Emerging roles for riboflavin in functional rescue of mitochondrial β-oxidation flavoenzymes

Current Medicinal Chemistry

Volumn 17, Issue 32, 2010, Pages 3842-3854

  Henriques, Bárbara J ^a   Olsen, Rikke K ^b   Bross, Peter ^b   Gomes, Cláudio M ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Biophysics; Conformational destabilisation; Disease; Flavin; Mitochondrial metabolism; Protein folding; Riboflavin responsive

Indexed keywords

ELECTRON TRANSFERRING FLAVOPROTEIN; ELECTRON TRANSFERRING FLAVOPROTEIN DEHYDROGENASE; FLAVINE MONONUCLEOTIDE; FLAVOPROTEIN; GLUTARYL COENZYME A DEHYDROGENASE; ISOBUTYRYL COENZYME A DEHYDROGENASE; ISOVALERYL COENZYME A DEHYDROGENASE; MEDIUM CHAIN ACYL COENZYME A DEHYDROGENASE; QUERCETIN; RIBOFLAVIN; UNCLASSIFIED DRUG;

ARTICLE; BUTYRYL COENZYME A DEHYDROGENASE DEFICIENCY; COMPLEX I DEFICIENCY; COMPLEX II DEFICIENCY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME STABILITY; FATTY ACID OXIDATION; HUMAN; MEDIUM CHAIN ACYL COENZYME A DEHYDROGENASE DEFICIENCY; MISSENSE MUTATION; MITOCHONDRIAL RESPIRATION; MULTIPLE ACYL COA DEHYDROGENASE DEFICIENCY; OXIDATION REDUCTION REACTION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RIBOFLAVIN DEFICIENCY; VITAMIN METABOLISM; VITAMIN SUPPLEMENTATION;

CARNITINE ACYLTRANSFERASES; HUMANS; MITOCHONDRIA; MULTIPLE ACYL COENZYME A DEHYDROGENASE DEFICIENCY; OXIDATION-REDUCTION; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; RIBOFLAVIN;

EID: 78650709553     PISSN: 09298673     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986710793205462     Document Type: Article

References (104)

1. Massey, V. The chemical and biological versatility of riboflavin. Biochem. Soc. Trans., 2000, 28(4), 283-96.
2. Muller, F. The flavin redox-system and its biological function In Radicals in Biochemistry, Boschke, F. L., Ed. Springer Berlin/Heidelberg 1983; Vol. 108.
3. Grosch, B. A. Food Chemistry. Second edition ed.; Springer: 1999.
4. Depeint, F.; Bruce, W. R.; Shangari, N.; Mehta, R.; O'Brien, P. J., Mitochondrial function and toxicity: role of the B vitamin family on mitochondrial energy metabolism. Chem. Biol. Interact., 2006, 163 (1-2), 94-112.
5. Yamamoto, S.; Inoue, K.; Ohta, K. Y.; Fukatsu, R.; Maeda, J. Y.; Yoshida, Y.; Yuasa, H. Identification and functional characterization of rat riboflavin transporter 2. J. Biochem., 2009, 145(4), 437-43.
6. Tzagoloff, A.; Jang, J.; Glerum, D. M.; Wu, M. FLX1 codes for a carrier protein involved in maintaining a proper balance of flavin nucleotides in yeast mitochondria. J. Biol. Chem., 1996, 271(13), 7392-7.
7. Spaan, A. N.; Ijlst, L.; van Roermund, C. W.; Wijburg, F. A.; Wanders, R. J.; Waterham, H. R. Identification of the human mitochondrial FAD transporter and its potential role in multiple acyl-CoA dehydrogenase deficiency. Mol. Genet. Metab., 2005, 86(4), 441-7.
8. Gregersen, N. Riboflavin-responsive defects of beta-oxidation. J. Inherit. Metab. Dis., 1985, 8 Suppl 1, 65-9.
9. Harpey, J. P.; Charpentier, C.; Goodman, S. I.; Darbois, Y.; Lefebvre, G.; Sebbah, J. Multiple acyl-CoA dehydrogenase deficiency occurring in pregnancy and caused by a defect in riboflavin metabolism in the mother. Study of a kindred with seven deaths in infancy: Value of riboflavin therapy in preventing this syndrome. J. Pediatr., 1983, 103(3), 394-8.
10. Chiong, M. A.; Sim, K. G.; Carpenter, K.; Rhead, W.; Ho, G.; Olsen, R. K.; Christodoulou, J. Transient multiple acyl-CoA dehydrogenation deficiency in a newborn female caused by maternal riboflavin deficiency. Mol. Genet. Metab., 2007, 92 (1-2), 109-14.
11. Rhead, W.; Roettger, V.; Marshall, T.; Amendt, B. Multiple acylcoenzyme A dehydrogenation disorder responsive to riboflavin: substrate oxidation, flavin metabolism, and flavoenzyme activities in fibroblasts. Pediatr. Res., 1993, 33(2), 129-35.
12. Hoppel, C.; DiMarco, J. P.; Tandler, B. Riboflavin and rat hepatic cell structure and function. Mitochondrial oxidative metabolism in deficiency states. J. Biol. Chem., 1979, 254(10), 4164-70.
13. Ross, N. S.; Hansen, T. P. Riboflavin deficiency is associated with selective preservation of critical flavoenzyme-dependent metabolic pathways. Biofactors, 1992, 3(3), 185-190.
14. Sakurai, T.; Miyazawa, S.; Furuta, S.; Hashimoto, T. Riboflavin deficiency and beta-oxidation systems in rat liver. Lipids, 1982, 17(9), 598-604.
15. Veitch, K.; Draye, J. P.; Vamecq, J.; Causey, A. G.; Bartlett, K.; Sherratt, H. S.; Van, H. F. Altered acyl-CoA metabolism in riboflavin deficiency. Biochim. Biophys. Acta, 1989, 1006(3), 335-343.
16. Ross, N. S.; Hoppel, C. L., Acyl-CoA dehydrogenase activity in the riboflavin-deficient rat. Effects of starvation. Biochem. J., 1987, 244(2), 387-91.
17. Veitch, K.; Draye, J. P.; Van Hoof, F.; Sherratt, H. S. Effects of riboflavin deficiency and clofibrate treatment on the five acyl-CoA dehydrogenases in rat liver mitochondria. Biochem. J., 1988, 254(2), 477-81.
18. Nagao, M.; Tanaka, K. FAD-dependent regulation of transcription, translation, post-translational processing, and post-processing stability of various mitochondrial acyl-CoA dehydrogenases and of electron transfer flavoprotein and the site of holoenzyme formation. J. Biol. Chem., 1992, 267(25), 17925-32.
19. Manthey, K. C.; Rodriguez-Melendez, R.; Hoi, J. T.; Zempleni, J. Riboflavin deficiency causes protein and DNA damage in HepG2 cells, triggering arrest in G1 phase of the cell cycle. J. Nutr. Biochem., 2006, 17(4), 250-6.
20. Tu, B. P.; Ho-Schleyer, S. C.; Travers, K. J.; Weissman, J. S. Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science, 2000, 290(5496), 1571-4.
21. Camporeale, G.; Zempleni, J. Oxidative folding of interleukin-2 is impaired in flavin-deficient jurkat cells, causing intracellular accumulation of interleukin-2 and increased expression of stress response genes. J. Nutr., 2003, 133(3), 668-72.
22. Manthey, K. C.; Chew, Y. C.; Zempleni, J. Riboflavin deficiency impairs oxidative folding and secretion of apolipoprotein B-100 in HepG2 cells, triggering stress response systems. J. Nutr., 2005, 135(5), 978-82.
23. Atamna, H. Heme, iron, and the mitochondrial decay of ageing. Ageing Res. Rev., 2004, 3(3), 303-18.
24. Fishman, S. M.; Christian, P.; West, K. P. The role of vitamins in the prevention and control of anaemia. Public Health Nutr., 2000, 3(2), 125-50.
25. Powers, H. J. Riboflavin (vitamin B-2) and health. Am. J. Clin. Nutr., 2003, 77(6), 1352-60.
26. Ghisla, S.; Massey, V. New flavins for old: artificial flavins as active site probes of flavoproteins. Biochem. J., 1986, 239(1), 1-12.
27. Edmondson, D.; Ghisla, S. Flavoenzyme structure and function. Approaches using flavin analogues. Methods Mol. Biol., 1999, 131, 157-79.
28. Susin, S. A.; Lorenzo, H. K.; Zamzami, N.; Marzo, I.; Snow, B. E.; Brothers, G. M.; Mangion, J.; Jacotot, E.; Costantini, P.; Loeffler, M.; Larochette, N.; Goodlett, D. R.; Aebersold, R.; Siderovski, D. P.; Penninger, J. M.; Kroemer, G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature, 1999, 397(6718), 441-6.
29. Ishikawa, T.; Matsumoto, A.; Kato, T., Jr.; Togashi, S.; Ryo, H.; Ikenaga, M.; Todo, T.; Ueda, R.; Tanimura, T. DCRY is a Drosophila photoreceptor protein implicated in light entrainment of circadian rhythm. Genes Cells, 1999, 4(1), 57-65.
30. Moore, E. G.; Ghisla, S.; Massey, V., Properties of flavins where the 8-methyl group is replaced by mercapto-residues. J. Biol. Chem., 1979, 254(17), 8173-8.
31. Massey, V.; Ghisla, S.; Moore, E. G. 8-Mercaptoflavins as active site probes of flavoenzymes. J. Biol. Chem., 1979, 254(19), 9640-50.
32. Joosten, V.; van Berkel, W. J. Flavoenzymes. Curr. Opin. Chem. Biol., 2007, 11(2), 195-202.
33. Mewies, M.; McIntire, W. S.; Scrutton, N. S. Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: the current state of affairs. Protein Sci., 1998, 7(1), 7-20.
34. Tam-Chang, S. W.; Mason, J.; Iverson, I.; Hwang, K. O.; Leonard, C. Modulating the pH-dependent redox potential of a flavin analog via incorporation into a self-assembled monolayer on gold. Chem. Commun., 1999(1), 65-66.
35. Mancini-Samuelson, G. J.; Kieweg, V.; Sabaj, K. M.; Ghisla, S.; Stankovich, M. T. Redox properties of human medium-chain acyl-CoA dehydrogenase, modulation by charged active-site amino acid residues. Biochemistry, 1998, 37(41), 14605-12.
36. Salazar, D.; Zhang, L.; deGala, G. D.; Frerman, F. E. Expression and characterization of two pathogenic mutations in human electron transfer flavoprotein. J. Biol. Chem., 1997, 272(42), 26425-33.
37. Paulsen, K. E.; Orville, A. M.; Frerman, F. E.; Lipscomb, J. D.; Stankovich, M. T. Redox properties of electron-transfer flavoprotein ubiquinone oxidoreductase as determined by EPR-spectroelectrochemistry. Biochemistry, 1992, 31(47), 11755-61.
38. Bartlett, K.; Eaton, S. Mitochondrial beta-oxidation. Eur. J. Biochem., 2004, 271(3), 462-9.
39. DiMauro, S.; DiMauro, P. M. Muscle carnitine palmityltransferase deficiency and myoglobinuria. Science, 1973, 182(115), 929-31.
40. Karpati, G.; Carpenter, S.; Engel, A. G.; Watters, G.; Allen, J.; Rothman, S.; Klassen, G.; Mamer, O. A. The syndrome of systemic carnitine deficiency. Clinical, morphologic, biochemical, and pathophysiologic features. Neurology, 1975, 25(1), 16-24.
41. Gregersen, N.; Lauritzen, R.; Rasmussen, K. Suberylglycine excretion in the urine from a patient with dicarboxylic aciduria. Clin. Chim. Acta, 1976, 70(3), 417-25.
42. Przyrembel, H.; Wendel, U.; Becker, K.; Bremer, H. J.; Bruinvis, L.; Ketting, D.; Wadman, S. K. Glutaric aciduria type II: report on a previously undescribed metabolic disorder. Clin. Chim. Acta, 1976, 66(2), 227-39.
43. Gregersen, N.; Andresen, B. S.; Corydon, M. J.; Corydon, T. J.; Olsen, R. K.; Bolund, L.; Bross, P. Mutation analysis in mitochondrial fatty acid oxidation defects: Exemplified by acyl-CoA dehydrogenase deficiencies, with special focus on genotypephenotype relationship. Hum. Mutat., 2001, 18(3), 169-89.
44. de Lonlay, P.; Giurgea, I.; Touati, G.; Saudubray, J. M. Neonatal hypoglycaemia: aetiologies. Semin. Neonatol., 2004, 9(1), 49-58.
45. Rinaldo, P.; Matern, D.; Bennett, M. J., Fatty acid oxidation disorders. Annu. Rev. Physiol., 2002, 64, 477-502.
46. Duran, M.; Cleutjens, C. B.; Ketting, D.; Dorland, L.; de Klerk, J. B.; van Sprang, F. J.; Berger, R. Diagnosis of medium-chain acyl-CoA dehydrogenase deficiency in lymphocytes and liver by a gas chromatographic method: the effect of oral riboflavin supplementation. Pediatr. Res., 1992, 31(1), 39-42.
47. Amendt, B. A.; Rhead, W. J. The multiple acyl-coenzyme A dehydrogenation disorders, glutaric aciduria type II and ethylmalonicadipic aciduria. Mitochondrial fatty acid oxidation, acyl-coenzyme A dehydrogenase, and electron transfer flavoprotein activities in fibroblasts. J. Clin. Invest., 1986, 78(1), 205-13.
48. Amendt, B. A.; Moon, A.; Teel, L.; Rhead, W. J. Long-chain acylcoenzyme A dehydrogenase deficiency: biochemical studies in fibroblasts from three patients. Pediatr. Res., 1988, 23(6), 603-605.
49. Dawson, D. B.; Waber, L.; Hale, D. E.; Bennett, M. J. Transient organic aciduria and persistent lacticacidemia in a patient with short-chain acyl-coenzyme A dehydrogenase deficiency. J. Pediatr., 1995, 126(1), 69-71.
50. Kmoch, S.; Zeman, J.; Hrebicek, M.; Ryba, L.; Kristensen, M. J.; Gregersen, N. Riboflavin-responsive epilepsy in a patient with SER209 variant form of short-chain acyl-CoA dehydrogenase. J. Inherit. Metab. Dis., 1995, 18(2), 227-229.
51. van Maldegem, B. T.; Duran, M.; Wanders, R. J.; Waterham, H. R.; Wijburg, F. A. Flavin adenine dinucleotide status and the effects of high-dose riboflavin treatment in short-chain acyl-CoA dehydrogenase deficiency. Pediatr. Res., 2010, 67(3), 304-308.
52. Pedersen, C. B.; Bross, P.; Winter, V. S.; Corydon, T. J.; Bolund, L.; Bartlett, K.; Vockley, J.; Gregersen, N. Misfolding, degradation, and aggregation of variant proteins. The molecular pathogenesis of short chain acyl-CoA dehydrogenase (SCAD) deficiency. J. Biol. Chem., 2003, 278(48), 47449-47458.
53. Corydon, M. J.; Gregersen, N.; Lehnert, W.; Ribes, A.; Rinaldo, P.; Kmoch, S.; Christensen, E.; Kristensen, T. J.; Andresen, B. S.; Bross, P.; Winter, V.; Martinez, G.; Neve, S.; Jensen, T. G.; Bolund, L.; Kolvraa, S. Ethylmalonic aciduria is associated with an amino acid variant of short chain acyl-coenzyme A dehydrogenase. Pediatr. Res., 1996, 39(6), 1059-1066.
54. Nagan, N.; Kruckeberg, K. E.; Tauscher, A. L.; Bailey, K. S.; Rinaldo, P.; Matern, D. The frequency of short-chain acyl-CoA dehydrogenase gene variants in the US population and correlation with the C (4)-acylcarnitine concentration in newborn blood spots. Mol. Genet. Metab., 2003, 78(4), 239-246.
55. Gregersen, N.; Andresen, B. S.; Pedersen, C. B.; Olsen, R. K.; Corydon, T. J.; Bross, P. Mitochondrial fatty acid oxidation defects-remaining challenges. J. Inherit. Metab. Dis., 2008, 31(5), 643-657.
56. Ames, B. N.; Elson-Schwab, I.; Silver, E. A. High-dose vitamin therapy stimulates variant enzymes with decreased coenzyme binding affinity (increased K (m)): relevance to genetic disease and polymorphisms. Am. J. Clin. Nutr., 2002, 75(4), 616-658.
57. Angelini, C.; Federico, A.; Reichmann, H.; Lombes, A.; Chinnery, P.; Turnbull, D. Task force guidelines handbook: EFNS guidelines on diagnosis and management of fatty acid mitochondrial disorders. Eur. J. Neurol., 2006, 13(9), 923-929.
58. al-Essa, M. A.; Rashed, M. S.; Bakheet, S. M.; Patay, Z. J.; Ozand, P. T. Glutaric aciduria type II: observations in seven patients with neonatal-and late-onset disease. J. Perinatol., 2000, 20(2), 120-128.
59. Frerman, F. E.; Goodman, S. I. Defects of electron transfer flavoprotein and electron transfer flavoprotein ubiquinone oxidoreductase; glutaric acidemia type II. In The metabolic and molecular bases of inherited diseases, Scriver, C. R.;.; Beaudet, A. L.; Sly, W. S.; Valle, D., Eds. McGraw-Hill: New York, 2001; pp. 2357-2365.
60. Bernsen, P. L.; Gabreels, F. J.; Ruitenbeek, W.; Sengers, R. C.; Stadhouders, A. M.; Renier, W. O. Successful treatment of pure myopathy, associated with complex I deficiency, with riboflavin and carnitine. Arch. Neurol., 1991, 48(3), 334-8.
61. Bernsen, P. L.; Gabreels, F. J.; Ruitenbeek, W.; Hamburger, H. L. Treatment of complex I deficiency with riboflavin. J. Neurol. Sci., 1993, 118(2), 181-7.
62. Griebel, V.; Krageloh-Mann, I.; Ruitenbeek, W.; Trijbels, J. M.; Paulus, W. A mitochondrial myopathy in an infant with lactic acidosis. Dev. Med. Child. Neurol., 1990, 32(6), 528-31.
63. Bugiani, M.; Lamantea, E.; Invernizzi, F.; Moroni, I.; Bizzi, A.; Zeviani, M.; Uziel, G. Effects of riboflavin in children with complex II deficiency. Brain Dev., 2006, 28(9), 576-81.
64. Pinard, J. M.; Marsac, C.; Barkaoui, E.; Desguerre, I.; Birch-Machin, M.; Reinert, P.; Ponsot, G. Leigh syndrome and leukodystrophy due to partial succinate dehydrogenase deficiency: regression with riboflavin. Arch. Pediatr., 1999, 6(4), 421-6.
65. Gregersen, N.; Wintzensen, H.; Christensen, S. K.; Christensen, M. F.; Brandt, N. J.; Rasmussen, K. C6-C10-dicarboxylic aciduria: investigations of a patient with riboflavin responsive multiple acyl-CoA dehydrogenation defects. Pediatr. Res., 1982, 16(10), 861-8.
66. Antozzi, C.; Garavaglia, B.; Mora, M.; Rimoldi, M.; Morandi, L.; Ursino, E.; DiDonato, S. Late-onset riboflavin-responsive myopathy with combined multiple acyl coenzyme A dehydrogenase and respiratory chain deficiency. Neurology, 1994, 44(11), 2153-2158.
67. 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.; Andersen, O.; Oldfors, A.; Holme, E.; Gregersen, N.; Turnbull, D. M.; Morris, A. A. ETFDH mutations as a major cause of riboflavin-responsive multiple acyl-CoA dehydrogenation deficiency. Brain, 2007, 130 (Pt 8), 2045-54.
68. Wen, B.; Dai, T.; Li, W.; Zhao, Y.; Liu, S.; Zhang, C.; Li, H.; Wu, J.; Li, D.; Yan, C. Riboflavin-responsive lipid-storage myopathy caused by ETFDH gene mutations. J. Neurol. Neurosurg. Psychiatry, 2010, 81(2), 231-236.
69. Vergani, L.; Barile, M.; Angelini, C.; Burlina, A. B.; Nijtmans, L.; Freda, M. P.; Brizio, C.; Zerbetto, E.; Dabbeni-Sala, F. Riboflavin therapy. Biochemical heterogeneity in two adult lipid storage myopathies. Brain, 1999, 122 (Pt 12), 2401-11.
70. Gianazza, E.; Vergani, L.; Wait, R.; Brizio, C.; Brambilla, D.; Begum, S.; Giancaspero, T. A.; Conserva, F.; Eberini, I.; Bufano, D.; Angelini, C.; Pegoraro, E.; Tramontano, A.; Barile, M. Coordinated and reversible reduction of enzymes involved in terminal oxidative metabolism in skeletal muscle mitochondria from a riboflavin-responsive, multiple acyl-CoA dehydrogenase deficiency patient. Electrophoresis, 2006, 27 (5-6), 1182-98.
71. Gempel, K.; Topaloglu, H.; Talim, B.; Schneiderat, P.; Schoser, B. G.; Hans, V. H.; Palmafy, B.; Kale, G.; Tokatli, A.; Quinzii, C.; Hirano, M.; Naini, A.; DiMauro, S.; Prokisch, H.; Lochmuller, H.; Horvath, R. The myopathic form of coenzyme Q10 deficiency is caused by mutations in the electron-transferring- flavoprotein dehydrogenase (ETFDH) gene. Brain, 2007, 130 (Pt 8), 2037-2044.
72. Liang, W. C.; Ohkuma, A.; Hayashi, Y. K.; Lopez, L. C.; Hirano, M.; Nonaka, I.; Noguchi, S.; Chen, L. H.; Jong, Y. J.; Nishino, I. ETFDH mutations, CoQ10 levels, and respiratory chain activities in patients with riboflavin-responsive multiple acyl-CoA dehydrogenase deficiency. Neuromuscul. Disord., 2009, 19(3), 212-216.
73. Law, L. K.; Tang, N. L.; Hui, J.; Fung, S. L.; Ruiter, J.; Wanders, R. J.; Fok, T. F.; Lam, C. W. Novel mutations in ETFDH gene in Chinese patients with riboflavin-responsive multiple acyl-CoA dehydrogenase deficiency. Clin. Chim. Acta, 2009, 404(2), 95-99.
74. Ishii, K.; Komaki, H.; Ohkuma, A.; Nishino, I.; Nonaka, I.; Sasaki, M. Central nervous system and muscle involvement in an adolescent patient with riboflavin-responsive multiple acyl-CoA dehydrogenase deficiency. Brain Dev., 2010, 32(8), 669-672.
75. Er, T. K.; Liang, W. C.; Chang, J. G.; Jong, Y. J. High resolution melting analysis facilitates mutation screening of ETFDH gene: applications in riboflavin-responsive multiple acyl-CoA dehydrogenase deficiency. Clin. Chim. Acta, 2010, 411 (9-10), 690-699.
76. Yotsumoto, Y.; Hasegawa, Y.; Fukuda, S.; Kobayashi, H.; Endo, M.; Fukao, T.; Yamaguchi, S. Clinical and molecular investigations of Japanese cases of glutaric acidemia type 2. Mol. Genet. Metab., 2008, 94(1), 61-67.
77. 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.; Ali, D. W.; Bennett, M. J.; Balice-Gordon, R. J. Mechanisms underlying metabolic and neural defects in zebrafish and human multiple acyl-CoA dehydrogenase deficiency (MADD). PLoS One, 2009, 4(12), e8329.
78. Turnbull, D. M.; Shepherd, I. M.; Ashworth, B.; Bartlett, K.; Johnson, M. A.; Cullen, M. J.; Jackson, S.; Sherratt, H. S. Lipid storage myopathy associated with low acyl-CoA dehydrogenase activities. Brain, 1988, 111 (Pt 4), 815-828.
79. DiDonato, S.; Gellera, C.; Peluchetti, D.; Uziel, G.; Antonelli, A.; Lus, G.; Rimoldi, M. Normalization of short-chain acylcoenzyme A dehydrogenase after riboflavin treatment in a girl with multiple acylcoenzyme A dehydrogenase-deficient myopathy. Ann. Neurol., 1989, 25(5), 479-484.
80. Peluchetti, D.; Antozzi, C.; Roi, S.; DiDonato, S.; Cornelio, F. Riboflavin responsive multiple acyl-CoA dehydrogenase deficiency: functional evaluation of recovery after high dose vitamin supplementation. J. Neurol. Sci., 1991, 105(1), 93-98.
81. Henriques, B. J.; Rodrigues, J. V.; Olsen, R. K.; Bross, P.; Gomes, C. M. Role of flavinylation in a mild variant of multiple acyl-CoA dehydrogenation deficiency: a molecular rationale for the effects of riboflavin supplementation. J. Biol. Chem., 2009, 284(7), 4222-9.
82. Lundemose, J. B.; Kolvraa, S.; Gregersen, N.; Christensen, E.; Gregersen, M. Fatty acid oxidation disorders as primary cause of sudden and unexpected death in infants and young children: an investigation performed on cultured fibroblasts from 79 children who died aged between 0-4 years. Mol. Pathol., 1997, 50(4), 212-217.
83. Olsen, R. K.; Pourfarzam, M.; Morris, A. A.; Dias, R. C.; Knudsen, I.; Andresen, B. S.; Gregersen, N.; Olpin, S. E. Lipid-storage myopathy and respiratory insufficiency due to ETFQO mutations in a patient with late-onset multiple acyl-CoA dehydrogenation deficiency. J. Inherit. Metab. Dis., 2004, 27(5), 671-678.
84. Curcoy, A.; Olsen, R. K.; Ribes, A.; Trenchs, V.; Vilaseca, M. A.; Campistol, J.; Osorio, J. H.; Andresen, B. S.; Gregersen, N. Lateonset form of beta-electron transfer flavoprotein deficiency. Mol. Genet. Metab., 2003, 78(4), 247-249.
85. Olsen, R. K.; Andresen, B. S.; Christensen, E.; Bross, P.; Skovby, F.; Gregersen, N. Clear relationship between ETF/ETFDH genotype and phenotype in patients with multiple acyl-CoA dehydrogenation deficiency. Hum. Mutat., 2003, 22(1), 12-23.
86. Bafunno, V.; Giancaspero, T. A.; Brizio, C.; Bufano, D.; Passarella, S.; Boles, E.; Barile, M. Riboflavin uptake and FAD synthesis in Saccharomyces cerevisiae mitochondria: involvement of the Flx1p carrier in FAD export. J. Biol. Chem., 2004, 279(1), 95-102.
87. Saijo, T.; Tanaka, K. Isoalloxazine ring of FAD is required for the formation of the core in the Hsp60-assisted folding of medium chain acyl-CoA dehydrogenase subunit into the assembly competent conformation in mitochondria. J. Biol. Chem., 1995, 270(4), 1899-907.
88. Sato, K.; Nishina, Y.; Shiga, K. Preparation of separated alpha and beta subunits of electron-transferring flavoprotein in unfolded forms and their restoration to the native holoprotein form. J. Biochem., 1994, 116(1), 147-55.
89. Bross, P.; Jespersen, C.; Jensen, T. G.; Andresen, B. S.; Kristensen, M. J.; Winter, V.; Nandy, A.; Krautle, F.; Ghisla, S.; Bolundi, L.; et al. Effects of two mutations detected in medium chain acyl-CoA dehydrogenase (MCAD)-deficient patients on folding, oligomer assembly, and stability of MCAD enzyme. and stability of MCAD enzyme. J. Biol. Chem., 1995, 270(17), 10284-90.
90. Bross, P.; Andresen, B. S.; Winter, V.; Krautle, F.; Jensen, T. G.; Nandy, A.; Kolvraa, S.; Ghisla, S.; Bolund, L.; Gregersen, N. Cooverexpression of bacterial GroESL chaperonins partly overcomes non-productive folding and tetramer assembly of E. coli-expressed human medium-chain acyl-CoA dehydrogenase (MCAD) carrying the prevalent disease-causing K304E mutation. Biochim. Biophys. Acta, 1993, 1182(3), 264-74.
91. Saijo, T.; Kim, J. J.; Kuroda, Y.; Tanaka, K. The roles of threonine-136 and glutamate-137 of human medium chain acyl-CoA dehydrogenase in FAD binding and peptide folding using site-directed mutagenesis: creation of an FAD-dependent mutant, T136D. Arch. Biochem. Biophys., 1998, 358(1), 49-57.
92. Andresen, B. S.; Bross, P.; Udvari, S.; Kirk, J.; Gray, G.; Kmoch, S.; Chamoles, N.; Knudsen, I.; Winter, V.; Wilcken, B.; Yokota, I.; Hart, K.; Packman, S.; Harpey, J. P.; Saudubray, J. M.; Hale, D. E.; Bolund, L.; Kolvraa, S.; Gregersen, N. The molecular basis of medium-chain acyl-CoA dehydrogenase (MCAD) deficiency in compound heterozygous patients: is there correlation between genotype and phenotype? Hum. Mol. Genet., 1997, 6(5), 695-707.
93. Kuchler, B.; Abdel-Ghany, A. G.; Bross, P.; Nandy, A.; Rasched, I.; Ghisla, S. Biochemical characterization of a variant human medium-chain acyl-CoA dehydrogenase with a disease-associated mutation localized in the active site. Biochem. J., 1999, 337 (Pt 2), 225-30.
94. Kieweg, V.; Krautle, F. G.; Nandy, A.; Engst, S.; Vock, P.; Abdel-Ghany, A. G.; Bross, P.; Gregersen, N.; Rasched, I.; Strauss, A.; Ghisla, S. Biochemical characterization of purified, human recombinant Lys304->Glu medium-chain acyl-CoA dehydrogenase containing the common disease-causing mutation and comparison with the normal enzyme. Eur. J. Biochem., 1997, 246(2), 548-56.
95. Sato, K.; Nishina, Y.; Shiga, K. In vitro refolding and unfolding of subunits of electron-transferring flavoprotein: characterization of the folding intermediates and the effects of FAD and AMP on the folding reaction. J. Biochem. (Tokyo), 1996, 120(2), 276-85.
96. Schiff, M.; Froissart, R.; Olsen, R. K.; Acquaviva, C.; Vianey-Saban, C. Electron transfer flavoprotein deficiency: functional and molecular aspects. Mol. Genet. Metab., 2006, 88(2), 153-158.
97. McAndrew, R. P.; Wang, Y.; Mohsen, A. W.; He, M.; Vockley, J.; Kim, J. J. Structural basis for substrate fatty acyl chain specificity: crystal structure of human very-long-chain acyl-CoA dehydrogenase. J. Biol. Chem., 2008, 283(14), 9435-43.
98. Lee, H. J.; Wang, M.; Paschke, R.; Nandy, A.; Ghisla, S.; Kim, J. J. Crystal structures of the wild type and the Glu376Gly/Thr255Glu mutant of human medium-chain acyl-CoA dehydrogenase: influence of the location of the catalytic base on substrate specificity. Biochemistry, 1996, 35(38), 12412-20.
99. Fu, Z.; Wang, M.; Paschke, R.; Rao, K. S.; Frerman, F. E.; Kim, J. J. Crystal structures of human glutaryl-CoA dehydrogenase with and without an alternate substrate: structural bases of dehydrogenation and decarboxylation reactions. Biochemistry, 2004, 43(30), 9674-84.
100. Dwyer, T. M.; Rao, K. S.; Goodman, S. I.; Frerman, F. E. Proton abstraction reaction, steady-state kinetics, and oxidation-reduction potential of human glutaryl-CoA dehydrogenase. Biochemistry, 2000, 39(37), 11488-99.
101. Tiffany, K. A.; Roberts, D. L.; Wang, M.; Paschke, R.; Mohsen, A. W.; Vockley, J.; Kim, J. J. Structure of human isovaleryl-CoA dehydrogenase at 2.6 A resolution: structural basis for substrate specificity. Biochemistry, 1997, 36(28), 8455-64.
102. Battaile, K. P.; Nguyen, T. V.; Vockley, J.; Kim, J. J. Structures of isobutyryl-CoA dehydrogenase and enzyme-product complex: comparison with isovaleryl-and short-chain acyl-CoA dehydrogenases. J. Biol. Chem., 2004, 279(16), 16526-34.
103. Roberts, D. L.; Frerman, F. E.; Kim, J. J. Three-dimensional structure of human electron transfer flavoprotein to 2.1-A resolution. Proc. Natl. Acad. Sci. U S A, 1996, 93(25), 14355-60.
104. Zhang, J.; Frerman, F. E.; Kim, J. J. Structure of electron transfer flavoprotein-ubiquinone oxidoreductase and electron transfer to the mitochondrial ubiquinone pool. Proc. Natl. Acad. Sci. U. S. A., 2006, 103(44), 16212-7.