Drosophila sbo regulates lifespan through its function in the synthesis of coenzyme Q in vivo

Journal of Genetics and Genomics

Volumn 38, Issue 6, 2011, Pages 225-234

  Liu, Jiyong ^a,b   Wu, Qinghua ^a,b   He, Dianlu ^a   Ma, Tengyu ^a   Du, Li ^a   Dui, Wen ^a,b   Guo, Xiaoyan ^a,c   Jiao, Renjie ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Coenzyme Q; Drosophila; Insulin signaling; Lifespan; Sbo

Indexed keywords

4 HYDROXYBENZOIC ACID; INSULIN; ISOPRENOID; SOMATOMEDIN; UBIDECARENONE; UBIQUINONE;

ALLELE; ARTICLE; BIOSYNTHESIS; CATALYSIS; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE; GENE EXPRESSION; GENETIC CODE; HETEROZYGOTE; HUMAN; IN VIVO STUDY; LETHALITY; LIFE EXTENSION; LIFESPAN; MALE; MOLECULAR BIOLOGY; MUTANT; MUTATION; NONHUMAN; PREDICTION; PRENYLATION; PROKARYOTE; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SMALL BOY GENE; SYNTHESIS;

ALKYL AND ARYL TRANSFERASES; AMINO ACID SEQUENCE; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; HUMANS; LARVA; LONGEVITY; MALE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; PARABENS; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; UBIQUINONE;

ANIMALIA; EUKARYOTA; PROKARYOTA;

EID: 79959380753     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2011.05.002     Document Type: Article

References (50)

1. Artuch R., Salviati L., Jackson S., Hirano M., Navas P. Coenzyme Q10 deficiencies in neuromuscular diseases. Adv. Exp. Med. Biol. 2009, 652:117-128.
2. Ashby M.N., Kutsunai S.Y., Ackerman S., Tzagoloff A., Edwards P.A. COQ2 is a candidate for the structural gene encoding para-hydroxybenzoate: polyprenyltransferase. J. Biol. Chem. 1992, 267:4128-4136.
3. Bader M., Muse W., Ballou D.P., Gassner C., Bardwell J.C.A. Oxidative protein folding is driven by the electron transport system. Cell 1999, 98:217-227.
4. Battino M., Gorini A., Villa R.F., Genova M.L., Bovina C., Sassi S., Littarru G.P., Lenaz G. Coenzyme Q content in synaptic and non-synaptic mitochondria from different brain regions in the ageing rat. Mech. Ageing Dev. 1995, 78:173-187.
5. Bauer J.H., Chang C., Morris S.N.S., Hozier S., Andersen S., Waitzman J.S., Helfand S.L. Expression of dominant-negative Dmp53 in the adult fly brain inhibits insulin signaling. Proc. Natl. Acad. Sci. USA 2007, 104:13355-13360.
6. Beyer R.E., Burnett B.A., Cartwright K.J., Edington D.W., Falzon M.J., Kreitman K.R., Kuhn T.W., Ramp B.J., Rhee S.Y., Rosenwasser M.J., Stein M., An L.C. Tissue coenzyme Q (ubiquinone) and protein concentrations over the life span of the laboratory rat. Mech. Ageing Dev. 1985, 32:267-281.
7. Bohni R., Riesgo-Escovar J., Oldham S., Brogiolo W., Stocker H., Andruss B.F., Beckingham K., Hafen E. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 1999, 97:865-875.
8. Britton J.S., Lockwood W.K., Li L., Cohen S.M., Edgar B.A. Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2002, 2:239-249.
9. Clancy D.J., Gems D., Harshman L.G., Oldham S., Stocker H., Hafen E., Leevers S.J., Partridge L. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 2001, 292:104-106.
10. Copeland J.M., Cho J., Lo T., Hur J.H., Bahadorani S., Arabyan T., Rabie J., Soh J., Walker D.W. Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain. Curr. Biol. 2009, 19:1591-1598.
11. Crane F.L., Hatefi Y., Lester R.L., Widmer C. Isolation of a quinone from beef heart mitochondria. Biochim. Biophys. Acta 1957, 25:220-221.
12. Cristina D., Cary M., Lunceford A., Clarke C., Kenyon C. A regulated response to impaired respiration slows behavioral rates and increases lifespan in Caenorhabditis elegans. PLoS Genet. 2009, 5:e1000450.
13. Dillin A., Hsu A.L., Arantes-Oliveira N.A., Lehrer-Graiwer J., Hsin H., Fraser A.G., Kamath R.S., Ahringer J., Kenyon C. Rates of behavior and aging specified by mitochondrial function during development. Science 2002, 298:2398-2401.
14. Edgar B.A. How flies get their size: genetics meets physiology. Nat. Rev. Genet. 2006, 7:907-916.
15. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300:1005-1016.
16. Ernster L., Dallner G. Biochemical, physiological and medical aspects of ubiquinone function. Biochim. Biophys. Acta 1995, 1271:195-204.
17. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature 2000, 404:394-398.
18. Feng J.L., Bussiere F., Hekimi S. Mitochondrial electron transport is a key determinant of life span in Caenorhabditis elegans. Dev. Cell 2001, 1:633-644.
19. Finn R.D., Mistry J., Tate J., Coggill P., Heger A., Pollington J.E., Gavin O.L., Gunasekaran P., Ceric G., Forslund K., Holm L., Sonnhammer E.L.L., Eddy S.R., Bateman A. The Pfam protein families database. Nucleic Acids Res. 2010, 38:D211-D222.
20. Forsgren M., Attersand A., Lake S., Grunler J., Swiezewska E., Dallner G., Climent I. Isolation and functional expression of human COQ2, a gene encoding a polyprenyl transferase involved in the synthesis of CoQ. Biochem. J. 2004, 382:519-526.
21. Fuss B., Becker T., Zinke I., Hoch M. The cytohesin Steppke is essential for insulin signalling in Drosophila. Nature 2006, 444:945-948.
22. Ganetzky B., Flanagan J.R. On the relationship between senescence and age-related changes in two wild-type strains of Drosophila melanogaster. Exp. Gerontol. 1978, 13:189-196.
23. Gargano J.W., Martin I., Bhandari P., Grotewiel M.S. Rapid iterative negative geotaxis (RING): a new method for assessing age-related locomotor decline in Drosophila. Exp. Gerontol. 2005, 40:386-395.
24. Hyun S., Lee J.H., Jin H., Nam J., Namkoong B., Lee G., Chung J., Kim V.N. Conserved microRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 2009, 139:1096-1108.
25. Ishii N., Senoo-Matsuda N., Miyake K., Yasuda K., Ishii T., Hartman P.S., Furukawa S. Coenzyme Q10 can prolong C. elegans lifespan by lowering oxidative stress. Mech. Ageing Dev. 2004, 125:41-46.
26. Jonassen T., Clarke C.F. Isolation and functional expression of human COQ3, a gene encoding a methyltransferase required for ubiquinone biosynthesis. J. Biol. Chem. 2000, 275:12381-12387.
27. Jonassen T., Larsen P.L., Clarke C.F. A dietary source of coenzyme Q is essential for growth of long-lived Caenorhabditis elegans clk-1 mutants. Proc. Natl. Acad. Sci. USA 2001, 98:421-426.
28. Kalen A., Appelkvist E.L., Dallner G. Age-related changes in the lipid compositions of rat and human tissues. Lipids 1989, 24:579-584.
29. Kawamukai M. Biosynthesis and bioproduction of coenzyme Q10 by yeasts and other organisms. Biotechnol. Appl. Biochem. 2009, 53:217-226.
30. Larsen P.L., Clarke C.F. Extension of life-span in Caenorhabditis elegans by a diet lacking coenzyme Q. Science 2002, 295:120-123.
31. Lass A., Kwong L., Sohal R.S. Mitochondrial coenzyme Q content and aging. Biofactors 1999, 9:199-205.
32. Levavasseur F., Miyadera H., Sirois J., Tremblay M.L., Kita K., Shoubridge E., Hekimi S. Ubiquinone is necessary for mouse embryonic development but is not essential for mitochondrial respiration. J. Biol. Chem. 2001, 276:46160-46164.
33. Liu X.X., Jiang N., Hughes B., Bigras E., Shoubridge E., Hekimi S. Evolutionary conservation of the clk-1-dependent mechanism of longevity: loss of mclk1 increases cellular fitness and lifespan in mice. Gene Dev. 2005, 19:2424-2434.
34. Palmer M.R., Sackton T.B. The effects of dietary coenzyme Q on Drosophila life span. Aging Cell 2003, 2:335-339.
35. Park J., Lee S.B., Lee S., Kim Y., Song S., Kim S., Bae E., Kim J., Shong M., Kim J.-M., Chung J. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 2006, 441:1157-1161.
36. Pepe S., Marasco S.F., Haas S.J., Sheeran F.L., Krum H., Rosenfeldt F.L. Coenzyme Q10 in cardiovascular disease. Mitochondrion 2007, 7(Suppl.):S154-S167.
37. Rera M., Monnier V., Tricoire H. Mitochondrial electron transport chain dysfunction during development does not extend lifespan in Drosophila melanogaster. Mech. Ageing Dev. 2010, 131:156-164.
38. Sacconi S., Trevisson E., Salviati L., Aymé S., Rigal O., Garcia Redondo A., Mancuso M., Siciliano G., Tonin P., Angelini C., Auré K., Lombès A., Desnuelle C. Coenzyme Q10 is frequently reduced in muscle of patients with mitochondrial myopathy. Neuromuscular Disord. 2010, 20:44-48.
39. Samuelson A.V., Carr C.E., Ruvkun G. Gene activities that mediate increased life span of C. elegans insulin-like signaling mutants. Gene Dev. 2007, 21:2976-2994.
40. Slack C., Werz C., Wieser D., Alic N., Foley A., Stocker H., Withers D.J., Thornton J.M., Hafen E., Partridge L. Regulation of lifespan, metabolism, and stress responses by the Drosophila SH2B protein, Lnk. PLoS Genet. 2010, 6:e1000881.
41. Sohal R.S., Forster M.J. Coenzyme Q, oxidative stress and aging. Mitochondrion 2007, 7(Suppl.):S103-S111.
42. Sonnhammer E.L., von Heijne G., Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 1998, 6:175-182.
43. Suzuki K., Okada K., Kamiya Y., Zhu X.F., Nakagawa T., Kawamukai M., Matsuda H. Analysis of the decaprenyl diphosphate synthase (dps) gene in fission yeast suggests a role of ubiquinone as an antioxidant. J. Biochem. 1997, 121:496-505.
44. Taguchi A., White M.F. Insulin-like signaling, nutrient homeostasis, and life span. Annu. Rev. Physiol. 2008, 70:191-212.
45. Turunen M., Olsson J., Dallner G. Metabolism and function of coenzyme Q. Biochim. Biophys. Acta 2004, 1660:171-199.
46. Werz C., Kohler K., Hafen E., Stocker H. The Drosophila SH2B family adaptor Lnk acts in parallel to chico in the insulin signaling pathway. PLoS Genet. 2009, 5:e1000596.
47. Winrow M.J., Rudney H. The incorporation of p-hydroxybenzoic acid and isopentenyl pyrophphate into ubiquinone precursors by cell-free preparations of rat tissues. Biochem. Biophys. Res. Commun. 1969, 37:833-840.
48. Wong A., Boutis P., Hekimi S. Mutations in the clk-1 gene of Caenorhabditis elegans affect developmental and behavioral timing. Genetics 1995, 139:1247-1259.
49. Yazaki K., Kunihisa M., Fujisaki T., Sato F. Geranyl diphosphate: 4-hydroxybenzoate geranyltransferase from Lithospermum erythrorhizon-Cloning and characterization of a key enzyme in shikonin biosynthesis. J. Biol. Chem. 2002, 277:6240-6246.
50. Zinke I., Kirchner C., Chao L.C., Tetzlaff M.T., Pankratz M.J. Suppression of food intake and growth by amino acids in Drosophila: the role of pumpless, a fat body expressed gene with homology to vertebrate glycine cleavage system. Development 1999, 126:5275-5284.