Expression of the human atypical kinase ADCK3 rescues coenzyme Q biosynthesis and phosphorylation of Coq polypeptides in yeast coq8 mutants

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1811, Issue 5, 2011, Pages 348-360

  Xie, Letian X ^a   Hsieh, Edward J ^a,b   Watanabe, Shota ^a   Allan, Christopher M ^a   Chen, Jia Y ^a   Tran, Uyenphuong C ^a,c   Clarke, Catherine F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

2D IEF SDS PAGE; coenzyme Q; open reading frame; ORF; Q; two dimensional isoelectric focusing sodium dodecyl sulfate polyacrylamide gel electrophoresis

Indexed keywords

ADCK3 ENZYME; PHOSPHOTRANSFERASE; UBIQUINONE; UBIQUINONE 3P; UBIQUINONE 5P; UBIQUINONE 7P; UBIQUINONE 8P; UNCLASSIFIED DRUG;

ARTICLE; ENZYME PHOSPHORYLATION; ENZYME SYNTHESIS; FUNGAL GENE; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDES; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; UBIQUINONE;

SACCHAROMYCES CEREVISIAE;

EID: 79953795039     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2011.01.009     Document Type: Article

References (87)

1. S. Ghisla, and C. Thorpe Acyl-CoA dehydrogenases. A mechanistic overview Eur. J. Biochem. 271 2004 494 508
2. G. Lenaz, and A. De Santis A survey of the function and specificity of ubiquione in the mitochondrial respiratory chain G. Lenaz, Coenzyme Q 1985 John Wiley & Sons Chichester, U.K. 165 199
3. T.M. Hildebrandt, and M.K. Grieshaber Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria FEBS J. 275 2008 3352 3361 (Pubitemid 351813547)
4. S. Hill, K. Hirano, V.V. Shmanai, B.N. Marbois, D. Vidovic, A.V. Bekish, B. Kay, V. Tse, J. Fine, C.F. Clarke, and M.S. Shchepinov Isotope-reinforced polyunsaturated fatty acids protect yeast cells from oxidative stress Free Radic. Biol. Med. 50 2010 130 138
5. M. Bentinger, K. Brismar, and G. Dallner The antioxidant role of coenzyme Q Mitochondrion 7S 2007 S41 S50
6. L. Papucci, N. Schiavone, E. Witort, M. Donnini, A. Lapucci, A. Tempestini, L. Formigli, S. Zecchi-Orlandini, G. Orlandini, G. Carella, R. Brancato, and S. Capaccioli Coenzyme Q10 prevents apoptosis by inhibiting mitochondrial depolarization independently of its free radical scavenging property J. Biol. Chem. 278 2003 28220 28228 (Pubitemid 36900022)
7. L. Walter, H. Miyoshi, X. Leverve, P. Bernard, and E. Fontaine Regulation of the mitochondrial permeability transition pore by ubiquinone analogs. A progress report Free Radic. Res. 36 2002 405 412 (Pubitemid 35154089)
8. F. Devun, L. Walter, J. Belliere, C. Cottet-Rousselle, X. Leverve, and E. Fontaine Ubiquinone analogs: a mitochondrial permeability transition pore-dependent pathway to selective cell death PLoS ONE 5 2010 e11792
9. D.R. Green, and J.C. Reed Mitochondria and apoptosis Science 281 1998 1309 1312 (Pubitemid 28406816)
10. L. Azzolin, S. von Stockum, E. Basso, V. Petronilli, M.A. Forte, and P. Bernardi The mitochondrial permeability transition from yeast to mammals FEBS Lett. 584 2010 2504 2509
11. M. Kawamukai Biosynthesis and bioproduction of coenzyme Q10 by yeasts and other organisms Biotechnol. Appl. Biochem. 53 2009 217 226
12. R.E. Olson, and H. Rudney Biosynthesis of ubiquinone Vitam. Horm. 40 1983 1 43
13. B. Marbois, L.X. Xie, S. Choi, K. Hirano, K. Hyman, and C.F. Clarke para-Aminobenzoic acid is a precursor in coenzyme Q6 biosynthesis in Saccharomyces cerevisiae J. Biol. Chem. 285 2010 27827 27838
14. F. Pierrel, O. Hamelin, T. Douki, S. Kieffer-Jaquinod, U. Muhlenhoff, M. Ozeir, R. Lill, and M. Fontecave Involvement of mitochondrial ferredoxin and para-aminobenzoic acid in yeast coenzyme Q biosynthesis Chem. Biol. 17 2010 449 459
15. U.C. Tran, and C.F. Clarke Endogenous synthesis of coenzyme Q in eukaryotes Mitochondrion 7S 2007 S62 S71
16. B. Marbois, P. Gin, K.F. Faull, W.W. Poon, P.T. Lee, J. Strahan, J.N. Shepherd, and C.F. Clarke Coq3 and Coq4 define a polypeptide complex in yeast mitochondria for the biosynthesis of coenzyme Q J. Biol. Chem. 280 2005 20231 20238 (Pubitemid 40776719)
17. B. Marbois, P. Gin, M. Gulmezian, and C.F. Clarke The yeast Coq4 polypeptide organizes a mitochondrial protein complex essential for coenzyme Q biosynthesis Biochim. Biophys. Acta 1791 2009 69 75
18. E.J. Hsieh, P. Gin, M. Gulmezian, U.C. Tran, R. Saiki, B.N. Marbois, and C.F. Clarke Saccharomyces cerevisiae Coq9 polypeptide is a subunit of the mitochondrial coenzyme Q biosynthetic complex Arch. Biochem. Biophys. 463 2007 19 26 (Pubitemid 46879701)
19. S.L. Rea, B.H. Graham, E. Nakamaru-Ogiso, A. Kar, and M.J. Falk Bacteria, yeast, worms, and flies: exploiting simple model organisms to investigate human mitochondrial diseases Dev. Disabil. Res. Rev. 16 2010 200 218
20. 1 complex EMBO J. 10 1991 2023 2031 (Pubitemid 21905672)
21. G. Brasseur, G. Tron, G. Dujardin, P.P. Slonimski, and P. Brivet-Chevillotte The nuclear ABC1 gene is essential for the correct conformation and functioning of the cytochrome bc1 complex and the neighbouring complexes II and IV in the mitochondrial respiratory chain Eur. J. Biochem. 246 1997 103 111 (Pubitemid 27229675)
22. T.Q. Do, A.Y. Hsu, T. Jonassen, P.T. Lee, and C.F. Clarke A defect in coenzyme Q biosynthesis is responsible for the respiratory deficiency in Saccharomyces cerevisiae abc1 mutants J. Biol. Chem. 276 2001 18161 18168
23. E.J. Hsieh, J.B. Dinoso, and C.F. Clarke A tRNA(TRP) gene mediates the suppression of cbs2-223 previously attributed to ABC1/COQ8 Biochem. Biophys. Res. Commun. 317 2004 648 653 (Pubitemid 38452532)
24. D.R. Macinga, G.M. Cook, R.K. Poole, and P.N. Rather Identification and characterization of aarF, a locus required for production of ubiquinone in Providencia stuartii and Escherichia coli and for expression of 2′-N-acetyltransferase in P. stuartii J. Bacteriol. 180 1998 128 135 (Pubitemid 28023792)
25. W.W. Poon, D.E. Davis, H.T. Ha, T. Jonassen, P.N. Rather, and C.F. Clarke Identification of Escherichia coli ubiB, a gene required for the first monooxygenase step in ubiquinone biosynthesis J. Bacteriol. 182 2000 5139 5146
26. J. Mollet, A. Delahodde, V. Serre, D. Chretien, D. Schlemmer, A. Lombes, N. Boddaert, I. Desguerre, P. de Lonlay, H.O. de Baulny, A. Munnich, and A. Rotig CABC1 gene mutations cause ubiquinone deficiency with cerebellar ataxia and seizures Am. J. Hum. Genet. 82 2008 623 630 (Pubitemid 351735957)
27. C. Lagier-Tourenne, M. Tazir, L.C. Lopez, C.M. Quinzii, M. Assoum, N. Drouot, C. Busso, S. Makri, L. Ali-Pacha, T. Benhassine, M. Anheim, D.R. Lynch, C. Thibault, F. Plewniak, L. Bianchetti, C. Tranchant, O. Poch, S. DiMauro, J.L. Mandel, M.H. Barros, M. Hirano, and M. Koenig ADCK3, an ancestral kinase, is mutated in a form of recessive ataxia associated with coenzyme Q10 deficiency Am. J. Hum. Genet. 82 2008 661 672 (Pubitemid 351735958)
28. C.J. Leonard, L. Aravind, and E.V. Koonin Novel families of putative protein kinases in bacteria and archaea: evolution of the "eukaryotic" protein kinase superfamily Genome Res. 8 1998 1038 1047 (Pubitemid 28532492)
29. G. Manning, D.B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam The protein kinase complement of the human genome Science 298 2002 1912 1934 (Pubitemid 35425239)
30. A. Johnson, P. Gin, B.N. Marbois, E.J. Hsieh, M. Wu, M.H. Barros, C.F. Clarke, and A. Tzagoloff COQ9, a new gene required for the biosynthesis of coenzyme Q in Saccharomyces cerevisiae J. Biol. Chem. 280 2005 31397 31404 (Pubitemid 41291880)
31. M.H. Barros, A. Johnson, P. Gin, B.N. Marbois, C.F. Clarke, and A. Tzagoloff The Saccharomyces cerevisiae COQ10 gene encodes a START domain protein required for function of coenzyme Q in respiration J. Biol. Chem. 280 2005 42627 42635 (Pubitemid 43049221)
32. C. Busso, E.B. Tahara, R. Ogusucu, O. Augusto, J.R. Ferreira-Junior, A. Tzagoloff, A.J. Kowaltowski, and M.H. Barros Saccharomyces cerevisiae coq10 null mutants are responsive to antimycin A FEBS J. 2010
33. S. Padilla, U.C. Tran, M. Jimenez-Hidalgo, J.M. Lopez-Martin, A. Martin-Montalvo, C.F. Clarke, P. Navas, and C. Santos-Ocana Hydroxylation of demethoxy-Q6 constitutes a control point in yeast coenzyme Q6 biosynthesis Cell. Mol. Life Sci. 66 2009 173 186
34. A. Tauche, U. Krause-Buchholz, and G. Rodel Ubiquinone biosynthesis in Saccharomyces cerevisiae: the molecular organization of O-methylase Coq3p depends on Abc1p/Coq8p FEMS Yeast Res. 8 2008 1263 1275
35. C.J. Sippel, R.R. Goewert, F.N. Slachman, and R.E. Olson The regulation of ubiquinone-6 biosynthesis by Saccharomyces cerevisiae J. Biol. Chem. 258 1983 1057 1061 (Pubitemid 13139350)
36. D. Burke, D. Dawson, and T. Stearns Methods in Yeast Genetics 2000 Cold Spring Harbor Laboratory Press Plainview, NY
37. R.J. Barkovich, A. Shtanko, J.A. Shepherd, P.T. Lee, D.C. Myles, A. Tzagoloff, and C.F. Clarke Characterization of the COQ5 gene from Saccharomyces cerevisiae. Evidence for a C-methyltransferase in ubiquinone biosynthesis J. Biol. Chem. 272 1997 9182 9188 (Pubitemid 27154925)
38. R. Elble A simple and efficient procedure for transformation of yeasts Biotechniques 13 1992 18 20
39. S.H. Ackerman, J. Martin, and A. Tzagoloff Characterization of ATP11 and detection of the encoded protein in mitochondria of Saccharomyces cerevisiae J. Biol. Chem. 267 1992 7386 7394
40. D.M. Glerum, T.J. Koerner, and A. Tzagoloff Cloning and characterization of COX14, whose product is required for assembly of yeast cytochrome oxidase J. Biol. Chem. 270 1995 15585 15590
41. A.Y. Hsu, W.W. Poon, J.A. Shepherd, D.C. Myles, and C.F. Clarke Complementation of coq3 mutant yeast by mitochondrial targeting of the Escherichia coli UbiG polypeptide: evidence that UbiG catalyzes both O-methylation steps in ubiquinone biosynthesis Biochemistry 35 1996 9797 9806 (Pubitemid 26302994)
42. B. Cormack Directed mutagenesis using the polymerase chain reaction V.B. Chanda, Current Protocols in Molecular Biology vol. 1 1997 John Wiley & Sons 8.5.1 8.5.10
43. B.S. Glick, and L.A. Pon Isolation of highly purified mitochondria from Saccharomyces cerevisiae Meth. Enzymol. 260 1995 213 223
44. 2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism Cell 69 1992 809 822
45. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
46. T. Jonassen, and C.F. Clarke Isolation and functional expression of human COQ3, a gene encoding a methyltransferase required for ubiquinone biosynthesis J. Biol. Chem. 275 2000 12381 12387 (Pubitemid 30241377)
47. M. Jasinski, D. Sudre, G. Schansker, M. Schellenberg, S. Constant, E. Martinoia, and L. Bovet AtOSA1, a member of the Abc1-like family, as a new factor in cadmium and oxidative stress response Plant Physiol. 147 2008 719 731 (Pubitemid 352844319)
48. G.I. Belogrudov, P.T. Lee, T. Jonassen, A.Y. Hsu, P. Gin, and C.F. Clarke Yeast COQ4 encodes a mitochondrial protein required for coenzyme Q synthesis Arch. Biochem. Biophys. 392 2001 48 58 (Pubitemid 32721613)
49. Y. Fujiki, A.L. Hubbard, S. Fowler, and P.B. Lazarow Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum J. Cell Biol. 93 1982 97 102 (Pubitemid 12117045)
50. M.P. Kamps, and B.M. Sefton Neither arginine nor histidine can carry out the function of lysine-295 in the ATP-binding site of p60src Mol. Cell. Biol. 6 1986 751 757 (Pubitemid 16135940)
51. S.K. Hanks, and T. Hunter Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification FASEB J. 9 1995 576 596
52. P. Gin, and C.F. Clarke Genetic evidence for a multi-subunit complex in coenzyme Q biosynthesis in yeast and the role of the Coq1 hexaprenyl diphosphate synthase J. Biol. Chem. 280 2005 2676 2681 (Pubitemid 40189372)
53. U.C. Tran, B. Marbois, P. Gin, M. Gulmezian, T. Jonassen, and C.F. Clarke Complementation of Saccharomyces cerevisiae coq7 mutants by mitochondrial targeting of the Escherichia coli UbiF polypeptide: two functions of yeast Coq7 polypeptide in coenzyme Q biosynthesis J. Biol. Chem. 281 2006 16401 16409
54. A. Tzagoloff, and C.L. Dieckmann PET genes of Saccharomyces cerevisiae Microbiol. Rev. 54 1990 211 225
55. A. Tzagoloff, A. Akai, and R.B. Needleman Assembly of the mitochondrial membrane system. Characterization of nuclear mutants of Saccharomyces cerevisiae with defects in mitochondrial ATPase and respiratory enzymes J. Biol. Chem. 250 1975 8228 8235
56. A. Tzagoloff, A. Akai, R.B. Needleman, and G. Zulch Assembly of the mitochondrial membrane system. Cytoplasmic mutants of Saccharomyces cerevisiae with lesions in enzymes of the respiratory chain and in the mitochondrial ATPase J. Biol. Chem. 250 1975 8236 8242
57. Z. Vajo, L.M. King, T. Jonassen, D.J. Wilkin, N. Ho, A. Munnich, C.F. Clarke, and C.A. Francomano Conservation of the Caenorhabditis elegans timing gene clk-1 from yeast to human: a gene required for ubiquinone biosynthesis with potential implications for aging Mamm. Genome 10 1999 1000 1004 (Pubitemid 29470942)
58. S.W. Baba, G.I. Belogrudov, J.C. Lee, P.T. Lee, J. Strahan, J.N. Shepherd, and C.F. Clarke Yeast coq5 C-methyltransferase is required for stability of other polypeptides involved in coenzyme Q biosynthesis J. Biol. Chem. 279 2004 10052 10059 (Pubitemid 38372608)
59. E.J. Hsieh Characterization of the Coenzyme Q Biosynthetic Genes ABC1/COQ8 and COQ9 in Yeast Saccharomyces cerevisiae Chemistry and Biochemistry 2006 University of California Los Angeles, Los Angeles 126
60. S. Facchin, R. Lopreiato, S. Stocchetto, G. Arrigoni, L. Cesaro, O. Marin, G. Carignani, and L.A. Pinna Structure-function analysis of yeast piD261/Bud32, an atypical protein kinase essential for normal cell life Biochem. J. 364 2002 457 463 (Pubitemid 34620806)
61. M. Spitaler, A. Villunger, H. Grunicke, and F. Uberall Unique structural and functional properties of the ATP-binding domain of atypical protein kinase C-iota J. Biol. Chem. 275 2000 33289 33296
62. S.S. Taylor, E. Radzio-Andzelm, and T. Hunter How do protein kinases discriminate between serine/threonine and tyrosine? Structural insights from the insulin receptor protein-tyrosine kinase FASEB J. 9 1995 1255 1266
63. L.N. Johnson, E.D. Lowe, M.E. Noble, and D.J. Owen The Eleventh Datta Lecture. The structural basis for substrate recognition and control by protein kinases FEBS Lett. 430 1998 1 11 (Pubitemid 28307022)
64. S.K. Hanks Genomic analysis of the eukaryotic protein kinase superfamily: a perspective Genome Biol. 4 2003 111
65. S.K. Hanks, A.M. Quinn, and T. Hunter The protein kinase family: conserved features and deduced phylogeny of the catalytic domains Science 241 1988 42 52
66. O. Delumeau, S. Dutta, M. Brigulla, G. Kuhnke, S.W. Hardwick, U. Volker, M.D. Yudkin, and R.J. Lewis Functional and structural characterization of RsbU, a stress signaling protein phosphatase 2C J. Biol. Chem. 279 2004 40927 40937 (Pubitemid 39287692)
67. A.C. Olivier, S. Lemaire, F. Van Bambeke, P.M. Tulkens, and E. Oldfield Role of rsbU and staphyloxanthin in phagocytosis and intracellular growth of Staphylococcus aureus in human macrophages and endothelial cells J. Infect. Dis. 200 2009 1367 1370
68. J.H. Shin, M.S. Brody, and C.W. Price Physical and antibiotic stresses require activation of the RsbU phosphatase to induce the general stress response in Listeria monocytogenes Microbiology 156 2010 2660 2669
69. A. Chi, C. Huttenhower, L.Y. Geer, J.J. Coon, J.E. Syka, D.L. Bai, J. Shabanowitz, D.J. Burke, O.G. Troyanskaya, and D.F. Hunt Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry Proc. Natl Acad. Sci. USA 104 2007 2193 2198 (Pubitemid 46391374)
70. C. Stark, T.C. Su, A. Breitkreutz, P. Lourenco, M. Dahabieh, B.J. Breitkreutz, M. Tyers, I. Sadowski, PhosphoGRID: a database of experimentally verified in vivo protein phosphorylation sites from the budding yeast Saccharomyces cerevisiae, Database (Oxford) 2010 (2010) bap026.
71. M.A. Zampol, C. Busso, F. Gomes, J.R. Ferreira-Junior, A. Tzagoloff, and M.H. Barros Over-expression of COQ10 in Saccharomyces cerevisiae inhibits mitochondrial respiration Biochem. Biophys. Res. Commun. 402 2010 82 87
72. 1 complex Cancer Res. 62 2002 1246 1250 (Pubitemid 34407771)
73. M. Gerards, B. van den Bosch, C. Calis, K. Schoonderwoerd, K. van Engelen, M. Tijssen, R. de Coo, A. van der Kooi, and H. Smeets Nonsense mutations in CABC1/ADCK3 cause progressive cerebellar ataxia and atrophy Mitochondrion 10 2010 510 515
74. C.M. Quinzii, and M. Hirano Coenzyme Q and mitochondrial disease Dev. Disabil. Res. Rev. 16 2010 183 188
75. R. Saiki, A.L. Lunceford, Y. Shi, B. Marbois, R. King, J. Pachuski, M. Kawamukai, D.L. Gasser, and C.F. Clarke Coenzyme Q10 supplementation rescues renal disease in Pdss2kd/kd mice with mutations in prenyl diphosphate synthase subunit 2 Am. J. Physiol. Ren. Physiol. 295 2008 F1535 F1544
76. B. Cardazzo, P. Hamel, W. Sakamoto, H. Wintz, and G. Dujardin Isolation of an Arabidopsis thaliana cDNA by complementation of a yeast abc1 deletion mutant deficient in complex III respiratory activity Gene 221 1998 117 125 (Pubitemid 28529615)
77. A.J. Ytterberg, J.B. Peltier, and K.J. van Wijk Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes Plant Physiol. 140 2006 984 997 (Pubitemid 43956251)
78. J.E. McEwen, C. Ko, B. Kloeckner-Gruissem, and R.O. Poyton Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae. Characterization of mutants in 34 complementation groups J. Biol. Chem. 261 1986 11872 11879 (Pubitemid 17206116)
79. R.S. Sikorski, and P. Hieter A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae Genetics 122 1989 19 27
80. T.W. Christianson, R.S. Sikorski, M. Dante, J.H. Shero, and P. Hieter Multifunctional yeast high-copy-number shuttle vectors Gene 110 1992 119 122
81. A.Y. Hsu, W.W. Poon, J.A. Shepherd, D.C. Myles, and C.F. Clarke Complementation of coq3 mutant yeast by mitochondrial targeting of the Escherichia coli UbiG polypeptide: evidence that UbiG catalyzes both O-methylation steps in ubiquinone biosynthesis Biochemistry 35 1996 9797 9806 (Pubitemid 26302994)
82. T.Q. Do, A.Y. Hsu, T. Jonassen, P.T. Lee, and C.F. Clarke A defect in coenzyme Q biosynthesis is responsible for the respiratory deficiency in Saccharomyces cerevisiae abc1 mutants J. Biol. Chem. 276 2001 18161 18168
83. W.J. Chen, and M.G. Douglas Phosphodiester bond cleavage outside mitochondria is required for the completion of protein import into the mitochondrial matrix Cell 49 1987 651 658
84. G. Daum, P.C. Bohni, and G. Schatz Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria J. Biol. Chem. 257 1982 13028 13033
85. A. Ohashi, J. Gibson, I. Gregor, and G. Schatz Import of proteins into mitochondria. The precursor of cytochrome c1 is processed in two steps, one of them heme-dependent J. Biol. Chem. 257 1982 13042 13047
86. L.M. Thompson, and L. McAlister-Henn Dispensable presequence for cellular localization and function of mitochondrial malate dehydrogenase from Saccharomyces cerevisiae J. Biol. Chem. 264 1989 12091 12096 (Pubitemid 19185385)
87. D.S. Reading, R.L. Hallberg, and A.M. Myers Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor Nature 337 1989 655 659