Human FAD synthase (isoform 2): A component of the machinery that delivers FAD to apo-flavoproteins

FEBS Journal

Volumn 278, Issue 22, 2011, Pages 4434-4449

  Torchetti, Enza M ^a   Bonomi, Francesco ^b   Galluccio, Michele ^c   Gianazza, Elisabetta ^b   Giancaspero, Teresa A ^a   Iametti, Stefania ^b   Indiveri, Cesare ^c   Barile, Maria ^a,d  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF CALABRIA   (Italy)

^d CNR   (Italy)

Author keywords

conformational changes; FAD synthase; flavin binding; FMN adenylyltransferase; protein stability

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOPROTEIN; FAD SYNTHASE ISOFORM 2; FLAVINE ADENINE NUCLEOTIDE; FLAVINE MONONUCLEOTIDE; FLAVOPROTEIN; HISTIDINE; ISOENZYME; METAL; UNCLASSIFIED DRUG; ACYL COENZYME A DESATURASE; FADS2 PROTEIN, HUMAN; RECOMBINANT PROTEIN;

ARTICLE; CATALYSIS; CONTROLLED STUDY; COVALENT BOND; ENZYME ACTIVITY; ENZYME BINDING; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME RELEASE; ENZYME SYNTHESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN HYDROLYSIS; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TRANSPORT; TEMPERATURE DEPENDENCE; BINDING SITE; CHEMISTRY; CIRCULAR DICHROISM; FLUORESCENCE; HUMAN; KINETICS; METABOLISM; PROTEIN BINDING;

APOPROTEINS; BINDING SITES; CATALYSIS; CIRCULAR DICHROISM; FATTY ACID DESATURASES; FLAVIN MONONUCLEOTIDE; FLAVIN-ADENINE DINUCLEOTIDE; FLUORESCENCE; HUMANS; KINETICS; PROTEIN BINDING; RECOMBINANT PROTEINS;

EID: 80255129380     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08368.x     Document Type: Article

References (52)

1. Massey V, (2000) The chemical and biological versatility of riboflavin. Biochem Soc Trans 28, 283-296.
2. Joosten V, &, van Berkel WJ, (2007) Flavoenzymes. Curr Opin Chem Biol 11, 195-202. (Pubitemid 46528360)
3. Ghisla S, &, Massey V, (1989) Mechanisms of flavoprotein-catalyzed reactions. Eur J Biochem 181, 1-17. (Pubitemid 19120201)
4. Depeint F, Bruce WR, Shangari N, Mehta R, &, O'Brien PJ, (2006) Mitochondrial function and toxicity: role of B vitamins on the one-carbon transfer pathways. Chem Biol Interact 163, 113-132. (Pubitemid 44572216)
5. Powers HJ, (2003) Riboflavin (vitamin B-2) and health. Am J Clin Nutr 77, 1352-1360. (Pubitemid 39655265)
6. Heuts DP, Scrutton NS, McIntire WS, &, Fraaije MW, (2009) What's in a covalent bond? On the role and formation of covalently bound flavin cofactors. FEBS J 276, 3405-3427.
7. Mewies M, McIntire WS, &, Scrutton NS, (1998) Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: the current state of affairs. Protein Sci 7, 7-20. (Pubitemid 28133742)
8. Decker K, &, Brandsch R, (1991) Flavoproteins with a covalent histidyl(N3)-8 alpha-riboflavin linkage. Biofactors 3, 69-81.
9. Brizio C, Otto A, Brandsch R, Passarella S, &, Barile M, (2000) A protein factor of rat liver mitochondrial matrix involved in flavinylation of dimethylglycine dehydrogenase. Eur J Biochem 267, 4346-4354. (Pubitemid 30461066)
10. Hao HX, Khalimonchuk O, Schraders M, Dephoure N, Bayley JP, Kunst H, Devilee P, Cremers CW, Schiffman JD, Bentz BG, et al. (2009) SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 325, 1139-1142.
11. Ghezzi D, Goffrini P, Uziel G, Horvath R, Klopstock T, Lochmuller H, D'Adamo P, Gasparini P, Strom TM, Prokisch H, et al. (2009) SDHAF1, encoding a LYR complex-II specific assembly factor, is mutated in SDH-defective infantile leukoencephalopathy. Nat Genet 41, 654-656.
12. Rutter J, Winge DR, &, Schiffman JD, (2010) Succinate dehydrogenase-assembly, regulation and role in human disease. Mitochondrion 10, 393-401.
13. Giancaspero TA, Wait R, Boles E, &, Barile M, (2008) Succinate dehydrogenase flavoprotein subunit expression in Saccharomyces cerevisiae- involvement of the mitochondrial FAD transporter, Flx1p. FEBS J 275, 1103-1117. (Pubitemid 351342207)
14. Manthey KC, Rodriguez-Melendez R, Hoi JT, &, Zempleni J, (2006) Riboflavin deficiency causes protein and DNA damage in HepG2 cells, triggering arrest in G1 phase of the cell cycle. J Nutr Biochem 17, 250-256.
15. Bugiani M, Lamantea E, Invernizzi F, Moroni I, Bizzi A, Zeviani M, &, Uziel G, (2006) Effects of riboflavin in children with complex II deficiency. Brain Dev 28, 576-581. (Pubitemid 44293175)
16. Henriques BJ, Rodrigues JV, Olsen RK, Bross P, &, Gomes CM, (2009) 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 284, 4222-4229.
17. Gonzalez-Cabo P, Ros S, &, Palau F, (2010) Flavin adenine dinucleotide rescues the phenotype of frataxin deficiency. PLoS ONE 5, e8872.
18. 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.
19. Gianazza E, Vergani L, Wait R, Brizio C, Brambilla D, Begum S, Giancaspero TA, Conserva F, Eberini I, Bufano D, et al. (2006) 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 27, 1182-1198.
20. Efimov I, Kuusk V, Zhang X, &, McIntire WS, (1998) Proposed steady-state kinetic mechanism for Corynebacterium ammoniagenes FAD synthetase produced by Escherichia coli. Biochemistry 37, 9716-9723. (Pubitemid 28319616)
21. Solovieva IM, Tarasov KV, &, Perumov DA, (2003) Main physicochemical features of monofunctional flavokinase from Bacillus subtilis. Biochemistry (Mosc) 68, 177-181.
22. Wu M, Repetto B, Glerum DM, &, Tzagoloff A, (1995) Cloning and characterization of FAD1, the structural gene for flavin adenine dinucleotide synthetase of Saccharomyces cerevisiae. Mol Cell Biol 15, 264-271. (Pubitemid 24379923)
23. Leulliot N, Blondeau K, Keller J, Ulryck N, Quevillon-Cheruel S, &, van Tilbeurgh H, (2010) Crystal structure of yeast FAD synthetase (Fad1) in complex with FAD. J Mol Biol 398, 641-646.
24. Huerta C, Borek D, Machius M, Grishin NV, &, Zhang H, (2009) Structure and mechanism of a eukaryotic FMN adenylyltransferase. J Mol Biol 389, 388-400.
25. Brizio C, Galluccio M, Wait R, Torchetti EM, Bafunno V, Accardi R, Gianazza E, Indiveri C, &, Barile M, (2006) Over-expression in Escherichia coli and characterization of two recombinant isoforms of human FAD synthetase. Biochem Biophys Res Commun 344, 1008-1016. (Pubitemid 44304386)
26. Gerdes SY, Scholle MD, D'Souza M, Bernal A, Baev MV, Farrell M, Kurnasov OV, Daugherty MD, Mseeh F, Polanuyer BM, et al. (2002) From genetic footprinting to antimicrobial drug targets: examples in cofactor biosynthetic pathways. J Bacteriol 184, 4555-4572. (Pubitemid 34832584)
27. Torchetti EM, Brizio C, Colella M, Galluccio M, Giancaspero TA, Indiveri C, Roberti M, &, Barile M, (2010) Mitochondrial localization of human FAD synthetase isoform 1. Mitochondrion 10, 263-273.
28. Lin J, Diamanduros A, Chowdhury SA, Scelsa S, Latov N, &, Sadiq SA, (2009) Specific electron transport chain abnormalities in amyotrophic lateral sclerosis. J Neurol 256, 774-782.
29. Galluccio M, Brizio C, Torchetti EM, Ferranti P, Gianazza E, Indiveri C, &, Barile M, (2007) Over-expression in Escherichia coli, purification and characterization of isoform 2 of human FAD synthetase. Protein Expr Purif 52, 175-181. (Pubitemid 46038749)
30. Barile M, Brizio C, De Virgilio C, Delfine S, Quagliariello E, &, Passarella S, (1997) Flavin adenine dinucleotide and flavin mononucleotide metabolism in rat liver-the occurrence of FAD pyrophosphatase and FMN phosphohydrolase in isolated mitochondria. Eur J Biochem 249, 777-785. (Pubitemid 27479050)
31. Oka M, &, McCormick DB, (1987) Complete purification and general characterization of FAD synthetase from rat liver. J Biol Chem 262, 7418-7422.
32. Giancaspero TA, Locato V, de Pinto MC, De Gara L, &, Barile M, (2009) The occurrence of riboflavin kinase and FAD synthetase ensures FAD synthesis in tobacco mitochondria and maintenance of cellular redox status. FEBS J 276, 219-231.
33. Schrecker AW, &, Kornberg A, (1950) Reversible enzymatic synthesis of flavin-adenine dinucleotide. J Biol Chem 182, 795-803.
34. Giri KV, Rao NA, Cama HR, &, Kumar SA, (1960) Studies on flavinadenine dinucleotide-synthesizing enzyme in plants. Biochem J 75, 381-386.
35. Barile M, Valenti D, Passarella S, &, Quagliariello E, (1997) 3-Azido-3′-deoxythmidine uptake into isolated rat liver mitochondria and impairment of ADP/ATP translocator. Biochem Pharmacol 53, 913-920. (Pubitemid 27224270)
36. Hagihara T, Fujio T, &, Aisaka K, (1995) Cloning of FAD synthetase gene from Corynebacterium ammoniagenes and its application to FAD and FMN production. Appl Microbiol Biotechnol 42, 724-729.
37. McCormick DB, Oka M, Bowers-Komro DM, Yamada Y, &, Hartman HA, (1997) Purification and properties of FAD synthetase from liver. Methods Enzymol 280, 407-413. (Pubitemid 28182377)
38. Gomes B, &, McCormick DB, (1983) Purification and general characterization of FAD synthetase from rat liver. Proc Soc Exp Biol Med 172, 250-254. (Pubitemid 13143197)
39. Ye H, &, Rouault TA, (2010) Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease. Biochemistry 49, 4945-4956.
40. Bonomi F, Iametti S, Morleo A, Ta D, &, Vickery LE, (2008) Studies on the mechanism of catalysis of iron-sulfur cluster transfer from IscU[2Fe2S] by HscA/HscB chaperones. Biochemistry 47, 12795-12801.
41. Padovani D, &, Banerjee R, (2009) A rotary mechanism for coenzyme B(12) synthesis by adenosyltransferase. Biochemistry 48, 5350-5357.
42. Yamada Y, Merrill AH Jr, &, McCormick DB, (1990) Probable reaction mechanisms of flavokinase and FAD synthetase from rat liver. Arch Biochem Biophys 278, 125-130. (Pubitemid 20121883)
43. Sandoval FJ, Zhang Y, &, Roje S, (2008) Flavin nucleotide metabolism in plants: monofunctional enzymes synthesize FAD in plastids. J Biol Chem 283, 30890-30900.
44. Berthold H, Scanarini M, Abney CC, Frorath B, &, Northemann W, (1992) Purification of recombinant antigenic epitopes of the human 68-kDa (U1) ribonucleoprotein antigen using the expression system pH6EX3 followed by metal chelating affinity chromatography. Protein Expr Purif 3, 50-56.
45. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
46. Casalin P, Pollegioni L, Curti B, &, Pilone Simonetta M, (1991) A study on apoenzyme from Rhodotorula gracilisd-amino acid oxidase. Eur J Biochem 197, 513-517.
47. Bafunno V, Giancaspero TA, Brizio C, Bufano D, Passarella S, Boles E, &, Barile M, (2004) Riboflavin uptake and FAD synthesis in Saccharomyces cerevisiae mitochondria: involvement of the Flx1p carrier in FAD export. J Biol Chem 279, 95-102. (Pubitemid 38044803)
48. Barile M, Brizio C, Valenti D, De Virgilio C, &, Passarella S, (2000) The riboflavin/FAD cycle in rat liver mitochondria. Eur J Biochem 267, 4888-4900. (Pubitemid 30619481)
49. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
50. Brizio C, Brandsch R, Bufano D, Pochini L, Indiveri C, &, Barile M, (2004) Over-expression in Escherichia coli, functional characterization and refolding of rat dimethylglycine dehydrogenase. Protein Expr Purif 37, 434-442. (Pubitemid 39187982)
51. Gianazza E, (2009) Casting immobilized pH gradients. In The Protein Protocols Handbook (, Walker JR, ed.), pp. 305-322. Humana Press, Totowa, NJ.
52. Gianazza E, Giacon P, Sahlin B, &, Righetti PG, (1985) Non-linear pH courses with immobilized pH gradients. Electrophoresis 6, 53-56.