Redox signalling and mitochondrial stress responses; lessons from inborn errors of metabolism

Journal of Inherited Metabolic Disease

Volumn 38, Issue 4, 2015, Pages 703-719

  Olsen, Rikke K J ^a,b   Cornelius, Nanna ^c   Gregersen, Niels ^a,b  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c Rigshospitalet   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ARTICLE; BIOGENESIS; CELL DEATH; CELL FUNCTION; CELL METABOLISM; CELL REGENERATION; CELLULAR STRESS RESPONSE; FATTY ACID OXIDATION; GENE CONTROL; HUMAN; INBORN ERROR OF METABOLISM; MITOCHONDRIAL GENOME; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; OXIDATIVE STRESS; PROTEIN QUALITY; REDOX STRESS; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; METABOLISM; ORGANELLE BIOGENESIS; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PHYSIOLOGY;

HUMANS; METABOLISM, INBORN ERRORS; MITOCHONDRIAL DISEASES; ORGANELLE BIOGENESIS; OXIDATION-REDUCTION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 84937250645     PISSN: 01418955     EISSN: 15732665     Source Type: Journal    
DOI: 10.1007/s10545-015-9861-5     Document Type: Article

References (142)

1. Ahuja P, Wanagat J, Wang Z et al (2013) Divergent mitochondrial biogenesis responses in human cardiomyopathy. Circulation 127:1957–1967
2. Aires V, Delmas D, Le Bachelier C et al (2014) Stilbenes and resveratrol metabolites improve mitochondrial fatty acid oxidation defects in human fibroblasts. Orphanet J Rare Dis 9:79
3. Aquilano K, Baldelli S, Pagliei B, Cannata SM, Rotilio G, Ciriolo MR (2013) p53 orchestrates the PGC-1alpha-mediated antioxidant response upon mild redox and metabolic imbalance. Antioxid Redox Signal 18:386–399
4. Archer SL (2013) Mitochondrial dynamics–mitochondrial fission and fusion in human diseases. N Engl J Med 369:2236–2251
5. Baldelli S, Aquilano K, Ciriolo MR (2013) Punctum on two different transcription factors regulated by PGC-1alpha: nuclear factor erythroid-derived 2-like 2 and nuclear respiratory factor 2. Biochim Biophys Acta 1830:4137–4146
6. Baldelli S, Aquilano K, Ciriolo MR (2014) PGC-1alpha buffers ROS-mediated removal of mitochondria during myogenesis. Cell Death Dis 5:e1515
7. Bastin J (2014) Regulation of mitochondrial fatty acid β-oxidation in human: what can we learn from inborn fatty acid β-oxidation deficiencies? Biochimie 96:113–120
8. Bastin J, Bonnefont JP, Djouadi F, Bresson JL (2014) Should the beneficial impact of bezafibrate on fatty acid oxidation disorders be questioned? J Inherit Metab Dis
9. Bates MG, Bourke JP, Giordano C, d’Amati G, Turnbull DM, Taylor RW (2012) Cardiac involvement in mitochondrial DNA disease: clinical spectrum, diagnosis, and management. Eur Heart J 33:3023–3033
10. Bauer S, Wanninger J, Neumeier M et al (2011) Elevated free fatty acids and impaired adiponectin bioactivity contribute to reduced SOD2 protein in monocytes of type 2 diabetes patients. Exp Mol Pathol 90:101–106
11. Bell EL, Emerling BM, Ricoult SJ, Guarente L (2011) SirT3 suppresses hypoxia inducible factor 1alpha and tumor growth by inhibiting mitochondrial ROS production. Oncogene 30:2986–2996
12. Bobba A, Amadoro G, Valenti D, Corsetti V, Lassandro R, Atlante A (2013) Mitochondrial respiratory chain complexes I and IV are impaired by beta-amyloid via direct interaction and through complex I-dependent ROS production, respectively. Mitochondrion 13:298–311
13. Bolisetty S, Jaimes EA (2013) Mitochondria and reactive oxygen species: physiology and pathophysiology. Int J Mol Sci 14:6306–6344
14. Bonnefont JP, Bastin J, Behin A, Djouadi F (2009) Bezafibrate for an inborn mitochondrial beta-oxidation defect. N Engl J Med 360:838–840
15. Bonnefont JP, Bastin J, Laforet P et al (2010) Long-term follow-up of bezafibrate treatment in patients with the myopathic form of carnitine palmitoyltransferase 2 deficiency. Clin Pharmacol Ther 88:101–108
16. Brenmoehl J, Hoeflich A (2013) Dual control of mitochondrial biogenesis by sirtuin 1 and sirtuin 3. Mitochondrion 13:755–761
17. Calabrese V, Cornelius C, Dinkova-Kostova AT et al (2012) Cellular stress responses, hormetic phytochemicals and vitagenes in aging and longevity. Biochim Biophys Acta 1822:753–783
18. Casarin A, Giorgi G, Pertegato V et al (2012) Copper and bezafibrate cooperate to rescue cytochrome c oxidase deficiency in cells of patients with SCO2 mutations. Orphanet J Rare Dis 7:21
19. Charniot JC, Sutton A, Bonnefont-Rousselot D et al (2011) Manganese superoxide dismutase dimorphism relationship with severity and prognosis in cardiogenic shock due to dilated cardiomyopathy. Free Radic Res 45:379–388
20. Chiribau CB, Cheng L, Cucoranu IC, Yu YS, Clempus RE, Sorescu D (2008) FOXO3A regulates peroxiredoxin III expression in human cardiac fibroblasts. J Biol Chem 283:8211–8217
21. Cornelius N, Frerman FE, Corydon TJ et al (2012) Molecular mechanisms of riboflavin responsiveness in patients with ETF-QO variations and multiple acyl-CoA dehydrogenation deficiency. Hum Mol Genet 21:3435–3448
22. Cornelius N, Byron C, Hargreaves I et al (2013) Secondary coenzyme Q10 deficiency and oxidative stress in cultured fibroblasts from patients with riboflavin responsive multiple Acyl-CoA dehydrogenation deficiency. Hum Mol Genet 22:3819–3827
23. Cornelius N, Gregersen N, Tümer Z, Olsen RK (2014a) Oxidative stress and mitochondrial defect in neuromuscular disorders: source or symptoms? In: Oxidative stress: causes, role in diseases and biological effects. Nova Biomedical, Huntington
24. Cornelius N, Corydon TJ, Gregersen N, Olsen RK (2014b) Cellular consequences of oxidative stress in riboflavin responsive multiple acyl-CoA dehydrogenation deficiency patient fibroblasts. Hum Mol Genet 23:4285–4301
25. Dai DF, Chen T, Wanagat J et al (2010) Age-dependent cardiomyopathy in mitochondrial mutator mice is attenuated by overexpression of catalase targeted to mitochondria. Aging Cell 9:536–544
26. De la Mata M, Garrido-Maraver J, Cotan D et al (2012) Recovery of MERRF fibroblasts and cybrids pathophysiology by coenzyme Q10. Neurotherapeutics 9:446–463
27. De Paepe B, Vandemeulebroecke K, Smet J et al (2014) Effect of resveratrol on cultured skin fibroblasts from patients with oxidative phosphorylation defects. Phytother Res 28:312–316
28. Demirovic D, Rattan SI (2013) Establishing cellular stress response profiles as biomarkers of homeodynamics, health and hormesis. Exp Gerontol 48:94–98
29. Desquiret-Dumas V, Gueguen N, Leman G et al (2013) Resveratrol induces a mitochondrial complex I-dependent increase in NADH oxidation responsible for sirtuin activation in liver cells. J Biol Chem 288:36662–36675
30. Djouadi F, Aubey F, Schlemmer D et al (2005) Bezafibrate increases very-long-chain acyl-CoA dehydrogenase protein and mRNA expression in deficient fibroblasts and is a potential therapy for fatty acid oxidation disorders. Hum Mol Genet 14:2695–2703
31. Dröse S, Brandt U (2012) Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv Exp Med Biol 748:145–169
32. Elstner M, Turnbull DM (2012) Transcriptome analysis in mitochondrial disorders. Brain Res Bull 88:285–293
33. Figge MT, Osiewacz HD, Reichert AS (2013) Quality control of mitochondria during aging: is there a good and a bad side of mitochondrial dynamics? Bioessays 35:314–322
34. Finley LW, Carracedo A, Lee J et al (2011) SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell 19:416–428
35. Fischer F, Hamann A, Osiewacz HD (2012) Mitochondrial quality control: an integrated network of pathways. Trends Biochem Sci 37:284–292
36. Gempel K, Topaloglu H, Talim B et al (2007) The myopathic form of coenzyme Q10 deficiency is caused by mutations in the electron-transferring-flavoprotein dehydrogenase (ETFDH) gene. Brain 130:2037–2044
37. Gobin-Limballe S, Djouadi F, Aubey F et al (2007) Genetic basis for correction of very-long-chain acyl-coenzyme A dehydrogenase deficiency by bezafibrate in patient fibroblasts: toward a genotype-based therapy. Am J Hum Genet 81:1133–1143
38. Golubitzky A, Dan P, Weissman S et al (2011) Screening for active small molecules in mitochondrial complex I deficient patient’s fibroblasts, reveals AICAR as the most beneficial compound. PLoS One 6:e26883
39. Goncalves RL, Quinlan CL, Perevoshchikova IV et al (2015) Sites of superoxide and hydrogen peroxide production by muscle mitochondria assessed ex vivo under conditions mimicking rest and exercise. J Biol Chem 290:209–227
40. Goodman SI, Binard RJ, Woontner MR, Frerman FE (2002) Glutaric acidemia type II: gene structure and mutations of the electron transfer flavoprotein:ubiquinone oxidoreductase (ETF:QO) gene. Mol Genet Metab 77:86–90
41. Grant CM (2008) Metabolic reconfiguration is a regulated response to oxidative stress. J Biol 7:1
42. Gregersen N, Bross P (2010) Protein misfolding and cellular stress: an overview. Methods Mol Biol 648:3–23
43. Gregersen N, Andresen BS, Pedersen CB, Olsen RK, Corydon TJ, Bross P (2008) Mitochondrial fatty acid oxidation defects–remaining challenges. J Inherit Metab Dis 31:643–657
44. Grunert SC (2014) Clinical and genetical heterogeneity of late-onset multiple acyl-coenzyme A dehydrogenase deficiency. Orphanet J Rare Dis 9:117
45. Guha M, Avadhani NG (2013) Mitochondrial retrograde signaling at the crossroads of tumor bioenergetics, genetics and epigenetics. Mitochondrion 13:577–591
46. Guo J, Lemire BD (2003) The ubiquinone-binding site of the saccharomyces cerevisiae succinate-ubiquinone oxidoreductase is a source of superoxide. J Biol Chem 278:47629–47635
47. Gut P, Verdin E (2013) The nexus of chromatin regulation and intermediary metabolism. Nature 502:489–498
48. Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT (2008) 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 28:718–731
49. Hagenbuchner J, Ausserlechner MJ (2013) Mitochondria and FOXO3: breath or die. Front Physiol 4:147
50. Hayashi G, Shen Y, Pedersen TL, Newman JW, Pook M, Cortopassi G (2014) Frataxin deficiency increases cyclooxygenase 2 and prostaglandins in cell and animal models of Friedreich’s ataxia. Hum Mol Genet 23:6838–6847
51. Heiss EH, Schachner D, Zimmermann K, Dirsch VM (2013) Glucose availability is a decisive factor for Nrf2-mediated gene expression. Redox Biol 1:359–365
52. Higdon A, Diers AR, Oh JY, Landar A, Darley-Usmar VM (2012) Cell signalling by reactive lipid species: new concepts and molecular mechanisms. Biochem J 442:453–464
53. Holley AK, Dhar SK, St Clair DK (2013) Curbing cancer’s sweet tooth: is there a role for MnSOD in regulation of the Warburg effect? Mitochondrion 13:170–188
54. Houtkooper RH, Pirinen E, Auwerx J (2012) Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 13:225–238
55. Huang J, Lemire BD (2009) Mutations in the C. elegans succinate dehydrogenase iron-sulfur subunit promote superoxide generation and premature aging. J Mol Biol 387:559–569
56. Huang D, Li T, Li X et al (2014) HIF-1-mediated suppression of acyl-CoA dehydrogenases and fatty acid oxidation is critical for cancer progression. Cell Rep 8:1930–1942
57. Jain A, Lamark T, Sjottem E et al (2010) p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J Biol Chem 285:22576–22591
58. Kansanen E, Jyrkkanen HK, Levonen AL (2012) Activation of stress signaling pathways by electrophilic oxidized and nitrated lipids. Free Radic Biol Med 52:973–982
59. Kauppinen A, Suuronen T, Ojala J et al (2013) Antagonistic crosstalk between NF-kB and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Sigal 25:1939–1948
60. Kemper MF, Stirone C, Krause DN, Duckles SP, Procaccio V (2014) Genomic and non-genomic regulation of PGC1 isoforms by estrogen to increase cerebral vascular mitochondrial biogenesis and reactive oxygen species protection. Eur J Pharmacol 723:322–329
61. Kim T, Yang Q (2013) Peroxisome-proliferator-activated receptors regulate redox signaling in the cardiovascular system. World J Cardiol 5:164–174
62. Kolker S, Burgard P, Sauer SW, Okun JG (2013) Current concepts in organic acidurias: understanding intra- and extracerebral disease manifestation. J Inherit Metab Dis 36:635–644
63. Komatsu M, Kurokawa H, Waguri S et al (2010) The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 12:213–223
64. Komen JC, Thorburn DR (2014) Turn up the power - pharmacological activation of mitochondrial biogenesis in mouse models. Br J Pharmacol 171:1818–1836
65. Koopman WJ, Willems PH, Smeitink JA (2012) Monogenic mitochondrial disorders. N Engl J Med 366:1132–1141
66. Koopman WJ, Distelmaier F, Smeitink JA, Willems PH (2013) OXPHOS mutations and neurodegeneration. EMBO J 32:9–29
67. Kops GJ, Dansen TB, Polderman PE et al (2002) Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419:316–321
68. Kotiadis VN, Duchen MR, Osellame LD (2014) Mitochondrial quality control and communications with the nucleus are important in maintaining mitochondrial function and cell health. Biochim Biophys Acta 1840:1254–1265
69. Kwak MK, Wakabayashi N, Greenlaw JL, Yamamoto M, Kensler TW (2003) Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol Cell Biol 23:8786–8794
70. Laplante M, Sabatini DM (2012) mTOR signaling in growth control and disease. Cell 149:274–293
71. Lee SK, Lee JO, Kim JH et al (2012) Coenzyme Q10 increases the fatty acid oxidation through AMPK-mediated PPARalpha induction in 3T3-L1 preadipocytes. Cell Signal 24:2329–2336
72. Levonen AL, Hill BG, Kansanen E, Zhang J, Darley-Usmar VM (2014) Redox regulation of antioxidants, autophagy, and the response to stress: implications for electrophile therapeutics. Free Radic Biol Med 71:196–207
73. Li XN, Song J, Zhang L et al (2009) Activation of the AMPK-FOXO3 pathway reduces fatty acid-induced increase in intracellular reactive oxygen species by upregulating thioredoxin. Diabetes 58:2246–2257
74. Li H, Fukuda S, Hasegawa Y et al (2010) Effect of heat stress and bezafibrate on mitochondrial beta-oxidation: comparison between cultured cells from normal and mitochondrial fatty acid oxidation disorder children using in vitro probe acylcarnitine profiling assay. Brain Dev 32:362–370
75. Lim JH, Lee YM, Chun YS, Chen J, Kim JE, Park JW (2010) Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Mol Cell 38:864–878
76. Liu TF, Brown CM, El GM et al (2012) Fueling the flame: bioenergy couples metabolism and inflammation. J Leukoc Biol 92:499–507
77. Lopes CA, Le BC, Mathieu L et al (2014) Beneficial effects of resveratrol on respiratory chain defects in patients’ fibroblasts involve estrogen receptor and estrogen-related receptor alpha signaling. Hum Mol Genet 23:2106–2119
78. Lopez-Lluch G, Hunt N, Jones B et al (2006) Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci U S A 103:1768–1773
79. Marinho HS, Real C, Cyrne L, Soares H, Antunes F (2014) Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol 2:535–562
80. Marmolino D, Manto M, Acquaviva F et al (2010) PGC-1alpha down-regulation affects the antioxidant response in Friedreich’s ataxia. PLoS One 5:e10025
81. Milisav I, Poljsak B, Suput D (2012) Adaptive response, evidence of cross-resistance and its potential clinical use. Int J Mol Sci 13:10771–10806
82. Mohelnikova-Duchonova B, Marsakova L, Vrana D et al (2011) Superoxide dismutase and nicotinamide adenine dinucleotide phosphate: quinone oxidoreductase polymorphisms and pancreatic cancer risk. Pancreas 40:72–78
83. Ngo JK, Pomatto LC, Davies KJ (2013) Upregulation of the mitochondrial Lon Protease allows adaptation to acute oxidative stress but dysregulation is associated with chronic stress, disease, and aging. Redox Biol 1:258–264
84. Nicolson GL, Ash ME (2014) Lipid replacement therapy: a natural medicine approach to replacing damaged lipids in cellular membranes and organelles and restoring function. Biochim Biophys Acta 1838:1657–1679
85. Nunnari J, Suomalainen A (2012) Mitochondria: in sickness and in health. Cell 148:1145–1159
86. Olsen RK, Andresen BS, Christensen E, Bross P, Skovby F, Gregersen N (2003) Clear relationship between ETF/ETFDH genotype and phenotype in patients with multiple acyl-CoA dehydrogenation deficiency. Hum Mutat 22:12–23
87. Olsen RK, Olpin SE, Andresen BS et al (2007) ETFDH mutations as a major cause of riboflavin-responsive multiple acyl-CoA dehydrogenation deficiency. Brain 130:2045–2054
88. Olsen RK, Cornelius N, Gregersen N (2013) Genetic and cellular modifiers of oxidative stress: what can we learn from fatty acid oxidation defects? Mol Genet Metab 110(Suppl):S31–S39
89. Olsson J, Jacobson TA, Paulsson JM et al (2011) Expression of neutrophil SOD2 is reduced after lipopolysaccharide stimulation: a potential cause of neutrophil dysfunction in chronic kidney disease. Nephrol Dial Transplant 26:2195–2201
90. Orngreen MC, Madsen KL, Preisler N et al (2014) Bezafibrate in skeletal muscle fatty acid oxidation disorders: a randomized clinical trial. Neurology 82:607–613
91. Orngreen MC, Vissing J, Laforet P (2015) No effect of bezafibrate in patients with CPTII and VLCAD deficiencies. J Inherit Metab Dis
92. Page EL, Chan DA, Giaccia AJ, Levine M, Richard DE (2008) Hypoxia-inducible factor-1alpha stabilization in nonhypoxic conditions: role of oxidation and intracellular ascorbate depletion. Mol Biol Cell 19:86–94
93. Palacios OM, Carmona JJ, Michan S et al (2009) Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1alpha in skeletal muscle. Aging (Albany NY) 1:771–783
94. Patsi J, Kervinen M, Finel M, Hassinen IE (2008) Leber hereditary optic neuropathy mutations in the ND6 subunit of mitochondrial complex I affect ubiquinone reduction kinetics in a bacterial model of the enzyme. Biochem J 409:129–137
95. Piantadosi CA, Suliman HB (2012) Redox regulation of mitochondrial biogenesis. Free Radic Biol Med 53:2043–2053
96. Picard M, Juster RP, McEwen BS (2014) Mitochondrial allostatic load puts the ‘gluc’ back in glucocorticoids. Nat Rev Endocrinol 10:303–310
97. Pinti M, Gibellini L, De BS et al (2011) Functional characterization of the promoter of the human Lon protease gene. Mitochondrion 11:200–206
98. Pizzimenti S, Ciamporcero E, Daga M et al (2013) Interaction of aldehydes derived from lipid peroxidation and membrane proteins. Front Physiol 4:242
99. Polvani S, Tarocchi M, Galli A (2012) PPARgamma and oxidative stress: Con(beta) catenating NRF2 and FOXO. PPAR Res 2012:641087
100. Ray LB (2010) Metabolism. Metabolism is not boring. Introduction. Science 330:1337
101. Ristow M, Schmeisser K (2014) Mitohormesis: promoting health and lifespan by increased levels of reactive oxygen species (ROS). Dose-Response 12:288–341
102. Rocha H, Ferreira R, Carvalho J et al (2011) Characterization of mitochondrial proteome in a severe case of ETF-QO deficiency. J Proteomics 75:221–228
103. Rodell A, Rasmussen LJ, Bergersen LH, Singh KK, Gjedde A (2013) Natural selection of mitochondria during somatic lifetime promotes healthy aging. Front Neuroenerg 5:7
104. Rodrigues JV, Gomes CM (2012) Mechanism of superoxide and hydrogen peroxide generation by human electron-transfer flavoprotein and pathological variants. Free Radic Biol Med 53:12–19
105. Safdar A, Little JP, Stokl AJ, Hettinga BP, Akhtar M, Tarnopolsky MA (2011) Exercise increases mitochondrial PGC-1alpha content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J Biol Chem 286:10605–10617
106. Salminen A, Kaarniranta K (2009) Regulation of the aging process by autophagy. Trends Mol Med 15:217–224
107. Salminen A, Hyttinen JM, Kaarniranta K (2011) AMP-activated protein kinase inhibits NF-kappaB signaling and inflammation: impact on healthspan and lifespan. J Mol Med (Berl) 89:667–676
108. Sanchis-Gomar F, Garcia-Gimenez JL, Gomez-Cabrera MC, Pallardo FV (2014) Mitochondrial biogenesis in health and disease. Molecular and therapeutic approaches. Curr Pharm Des 20:5619–5633
109. Scarpulla RC, Vega RB, Kelly DP (2012) Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab 23:459–466
110. Schapira AH (2006) Mitochondrial disease. Lancet 368:70–82
111. Schumacker PT (2011) SIRT3 controls cancer metabolic reprogramming by regulating ROS and HIF. Cancer Cell 19:299–300
112. Scott JL, Gabrielides C, Davidson RK et al (2010) Superoxide dismutase downregulation in osteoarthritis progression and end-stage disease. Ann Rheum Dis 69:1502–1510
113. Sebastiani M, Giordano C, Nediani C et al (2007) Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies. J Am Coll Cardiol 50:1362–1369
114. Sharma LK, Fang H, Liu J, Vartak R, Deng J, Bai Y (2011) Mitochondrial respiratory complex I dysfunction promotes tumorigenesis through ROS alteration and AKT activation. Hum Mol Genet 20:4605–4616
115. Shirwany NA, Zou MH (2014) AMPK: a cellular metabolic and redox sensor. A minireview. Front Biosci (Landmark Ed) 19:447–474
116. Siciliano G, Simoncini C, Lo Gerfo A et al (2012) Effects of aerobic training on exercise-related oxidative stress in mitochondrial myopathies. Neuromuscul Disord 3:S172–S177
117. Smeitink J, van den Heuvel L, DiMauro S (2001) The genetics and pathology of oxidative phosphorylation. Nat Rev Genet 2:342–352
118. Song Y, Selak MA, Watson CT et al (2009) Mechanisms underlying metabolic and neural defects in zebrafish and human multiple acyl-CoA dehydrogenase deficiency (MADD). PLoS One 4:e8329
119. Stanyer L, Jorgensen W, Hori O, Clark JB, Heales SJ (2008) Inactivation of brain mitochondrial Lon protease by peroxynitrite precedes electron transport chain dysfunction. Neurochem Int 53:95–101
120. St-Pierre J, Buckingham JA, Roebuck SJ et al (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277:44784–44790
121. Suliman HB, Piantadosi CA (2014) Mitochondrial biogenesis: regulation by endogenous gases during inflammation and organ stress. Curr Pharm Des 20:5653–5662
122. Sundaresan NR, Gupta M, Kim G, Rajamohan SB, Isbatan A, Gupta MP (2009) Sirt3 blocks the cardiac hypertrophic response by augmenting Foxo3a-dependent antioxidant defense mechanisms in mice. J Clin Invest 119:2758–2771
123. Tabas I, Glass CK (2013) Anti-inflammatory therapy in chronic disease: challenges and opportunities. Science 339:166–172
124. Tello D, Balsa E, Acosta-Iborra B et al (2011) Induction of the mitochondrial NDUFA4L2 protein by HIF-1α decreases oxygen consumption by inhibiting complex I activity. Cell Metab 14:768–779
125. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324:1029–1033
126. Vives-Bauza C, Zhou C, Huang Y et al (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A 107:378–383
127. Wajner M, Goodman SI (2011) Disruption of mitochondrial homeostasis in organic acidurias: insights from human and animal studies. J Bioenerg Biomembr 43:31–38
128. Wallace DC, Fan W (2010) Energetics, epigenetics, mitochondrial genetics. Mitochondrion 10:12–31
129. Wang Y, Yang J, Yang K et al (2012) The biphasic redox sensing of SENP3 accounts for the HIF-1 transcriptional activity shift by oxidative stress. Acta Pharmacol Sin 33:953–963
130. Watmough NJ, Frerman FE (2010) The electron transfer flavoprotein: ubiquinone oxidoreductases. Biochim Biophys Acta 1797:1910–1916
131. Wei YH, Wu SB, Ma YS, Lee HC (2009) Respiratory function decline and DNA mutation in mitochondria, oxidative stress and altered gene expression during aging. Chang Gung Med J 32:113–132
132. Wen B, Dai T, Li W et al (2010) Riboflavin-responsive lipid-storage myopathy caused by ETFDH gene mutations. J Neurol Neurosurg Psychiatry 81:231–236
133. Wu SB, Wei YH (2012) AMPK-mediated increase of glycolysis as an adaptive response to oxidative stress in human cells: implication of the cell survival in mitochondrial diseases. Biochim Biophys Acta 1822:233–247
134. Wu SB, Ma YS, Wu YT, Chen YC, Wei YH (2010) Mitochondrial DNA mutation-elicited oxidative stress, oxidative damage, and altered gene expression in cultured cells of patients with MERRF syndrome. Mol Neurobiol 41:256–266
135. Wu SB, Wu YT, Wu TP, Wei YH (2014) Role of AMPK-mediated adaptive responses in human cells with mitochondrial dysfunction to oxidative stress. Biochim Biophys Acta 1840:1331–1344
136. Yamaguchi S, Li H, Purevsuren J et al (2012) Bezafibrate can be a new treatment option for mitochondrial fatty acid oxidation disorders: evaluation by in vitro probe acylcarnitine assay. Mol Genet Metab 107:87–91
137. Yechoor VK, Patti ME, Ueki K et al (2004) Distinct pathways of insulin-regulated versus diabetes-regulated gene expression: an in vivo analysis in MIRKO mice. Proc Natl Acad Sci U S A 101:16525–16530
138. Youle RJ, van der Bliek AM (2012) Mitochondrial fission, fusion, and stress. Science 337:1062–1065
139. Zhang Q, Raoof M, Chen Y et al (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464:104–107
140. Zhang Z, Tsukikawa M, Peng M et al (2013) Primary respiratory chain disease causes tissue-specific dysregulation of the global transcriptome and nutrient-sensing signaling network. PLoS One 8:e69282
141. Zhou R, Yazdi AS, Menu P, Tschopp J (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469:221–225
142. Zolkipli Z, Pedersen CB, Lamhonwah AM, Gregersen N, Tein I (2011) Vulnerability to oxidative stress in vitro in pathophysiology of mitochondrial short-chain acyl-CoA dehydrogenase deficiency: response to antioxidants. PLoS One 6:e17534