandon G., Mousson B., and Stepien G. Quantification of OXPHOS gene transcripts during muscle cell differentiation in patients with mitochondrial myopathies. Exp. Cell Res. 246 (1999) 91-97
36. Marusich M.F., Robinson B.H., Taanman J.W., Kim S.J., Schillace R., Smith J.L., and Capaldi R.A. Expression of mtDNA and nDNA encoded respiratory chain proteins in chemically and genetically-derived Rho0 human fibroblasts: a comparison of subunit proteins in normal fibroblasts treated with ethidium bromide and fibroblasts from a patient with mtDNA depletion syndrome. Biochim. Biophys. Acta 1362 (1997) 145-159
37. van der Westhuizen F.H., van den Heuvel L.P., Smeets R., Veltman J.A., Pfundt R., van Kessel A.G., Ursing B.M., and Smeitink J.A. Human mitochondrial complex I deficiency: investigating transcriptional responses by microarray. Neuropediatrics 34 (2003) 14-22
38. Crimi M., Bordoni A., Menozzi G., Riva L., Fortunato F., Galbiati S., Del Bo R., Pozzoli U., Bresolin N., and Comi G.P. Skeletal muscle gene expression profiling in mitochondrial disorders. FASEB J. 19 (2005) 866-868
39. Crimi M., O'Hearn S.F., Wallace D.C., and Comi G.P. Molecular research technologies in mitochondrial diseases: the microarray approach. IUBMB Life 57 (2005) 811-818
40. Behan A., Doyle S., and Farrell M. Adaptive responses to mitochondrial dysfunction in the ρ° Namalwa cell. Mitochondrion 5 (2005) 173-193
41. Cízková A., Stránecký V., Ivánek R., Hartmannová H., Nosková L., Piherová L., Tesarová M., Hansíková H., Honzík T., Zeman J., Divina P., Potocká A., Paul J., Sperl W., Mayr J.A., Seneca S., Houstěk J., and Kmoch S. Development of a human mitochondrial oligonucleotide microarray (h-MitoArray) and gene expression analysis of fibroblast cell lines from 13 patients with isolated F1Fo ATP synthase deficiency. BMC Genomics 9 (2008) 38
42. Danielson S.R., Carelli V., Tan G., Martinuzzi A., Schapira A.H.V., Savontaus M., and Cortopassi G.A. Isolation of transcriptomal changes attributable to LHON mutations and the cybridization process. Brain 128 (2005) 1026-1037
43. Chevallet M., Lescuyer P., Diemer H., van Dorsselaer A., Leize-Wagner E., and Rabilloud T. Alterations of the mitochondrial proteome caused by the absence of mitochondrial DNA: a proteomic view. Electrophoresis 27 (2006) 1574-1583
44. Duborjal H., Beugnot R., De Camaret B.M., and Issartel J. Large functional range of steady-state levels of nuclear and mitochondrial transcripts coding for the subunits of the human mitochondrial OXPHOS system. Genome Res. 12 (2002) 1901-1909
45. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J.A., and Robinson J.P. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278 (2003) 8516-8525
46. Biswas G., Guha M., and Avadhani N.G. Mitochondria-to-nucleus stress signaling in mammalian cells: nature of nuclear gene targets, transcription regulation, and induced resistance to apoptosis. Gene 354 (2005) 13-139
47. 2+ signaling. Physiology 23 (2008) 84-94
48. Newsholme P., Haber E.P., and Hirabara S.M. Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity. J. Physiol. 583 (2007) 9-24
49. Ohtsuji M., Katsuoka F., Kobayashi A., Aburatani H., Hayes J.D., and Yamamoto M. Nrf1 and Nrf2 play distinct roles in activation of antioxidant response element-dependent genes. J. Biol. Chem. 283 (2008) 33554-33562
50. Miranda S., Foncea R., Guerrero J., and Leighton F. Oxidative stress and upregulation of mitochondrial biogenesis genes in mitochondrial DNA-depleted HeLa cells. Biochem. Biophys. Res. Commun. 258 (1999) 44-49
51. Suliman H.B., Carraway M.S., Welty-Wolf K.E., Whorton A.R., and Piantados C.A. Lipopolysaccharide stimulates mitochondrial biogenesis via activation of nuclear respiratory factor-1. J. Biol. Chem. 278 (2003) 41510-41518
52. Bergeron R., Ren J.M., Cadman K.S., Moore I.K., Perret P., Pypaert M., Young L.H., Semenkovich C.F., and Shulman G.I. Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am. J. Physiol., Endocrinol. Metab. 281 (2001) E1340-E1346
53. van Waveren C., and Moraes C.T. Transcriptional co-expression and co-regulation of genes coding for components of the oxidative phosphorylation system. BMC Genomics 9 (2008) 18
54. Scarpulla R.C. Nuclear control of respiratory gene expression in mammalian cells. J. Cell. Biochem. 97 (2006) 673-683
55. Kelly D.P., and Scarpulla R.C. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18 (2004) 357-368
56. Lee H.C., and Wei Y.H. Mitochondrial biogenesis and mitochondrial DNA maintenance. Int. J. Biochem. Cell Biol. 37 (2005) 822-834
57. Ramachandran B., Yu G., and Guiick T. Nuclear respiratory factor 1 controls myocyte enhancer factor 2A transcription to provide a mechanism for coordinate expression of respiratory chain subunits. J. Biol. Chem. 283 (2008) 11935-11946
58. Gleyzer N., Vercauteren K., and Scarpulla R.C. Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC4 family coactivators. Mol. Cell. Biol. 25 (2005) 1354-1366
59. Shadel G.S. Expression and maintenance of mitochondrial DNA: new insights into human disease pathology. Am. J. Pathol. 172 (2008) 1445-1456
60. Asin-Cayuela J., and Gustafsson C.M. Mitochondrial transcription and its regulation in mammalian cells. Trends Biochem. Sci. 32 (2007) 111-117
61. Falkenberg M., Larsson N.G., and Gustafsson C.M. DNA replication and transcription in mammalian mitochondria. Annu. Rev. Biochem. 76 (2007) 679-699
62. Williams R.S. Mitochondrial gene expression in mammalian striated muscle: evidence that variation in gene dosage is the major regulatory event. J. Biol. Chem. 261 (1986) 12390-12394
63. Kaufmann P., Koga Y., Shanske S., Hirano M., DiMauro S., King M.P., and Schon E.A. Mitochondrial DNA and RNA processing in MELAS. Ann. Neurol. 40 (1996) 172-180
64. Seidel-Rogol B.L., and Shadel G.S. Modulation of mitochondrial transcription in response to mtDNA depletion and repletion in HeLa cells. Nucleic Acids Res. 30 (2002) 1929-1934
65. Schultz R.A., Swoap S.J., McDaniel L.D., Zhang B., Koon E.C., Garry D.J., Li K., and Williams R.S. Differential expression of mitochondrial DNA replication factors in mammalian tissues. J. Biol. Chem. 273 (1998) 3447-3451
66. Davis A.F., Ropp P.A., Clayton D.A., and Copeland W.C. Mitochondrial DNA polymerase γ is expressed and translated in the absence of mitochondrial DNA maintenance and replication. Nucleic Acids Res. 24 (1996) 2753-2759
67. Tyynismaa H., Sembongi H., Bokori-Brown M., Granycome C., Ashley N., Poulton J., Jalanko A., Spelbrink J.N., Holt I.J., and Suomalainen A. Twinkle helicase is essential for mtDNA maintenance and regulates mtDNA copy number. Hum. Mol. Genet. 13 (2004) 3219-3227
68. Cotney J., Wang Z., and Shadel G.S. Relative abundance of the human mitochondrial transcription system and distinct roles for h-mtTFB1 and h-mtTFB2 in mitochondrial biogenesis and gene expression. Nucleic Acids Res. 35 (2007) 4042-4054
69. Virbasius J.V., and Scarpulla R.C. 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. U. S. A. 91 (1994) 1309-1313
70. Singal R., and Ginder G.D. DNA methylation. Blood 93 (1999) 4059-4070
71. Matsushima Y., Adan C., Garesse R., and Kaguni L.S. Drosophila mitochondrial transcription factor B1 modulates mitochondrial translation but not transcription or DNA copy number in Schneider cells. J. Biol. Chem. 280 (2005) 16815-16820
72. Yakes F.M., and 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. U. S. A. 94 (1997) 514-519
73. Mambo E., Gao X., Cohen Y., Guo Z., Talalay P., and Sidransky D. Electrophile and oxidant damage of mitochondrial DNA leading to rapid evolution of homoplasmic mutations. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 1838-1843
74. Fisher R.P., and Clayton D.A. Purification and characterization of human mitochondrial transcription factor 1. Mol. Cell. Biol. 8 (1988) 3496-3509
75. Takamatsu C., Umeda S., Ohsato T., Ohno T., Abe Y., Fukuoh A., Shinagawa H., Hamasaki N., and Kang D. Regulation of mitochondrial D-loops by transcription factor A and single-stranded DNA-binding protein. EMBO Rep. 3 (2002) 451-456
76. Mandavilli B.S., Santos J.H., and Van Houten B. Mitochondrial DNA repair and aging. Mutat. Res. 509 (2002) 127-151
77. Grishko V., Solomon M., Wilson G.L., LeDoux S.P., and Gillespie M.N. Oxygen radical-induced mitochondrial DNA damage and repair in pulmonary vascular endothelial cell phenotypes. Am. J. Physiol., Lung. Cell Mol. Physiol. 280 (2001) 1300-1308
78. Bogenhagen D.F. Repair of mtDNA in vertebrates. Am. J. Hum. Genet. 64 (1999) 1276-1281
79. Croteau D.L., and Bohr V.A. Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells. J. Biol. Chem. 272 (1997) 25409-25412
80. Bohr V.A. Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radic. Biol. Med. 32 (2002) 804-812