Succinate dehydrogenase flavoprotein subunit expression in Saccharomyces cerevisiae - Involvement of the mitochondrial FAD transporter, Flx1p

FEBS Journal

Volumn 275, Issue 6, 2008, Pages 1103-1117

  Giancaspero, Teresa A ^a   Wait, Robin ^b   Boles, Eckhard ^c   Barile, Maria ^a,d  

^a UNIVERSITY OF BARI   (Italy)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c GOETHE UNIVERSITY   (Germany)

^d NONE   (Italy)

Author keywords

Flavin; Flx1p; Mitochondrial FAD transporter; Post transcriptional control; Succinate dehydrogenase flavoprotein subunit

Indexed keywords

DIHYDROLIPOAMIDE DEHYDROGENASE; FLAVINE ADENINE NUCLEOTIDE; FLAVOPROTEIN; PROTEIN FLX1P; PROTEIN SUBUNIT; SUCCINATE DEHYDROGENASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; FLX1 GENE; GENE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REGULATORY SEQUENCE; SACCHAROMYCES CEREVISIAE; SDH1 GENE; TRANSCRIPTION REGULATION;

SACCHAROMYCES CEREVISIAE;

EID: 40349094993     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06270.x     Document Type: Article

References (61)

1. 1 McCormick DB (1989) Two interconnected B vitamins: riboflavin and pyridoxine. Physiol Rev 69, 1170–1198.
2. 2 Lipton SA & Bossy‐Wetzel E (2002) Duelling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 111, 147–150.
3. 3 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.
4. 4 Foraker AB, Khantwal CM & Swaan PW (2003) Current perspectives on the cellular uptake and trafficking of riboflavin. Adv Drug Deliv Rev 55, 1467–1483.
5. 5 Reihl P & Stolz J (2005) The monocarboxylate transporter homolog Mch5p catalyzes riboflavin (vitamin B2) uptake in Saccharomyces cerevisiae. J Biol Chem 280, 39809–39817.
6. 6 Perl M, Kearney EB & Singer TP (1976) Transport of riboflavin into yeast cells. J Biol Chem 25, 3221–3228.
7. 7 Koser SA (1968) Vitamin Requirements of Bacteria and Yeast. Charles C. Thomas, Springfield, IL.
8. 8 Stahmann KP, Revuelta JL & Seulberger H (2000) Three biotechnical processes using Ashbya gossypii, Candida famata, or Bacillus subtilis compete with chemical riboflavin production. Appl Microbiol Biotechnol 53, 509–516.
9. 9 Förster C, Revuelta JL & Krämer R (2001) Carrier‐mediated transport of riboflavin in Ashbya gossypii. Appl Microbiol Biotechnol 55, 85–89.
10. 10 Pallotta ML, Brizio C, Fratianni A, De Virgilio C, Barile M & Passarella S (1998) Saccharomyces cerevisiae mitochondria can synthesise FMN and FAD from externally added riboflavin and export them to the extramitochondrial phase. FEBS Lett 428, 245–249.
11. 11 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.
12. 12 Barile M, Passarella S, Bertoldi A & Quagliariello E (1993) Flavin adenine dinucleotide synthesis in isolated rat liver mitochondria caused by imported flavin mononucleotide. Arch Biochem Biophys 305, 442–447.
13. 13 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, 92–102.
14. 14 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.
15. 15 Tzagoloff A, Jang J, Glerum M & Wu M (1996) FLX1 codes for a carrier protein involved in maintaining a proper balance of flavin nucleotides in yeast mitochondria. J Biol Chem 271, 7392–7397.
16. 16 Dibrov E, Fu S & Lemire BD (1998) The Saccharomyces cerevisiae TCM62 gene encodes a chaperone necessary for the assembly of the mitochondrial succinate dehydrogenase (complex II). J Biol Chem 273, 32042–32048.
17. 17 Palmieri L, Vozza A, Agrimi G, De Marco V, Runswick MJ, Palmieri F & Walker JE (1999) Identification of the yeast mitochondrial transporter for oxaloacetate and sulfate. J Biol Chem 274, 22184–22190.
18. 18 Pastore D, Laus MN, Di Fonzo N & Passarella S (2002) Reactive oxygen species inhibit the succinate oxidation‐supported generation of membrane potential in wheat mitochondria. FEBS Lett 516, 15–19.
19. 19 Larsson C, Pahlman IL, Ansell R, Rigoulet M, Adler L & Gustafsson L (1998) The importance of the glycerol 3‐phosphate shuttle during aerobic growth of Saccharomyces cerevisiae. Yeast 14, 347–357.
20. 20 Lodi T, Alberti A, Guiard B & Ferrero I (1999) Regulation of the Saccharomyces cerevisiae DLD1 gene encoding the mitochondrial protein D‐lactate ferricytochrome c oxidoreductase by HAP1 and HAP2/3/4/5. Mol Gen Genet 262, 623–632.
21. 21 DeRisi JL, Iyer VR & Brown PO (1997) Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278, 680–686.
22. 22 Cereghino GP, Atencio DP, Saghbini M, Beiner J & Schleffer IE (1995) Glucose‐dependent turnover of the mRNAs encoding succinate dehydrogenase peptides in Saccharomyces cerevisiae: sequence elements in the 5′‐untranslated region of the Ip mRNA play a dominant role. Mol Biol Cell 6, 1125–1143.
23. 23 Robinson KM & Lemire BD (1996) Covalent attachment of FAD to the yeast succinate dehydrogenase flavoprotein requires import into mitochondria, presequence removal, and folding. J Biol Chem 271, 4055–4060.
24. 24 Lemire BD & Oyedotun KS (2002) The Saccharomyces cerevisiae mitochondrial succinate:ubiquinone oxidoreductase. Biochim Biophys Acta 1553, 102–116.
25. 25 de la Cruz BJ, Prieto S & Scheffler IE (2002) The role of the 5′ untranslated region (UTR) in glucose‐dependent mRNA decay. Yeast 19, 887–902.
26. 26 Buschlen S, Amillet JM, Guiard B, Fournier A, Marcireau C & Bolotin‐Fukuhara M (2003) The S. cerevisiae HAP complex, a key regulator of mitochondrial function, coordinates nuclear and mitochondrial gene expression. Comp Funct Genom 4, 37–46.
27. 27 Barile M, Valenti D, Brizio C, Quagliariello E & Passarella S (1998) Rat liver mitochondria can hydrolyse thiamine pyrophosphate to thiamine monophosphate which can cross the mitochondrial membrane in a carrier‐mediated process. FEBS Lett 435, 6–10.
28. 28 Trilisenco LV, Andreeva NA, Kulakovskaya TV, Vagabov VM & Kulaev IS (2003) Effect of inhibitors on polyphosphate metabolism in the yeast Saccharomyces cerevisiae under hypercompensation conditions. Biochemistry 68, 577–581.
29. 29 Robinson KM, von Kieckebusch‐Guck A & Lemire BD (1991) Isolation and characterization of a Saccharomyces cerevisiae mutant disrupted for the succinate dehydrogenase flavoprotein subunit. J Biol Chem 266, 21347–21350.
30. 30 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.
31. 31 Antozzi C, Garavaglia B, Mora M, Rimoldi M, Morandi L, Ursino E & DiDonato S (1994) Late‐onset riboflavin‐responsive myopathy with combined multiple acyl coenzyme A dehydrogenase and respiratory chain deficiency. Neurology 44, 2153–2158.
32. 32 Vergani L, Barile M, Angelini C, Burlina AB, Nijtmans L, Freda MP, Brizio C, Zerbetto E & Dabbeni‐Sala F (1999) Riboflavin therapy. Biochemical heterogeneity in two adult lipid storage myopathies. Brain 122, 2401–2411.
33. 33 Nagao M & Tanaka K (1992) 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 267, 17925–17932.
34. 34 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.
35. 35 Spaan AN, Ijlst L, van Roermund CWT, Wijburg FA, Wanders RJA & Waterham HR (2005) Identification of the human mitochondrial FAD transporter and its potential role in multiple acyl‐CoA dehydrogenase deficiency. Mol Genet Metab 86, 441–447.
36. 36 Zahedi RP, Sickmann A, Boehm AM, Winkler C, Zufall N, Schonfisch B, Guiard B, Pfanner N & Meisinger C (2006) Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins. Mol Biol Cell 17, 1436–1450.
37. 37 Langer T & Neupert W (1996) Regulated protein degradation in mitochondria. Experentia 52, 1069–1076.
38. 38 Arnold I & Langer T (2002) Membrane protein degradation by AAA proteases in mitochondria. Biochem Biophys Acta 1592, 89–96.
39. 39 Boles E & Andre B (2004) Role of transporter‐like sensors in glucose and amino‐acid signalling in yeast. In Molecular Mechanism Controlling Transmembrane Transport ( Boles E & Kramer R eds), pp. 121–153. Springer, Berlin, Germany.
40. 40 Holsbeeks I, Lagatie O, Van Nuland A, Van de Velde S & Thevelein JM (2004) The eukaryotic plasma membrane as a nutrient‐sensing device. Trends Biochem Sci 29, 556–564.
41. 41 Pirner HM & Stolz J (2006) Biotin sensing in Saccharomyces cerevisiae is mediated by a conserved DNA element and requires the activity of biotin‐protein ligase. J Biol Chem 281, 12381–12389.
42. 42 Weider M, Machnik A, Klebl F & Sauer N (2006) Vhr1p, a new transcription factor from budding yeast, regulates biotin‐dependent expression of VHT1 and BIO5. J Biol Chem 281, 13513–13524.
43. 43 Mojzita D & Hohmann S (2006) Pdc2 coordinates expression of the THI regulon in the yeast Saccharomyces cerevisiae. Mol Genet Genomics 276, 147–161.
44. 44 Huq MD, Tsai NP, Lin YP, Higgins L & Wei LN (2007) Vitamin B6 conjugation to nuclear corepressor RIP140 and its role in gene regulation. Nat Chem Biol 3, 161–165.
45. 45 Rodriguez‐Melendez R & Zempleni J (2003) Regulation of gene expression by biotin. J Nutr Biochem 14, 680–690.
46. 46 Oltean S & Banerjee R (2005) A B12‐responsive internal ribosome entry site (IRES) element in human methionine synthase. J Biol Chem 280, 32662–32668.
47. 47 Col B, Oltean S & Banerjee R (2007) Translational regulation of human methionine synthase by upstream open reading frames. Biochim Biophys Acta 1769, 532–540.
48. 48 Cliften P, Sudarsanam P, Desikan A, Fulton L, Fulton B, Majors J, Waterston R, Cohen BA & Johnston M. (2003) Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301, 71–76.
49. 49 Kellis M, Patterson N, Endrizzi M, Birren B & Lander ES (2003) Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423, 241–254.
50. 50 Boles E, de Jong‐Gubbels P & Pronk JT (1998) Identification and characterization of MAE1, the Saccharomyces cerevisiae structural gene encoding mitochondrial malic enzyme. J Bacteriol 80, 2875–2882.
51. 51 Güldener U, Heck S, Diedler T, Beinhauer J & Hegemann JH (1996) A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 24, 2519–2524.
52. 52 Gietz RD & Woods RA (2002) Transformation of yeast by lithium acetate/single‐stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350, 87–96.
53. 53 Huxley C, Greene D & Dunham I (1990) Rapid assessment of S. cerevisiae mating type by PCR. Trends Genet 6, 236.
54. 54 Bradford M (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.
55. 55 Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
56. 56 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.
57. 57 Makuc J, Paiva S, Schauen M, Kramer R, Andre B, Casal M, Leao C & Boles E (2001) The putative monocarboxylate permeases of the yeast Saccharomyces cerevisiae do not transport monocarboxylic acids across the plasma membrane. Yeast 18, 1131–1143.
58. 58 Horwitz JP, Chua J, Curby RJ, Tomson AJ, DaRooge MA, Fisher BE, Mauricio J & Klundt I (1964) Substrates for cytochemical demonstration of enzyme activity. I. some substituted 3‐indolyl‐beta‐d‐glycopyranosides. J Med Chem 7, 574–575.
59. 59 Brocklehurst KJ, Davies RA & Angius L (2004) Differences in regulatory properties between human and rat glucokinase regulatory protein. Biochem J 378, 693–697.
60. 60 Chelstowska A, Liu Z, Jia D, Amberg D & Butow RA (1999) Signalling between mitochondria and the nucleus regulates the expression of a new D‐lactate dehydrogenase activity in yeast. Yeast 15, 1377–1391.
61. 61 Roberti M, Bruni F, Loguercio Polosa P, Gadaleta MN & Cantatore P (2006) The Drosophila termination factor DmTTF regulates in vivo mitochondrial transcription. Nucleic Acids Res 34, 2109–2116.