Cellular consequences of oxidative stress in riboflavin responsive multiple acyl-CoA dehydrogenation deficiency patient fibroblasts

Human Molecular Genetics

Volumn 23, Issue 16, 2014, Pages 4285-4301

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

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A; DJ 1 PROTEIN; ENDOPEPTIDASE LA; MITOFUSIN 2; PROTEIN P62; REACTIVE OXYGEN METABOLITE; RIBOFLAVIN; SIRTUIN 3; UBIDECARENONE; ANTIOXIDANT; ELECTRON TRANSFER FLAVOPROTEIN UBIQUINONE OXIDOREDUCTASE; OXIDOREDUCTASE; UNCLASSIFIED DRUG; UBIQUINONE; VITAMIN;

ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; FATTY ACID OXIDATION; FIBROBLAST; HUMAN; HUMAN CELL; IN VITRO STUDY; METABOLIC REGULATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; MITOPHAGY; OXIDATIVE DEHYDROGENATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RIBOFLAVIN DEFICIENCY; RIBOFLAVIN RESPONSIVE MULTIPLE ACYL COENZYME A DEHYDROGENATION DEFICIENCY; APOPTOSIS; ENERGY METABOLISM; MULTIPLE ACYL COA DEHYDROGENASE DEFICIENCY; SKIN FIBROBLAST; ANALOGS AND DERIVATIVES; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; METABOLISM; NUCLEAR REPROGRAMMING; SKIN;

ANTIOXIDANTS; CELLS, CULTURED; CELLULAR REPROGRAMMING; FIBROBLASTS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MULTIPLE ACYL COENZYME A DEHYDROGENASE DEFICIENCY; OXIDATIVE STRESS; RIBOFLAVIN; SKIN; UBIQUINONE; VITAMINS;

EID: 84904739597     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu146     Document Type: Article

References (76)

1. McBride, H.M., Neuspiel, M. and Wasiak, S. (2006) Mitochondria: more than just a powerhouse. Curr. Biol., 16, R551-R560.
2. Drose, S. and Brandt, U. (2012) Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv. Exp. Med. Biol., 748, 145-169.
3. Lenaz, G. (2001) The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology.IUBMBLife, 52, 159-164.
4. Nakamura, T., Cho, D.H. and Lipton, S.A. (2012) Redox regulation of protein misfolding, mitochondrial dysfunction, synaptic damage, and cell death in neurodegenerative diseases. Exp. Neurol., 238, 12-21.
5. Pallardo, F.V., Lloret, A., Lebel, M., d'Ischia, M., Cogger, V.C., Le Couteur, D.G., Gadaleta, M.N., Castello, G. and Pagano, G. (2010) Mitochondrial dysfunction in some oxidative stress-related genetic diseases: Ataxia-Telangiectasia, Down Syndrome, Fanconi Anaemia and Werner Syndrome. Biogerontology, 11, 401-419.
6. Brieger, K., Schiavone, S., Miller, F.J. Jr and Krause, K.H. (2012) Reactive oxygen species: from health to disease. Swiss. Med. Wkly., 142, w13659.
7. Echtay, K.S. (2007) Mitochondrial uncoupling proteins - what is their physiological role? Free Radic. Biol. Med., 43, 1351-1371.
8. Fischer, F., Hamann, A. and Osiewacz, H.D. (2012) Mitochondrial quality control: an integrated network of pathways. Trends Biochem. Sci., 37, 284-292.
9. Frerman, F.E. andGoodman, S.I. (2001) In Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), The Metabolic and Molecular Bases of Inherited Diseases. McGraw-Hill, New York, pp. 2357-2365.
10. Ghisla, S. and Thorpe, C. (2004) Acyl-CoA dehydrogenases. A mechanistic overview. Eur. J. Biochem., 271, 494-508.
11. Gregersen, N., Rhead, W. and Christensen, E. (1990) Riboflavin responsive glutaric aciduria type II. Prog. Clin. Biol. Res., 321, 477-494.
12. Gregersen, N., Wintzensen, H., Christensen, S.K., Christensen, M.F., Brandt, N.J. and Rasmussen, K. (1982) C6-C10-dicarboxylic aciduria: investigations of a patient with riboflavin responsive multiple acyl-CoA dehydrogenation defects. Pediatr. Res., 16, 861-868.
13. Cornelius, N., Frerman, F.E., Corydon, T.J., Palmfeldt, J., Bross, P., Gregersen, N. and Olsen, R.K. (2012) Molecular mechanisms of riboflavin responsiveness in patients with ETF-QO variations and multiple acyl-CoA dehydrogenation deficiency. Hum. Mol. Genet., 21, 3435-3448.
14. Cornelius, N., Byron, C., Hargreaves, I., Guerra, P.F., Furdek, A.K., Land, J., Radford, W.W., Frerman, F., Corydon, T.J., Gregersen, N. and Olsen, R.K. (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.
15. Gempel, K., Topaloglu, H., Talim, B., Schneiderat, P., Schoser, B.G.H., Hans, V.H., Palmafy, B., Kale, G., Tokatli, A., Quinzii, C. 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.
16. Liang, W.C., Ohkuma, A., Hayashi, Y.K., Lopez, L.C., Hirano, M., Nonaka, I., Noguchi, S., Chen, L.H., Jong, Y.J. and Nishino, I. (2009) ETFDH mutations, CoQ10 levels, and respiratory chain activities in patients with riboflavin-responsive multiple acyl-CoA dehydrogenase deficiency. Neuromuscul. Disord., 19, 212-216.
17. Holley, A.K., Bakthavatchalu, V., Velez-Roman, J.M. and St Clair, D.K. (2011)Manganesesuperoxide dismutase: guardian of the powerhouse. Int. J. Mol. Sci., 12, 7114-7162.
18. Ngo, J.K. and Davies, K.J. (2009) Mitochondrial Lon protease is a human stress protein. Free Radic. Biol. Med., 46, 1042-1048.
19. Ugarte, N., Petropoulos, I. and Friguet, B. (2010) Oxidized mitochondrial protein degradation and repair in aging and oxidative stress. Antioxid. Redox. Signal., 13, 539-549.
20. Matsushima, Y., Goto, Y. and Kaguni, L.S. (2010) Mitochondrial Lon protease regulates mitochondrial DNA copy number and transcription by selective degradation of mitochondrial transcription factorA(TFAM). Proc. Natl. Acad. Sci. USA, 107, 18410-18415.
21. Lu, B., Yadav, S., Shah, P.G., Liu, T., Tian, B., Pukszta, S., Villaluna, N., Kutejova, E., Newlon, C.S., Santos, J.H. and Suzuki, C.K. (2007) Roles for the human ATP-dependent Lon protease in mitochondrial DNA maintenance. J. Biol. Chem., 282, 17363-17374.
22. Taira, T., Saito, Y., Niki, T., Iguchi-Ariga, S.M., Takahashi,K. and Ariga, H. (2004) DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep., 5, 213-218.
23. Irrcher, I., Aleyasin, H., Seifert, E.L., Hewitt, S.J., Chhabra, S., Phillips, M., Lutz, A.K., Rousseaux, M.W., Bevilacqua, L., Jahani-Asl, A. et al. (2010) Loss of the Parkinson's disease-linked gene DJ-1 perturbs mitochondrial dynamics. Hum. Mol. Genet., 19, 3734-3746.
24. Westermann, B. (2010) Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol., 11, 872-884.
25. Ashrafi, G. and Schwarz, T.L. (2013) The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death. Differ., 20, 31-42.
26. Liu, X., Weaver, D., Shirihai, O. and Hajnoczky, G. (2009) Mitochondrial 'kiss-and-run': interplay between mitochondrial motility and fusion-fission dynamics. EMBO J., 28, 3074-3089.
27. Twig, G., Elorza, A., Molina, A.J., Mohamed, H., Wikstrom, J.D., Walzer, G., Stiles, L., Haigh, S.E., Katz, S., Las, G. et al. (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J., 27, 433-446.
28. Kubli, D.A. and Gustafsson, A.B. (2012) Mitochondria and mitophagy: the yin and yang of cell death control. Circ. Res., 111, 1208-1221.
29. Komatsu,M. and Ichimura, Y. (2010) Physiological significance of selective degradation of p62 by autophagy. FEBS Lett., 584, 1374-1378.
30. Bjorkoy, G., Lamark, T., Pankiv, S., Overvatn, A., Brech, A. and Johansen, T. (2009) Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol., 452, 181-197.
31. Huang, C., Andres, A.M., Ratliff, E.P., Hernandez, G., Lee, P. and Gottlieb, R.A. (2011) Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS ONE, 6, e20975.
32. Geisler, S., Holmstrom, K.M., Skujat, D., Fiesel, F.C., Rothfuss, O.C., Kahle, P.J. and Springer, W. (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol., 12, 119-131.
33. Wolfe, L.A., He, M., Vockley, J., Payne, N., Rhead, W., Hoppel, C., Spector, E., Gernert, K. and Gibson, K.M. (2010) Novel ETF dehydrogenase mutations in a patient with mild glutaric aciduria type II and complex II-III deficiency in liver and muscle. J. Inherit. Metab. Dis.
34. Wen,B., Dai, T., Li, W., Zhao, Y., Liu, S., Zhang, C., Li, H.,Wu,J., Li, D. and Yan, C. (2010) Riboflavin-responsive lipid-storage myopathy caused by ETFDH gene mutations. J. Neurol. Neurosurg. Psychiatry, 81, 231-236.
35. Olsen, R.K., Olpin, S.E., Andresen, B.S., Miedzybrodzka, Z.H., Pourfarzam, M., Merinero, B., Frerman, F.E., Beresford, M.W., Dean, J.C., Cornelius, N. et al. (2007) ETFDH mutations as a major cause of riboflavin-responsive multiple acyl-CoA dehydrogenation deficiency. Brain, 130, 2045-2054.
36. Song, Y., Selak, M.A., Watson, C.T., Coutts, C., Scherer, P.C., Panzer, J.A., Gibbs, S., Scott, M.O., Willer, G., Gregg, R.G. et al. (2009) Mechanisms underlying metabolic and neural defects in zebrafish and human multiple acyl-CoA dehydrogenase deficiency (MADD). PLoS ONE, 4, e8329.
37. Rocha, H., Ferreira, R., Carvalho, J., Vitorino, R., Santa, C., Lopes, L., Gregersen, N., Vilarinho, L. and Amado, F. (2011) Characterization of mitochondrial proteome in a severe case of ETF-QO deficiency. J. Proteomics, 75, 221-228.
38. Holley, A.K., Dhar, S.K. and St Clair, D.K. (2013) Curbing cancer's sweet tooth: is there a role for MnSOD in regulation of the Warburg effect? Mitochondrion, 13, 170-188.
39. Finley, L.W., Carracedo, A., Lee, J., Souza, A., Egia, A., Zhang, J., Teruya-Feldstein, J., Moreira, P.I., Cardoso, S.M., Clish, C.B. et al. (2011) SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell, 19, 416-428.
40. Bell, E.L., Emerling, B.M., Ricoult, S.J. and Guarente, L. (2011) SirT3 suppresses hypoxia inducible factor 1alpha and tumor growth by inhibiting mitochondrial ROS production. Oncogene, 30, 2986-2996.
41. Tao, R., Coleman, M.C., Pennington, J.D., Ozden, O., Park, S.H., Jiang, H., Kim, H.S., Flynn, C.R., Hill, S., Hayes, M.W. et al. (2010) Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol. Cell, 40, 893-904.
42. Henriques, B.J., Olsen, R.K., Bross, P. and Gomes, C.M. (2010) Emerging roles for riboflavin in functional rescue of mitochondrial beta-oxidation flavoenzymes. Curr. Med. Chem., 17, 3842-3854.
43. Gregersen, N. and Olsen, R.K. (2010) Disease mechanisms and protein structures in fatty acid oxidation defects. J. Inherit. Metab. Dis., 33, 547-553.
44. Gregersen, N., Andresen, B.S., Pedersen, C.B., Olsen, R.K., Corydon, T.J. and Bross, P. (2008) Mitochondrial fatty acid oxidation defects - remaining challenges. J. Inherit. Metab. Dis., 31, 643-657.
45. Miao, L. and St Clair, D.K. (2009) Regulation of superoxide dismutase genes: implications in disease. Free Radic. Biol. Med., 47, 344-356.
46. Circu, M.L. and Aw, T.Y. (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med., 48, 749-762.
47. Pedersen, C.B., Zolkipli, Z., Vang, S., Palmfeldt, J., Kjeldsen, M., Stenbroen, V., Schmidt, S.P., Wanders, R.J., Ruiter, J.P., Wibrand, F. et al. (2010) Antioxidant dysfunction: potential risk for neurotoxicity in ethylmalonic aciduria. J. Inherit. Metab. Dis., 33, 211-222.
48. Schmidt, S.P., Corydon, T.J., Pedersen, C.B., Bross, P. and Gregersen, N. (2010) Misfolding of short-chain acyl-CoA dehydrogenase leads to mitochondrial fission and oxidative stress. Mol. Genet. Metab., 100, 155-162.
49. Olsen, R.K., Cornelius, N. and Gregersen, N. (2013) Genetic and cellular modifiers of oxidative stress: What can we learn from fatty acid oxidation defects? Mol. Genet. Metab.
50. Van, M.L. and Aertsen, A. (2009) Regulation and quality control by Lon-dependent proteolysis. Res. Microbiol., 160, 645-651.
51. Hansen, J., Corydon, T.J., Palmfeldt, J., Durr, A., Fontaine, B., Nielsen, M.N., Christensen, J.H., Gregersen, N. and Bross, P. (2008) Decreased expression of the mitochondrial matrix proteases Lon and ClpP in cells from a patient with hereditary spastic paraplegia (SPG13). Neuroscience, 153, 474-482.
52. Stanyer, L., Jorgensen, W., Hori, O., Clark, J.B. and Heales, S.J. (2008) Inactivation of brain mitochondrial Lon protease by peroxynitrite precedes electron transport chain dysfunction. Neurochem. Int., 53, 95-101.
53. Ngo, J.K., Pomatto, L.C. and Davies, K.J. (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.
54. Wen, B., Li, D., Shan, J., Liu, S., Li, W., Zhao, Y., Lin, P., Zheng, J., Li, D., Gong, Y. and Yan, C. (2013) Increased muscle coenzyme Q10 in riboflavin responsive MADD with ETFDH gene mutations due to secondary mitochondrial proliferation. Mol. Genet. Metab., 109, 154-160.
55. Kim, S.H., Scott, S.A., Bennett, M.J., Carson, R.P., Fessel, J., Brown, H.A. and Ess, K.C. (2013) Multi-organ abnormalities and mTORC1 activation in zebrafish model of multiple acyl-CoA dehydrogenase deficiency. PLoS Genet., 9, e1003563.
56. Morita, M., Gravel, S.P., Chenard, V., Sikstrom, K., Zheng, L., Alain, T., Gandin, V., Avizonis, D., Arguello, M., Zakaria, C. et al. (2013) mTORC1 controls mitochondrial activity and biogenesis through 4E-BP-dependent translational regulation. Cell Metab., 18, 698-711.
57. Khan, M.M., Ahmad, A., Ishrat, T., Khan, M.B., Hoda, M.N., Khuwaja, G., Raza, S.S., Khan, A., Javed, H., Vaibhav, K. and Islam, F. (2010) Resveratrol attenuates 6-hydroxydopamine-induced oxidative damage and dopamine depletion in rat model of Parkinson's disease. Brain Res., 1328, 139-151.
58. Maher, P., Dargusch, R., Bodai, L., Gerard, P.E., Purcell, J.M. and Marsh, J.L. (2011) ERK activation by the polyphenols fisetin and resveratrol provides neuroprotection in multiple models of Huntington's disease. Hum. Mol. Genet., 20, 261-270.
59. Ho, D.J., Calingasan, N.Y., Wille, E., Dumont, M. and Beal, M.F. (2010) Resveratrol protects against peripheral deficits in a mouse model of Huntington's disease. Exp. Neurol., 225, 74-84.
60. Anekonda, T.S. and Reddy, P.H. (2006) Neuronal protection by sirtuins in Alzheimer's disease. J. Neurochem., 96, 305-313.
61. Wenz, T., Diaz, F., Spiegelman, B.M. and Moraes, C.T. (2008) Activation of the PPAR/PGC-1alpha pathway prevents a bioenergetic deficit and effectively improves a mitochondrial myopathy phenotype. Cell Metab., 8, 249-256.
62. Li, D.,Dammer,E.B. and Sewer, M.B.(2012) Resveratrol stimulates cortisol biosynthesis by activating SIRT-dependent deacetylation of P450scc. Endocrinology, 153, 3258-3268.
63. Schirmer, H., Pereira, T.C., Rico, E.P., Rosemberg, D.B., Bonan, C.D., Bogo, M.R. and Souto, A.A. (2012) Modulatory effect of resveratrol on SIRT1, SIRT3, SIRT4, PGC1alpha andNAMPTgene expression profiles in wild-type adult zebrafish liver. Mol. Biol. Rep., 39, 3281-3289.
64. Li, H., Yan, Z., Zhu, J., Yang, J. and He, J. (2011) Neuroprotective effects of resveratrol on ischemic injury mediated by improving brain energy metabolism and alleviating oxidative stress in rats. Neuropharmacology, 60, 252-258.
65. Das, S., Khan, N., Mukherjee, S., Bagchi, D., Gurusamy, N., Swartz, H. and Das, D.K. (2008) Redox regulation of resveratrol-mediated switching of death signal into survival signal. Free Radic. Biol. Med., 44, 82-90.
66. Kode, A., Rajendrasozhan, S., Caito, S., Yang, S.R., Megson, I.L. and Rahman, I. (2008) Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol., 294, L478-L488.
67. Robb, E.L., Winkelmolen, L., Visanji, N., Brotchie, J. and Stuart, J.A. (2008) Dietary resveratrol administration increasesMnSODexpression and activity in mouse brain. Biochem. Biophys. Res. Commun., 372, 254-259.
68. Robb, E.L., Page, M.M., Wiens, B.E. and Stuart, J.A. (2008) Molecular mechanisms of oxidative stress resistance induced by resveratrol: Specific and progressive induction of MnSOD. Biochem. Biophys. Res. Commun., 367, 406-412.
69. Bonnefont, J.P., Bastin, J., Behin, A. and Djouadi, F. (2009) Bezafibrate for an inborn mitochondrial beta-oxidation defect. N. Engl. J Med., 360, 838-840.
70. Djouadi, F., Aubey, F., Schlemmer, D. and Bastin, J. (2005) Peroxisome proliferator activated receptor delta (PPARdelta) agonist but not PPARalpha corrects carnitine palmitoyl transferase 2 deficiency in human muscle cells. J. Clin. Endocrinol. Metab., 90, 1791-1797.
71. Quinzii, C.M., DiMauro, S. and Hirano, M. (2007) Human coenzyme Q10 deficiency. Neurochem. Res., 32, 723-727.
72. Hargreaves, I.P. (2014) CoenzymeQas a therapy for mitochondrial disease. Int. J. Biochem. Cell Biol., 49C, 105-111.
73. Horvath, R. (2012) Update on clinical aspects and treatment of selected vitamin-responsive disorders II (riboflavin and CoQ 10). J. Inherit. Metab. Dis., 35, 679-687.
74. Manthey, K.C., Chew, Y.C. and Zempleni, J. (2005) Riboflavin deficiency impairs oxidative folding and secretion of apolipoprotein B-100 in HepG2 cells, triggering stress response systems. J. Nutr., 135, 978-982.
75. Feder, S., Daniel, H. and Rehner, G. (1991) In vivo kinetics of intestinal absorption of riboflavin in rats. J. Nutr., 121, 72-79.
76. Zempleni, J. (1995) Determination of riboflavin and flavocoenzymes in human blood plasma by high-performance liquid chromatography. Ann. Nutr. Metab, 39, 224-226.