Osh6 overexpression extends the lifespan of yeast by increasing vacuole fusion

Cell Cycle

Volumn 11, Issue 11, 2012, Pages 2176-2188

  Gebre, Senetibeb ^a   Connor, Richard ^a   Xia, Yufeng ^a   Jawed, Sanaa ^a   Bush, John M ^a   Bard, Martin ^b   Elsalloukh, Hassan ^a   Tang, Fusheng ^a  

^a University of Arkansas   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Ergosterol; Lifespan; Osh6; Tor1; Vacuole

Indexed keywords

ERGOSTEROL; OXYSTEROL; SNARE PROTEIN;

ARTICLE; CELL VACUOLE; FUSION GENE; GENE; GENE INTERACTION; GENE OVEREXPRESSION; LIFESPAN; NONHUMAN; OSH6 GENE; PROMOTER REGION; TOR1 GENE; WILD TYPE; YEAST;

EID: 84861881131     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.20691     Document Type: Article

References (37)

1. Kaeberlein M, Powers RW, 3rd, Steffen KK, Westman EA, Hu D, Dang N, et al. Regulation of yeast replicative lifespan by TOR and Sch9 in response to nutrients. Science 2005; 310:1193-6; PMID:16293764; http://dx.doi.org/10.1126/ science.1115535.
2. Tang F, Watkins JW, Bermudez M, Gray R, Gaban A, Portie K, et al. A lifespan extending form of autophagy employs the vacuole-vacuole fusion machinery. Autophagy 2008; 4:874-86; PMID:18690010.
3. Wickner W. Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides and a Rab, all dancing in a ring on yeast vacuoles. Annu Rev Cell Dev Biol 2010; 26:115-36; PMID:20521906; http://dx.doi.org/10.1146/annurev- cellbio-100109-4131.
4. Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD. Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 2011; 144:389-401; PMID:21295699; http://dx.doi.org/10.1016/j.cell. 2010.12.034.
5. Michaillat L, Baars TL, Mayer A. Cell-free reconstitution of vacuole membrane fragmentation reveals regulation of vacuole size and number by TORC1. Mol Biol Cell 2012; 23:881-95; PMID:22238359; http://dx.doi.org/10.1091/mbc.E11- 08-0703.
6. Gary JD, Wurmser AE, Bonangelino CJ, Weisman LS, Emr SD. Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J Cell Biol 1998; 143:65-79; PMID:9763421; http://dx.doi.org/10.1083/jcb.143.1.65.
7. Duex JE, Tang F, Weisman LS. The Vac14p-Fig4p complex acts independently of Vac7p and couples PI3,5P2 synthesis and turnover. J Cell Biol 2006; 172:693-704; PMID:16492811; http://dx.doi.org/10.1083/jcb.200512105.
8. Efe JA, Botelho RJ, Emr SD. Atg18 regulates organelle morphology and Fab1 kinase activity independent of its membrane recruitment by phosphatidylinositol-3,5-bisphosphate. Mol Biol Cell 2007; 18:4232-44; PMID:17699591; http://dx.doi.org/10.1091/mbc.E07-04-0301.
9. Zinser E, Paltauf F, Daum G. Sterol composition of yeast organelle membranes and subcellular distribution of enzymes involved in sterol metabolism. J Bacteriol 1993; 175:2853-8; PMID:8491706.
10. Bagnat M, Keränen S, Shevchenko A, Shevchenko A, Simons K. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci USA 2000; 97:3254-9; PMID:10716729; http://dx.doi.org/10.1073/pnas.060034697.
11. Beh CT, Rine J. A role for yeast oxysterol-binding protein homologs in endocytosis and in the maintenance of intracellular sterol-lipid distribution. J Cell Sci 2004; 117:2983-96; PMID:15173322; http://dx.doi.org/10.1242/jcs.01157.
12. Beh CT, Cool L, Phillips J, Rine J. Overlapping functions of the yeast oxysterol-binding protein homologues. Genetics 2001; 157:1117-40; PMID:11238399.
13. Wang P, Duan W, Munn AL, Yang H. Molecular characterization of Osh6p, an oxysterol binding protein homolog in the yeast Saccharomyces cerevisiae. FEBS J 2005; 272:4703-15; PMID:16156791; http://dx.doi.org/10.1111/j.1742-4658.2005. 04886.x.
14. Raychaudhuri S, Im YJ, Hurley JH, Prinz WA. Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides. J Cell Biol 2006; 173:107-19; PMID:16585271; http://dx.doi.org/10.1083/jcb.200510084.
15. Schulz TA, Prinz WA. Sterol transport in yeast and the oxysterol binding protein homologue (OSH) family. Biochim Biophys Acta 2007; 1771:769-80; PMID:17434796.
16. Georgiev AG, Sullivan DP, Kersting MC, Dittman JS, Beh CT, Menon AK. Osh proteins regulate membrane sterol organization but are not required for sterol movement between the ER and PM. Traffic 2011; 12:1341-55; PMID:21689253; http://dx.doi.org/10.1111/j.1600-0854.2011.01234.x.
17. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, et al. Global analysis of protein expression in yeast. Nature 2003; 425:737-41; PMID:14562106; http://dx.doi.org/10.1038/nature02046.
18. Tarassov K, Messier V, Landry CR, Radinovic S, Serna Molina MM, Shames I, et al. An in vivo map of the yeast protein interactome. Science 2008; 320:1465-70; PMID:18467557; http://dx.doi.org/10.1126/science.1153878.
19. Wang P, Zhang Y, Li H, Chieu HK, Munn AL, Yang H. AAA ATPases regulate membrane association of yeast oxysterol binding proteins and sterol metabolism. EMBO J 2005; 24:2989-99; PMID:16096648; http://dx.doi.org/10.1038/sj.emboj. 7600764.
20. Cakar ZP, Sauer U, Bailey JE, Müller M, Stolz M, Wallimann T, et al. Vacuolar morphology and cell cycle distribution are modified by leucine limitation in auxotrophic Saccharomyces cerevisiae. Biol Cell 2000; 92:629-37; PMID:11374441; http://dx.doi.org/10.1016/S0248-4900(01)01111-X.
21. Munn AL, Heese-Peck A, Stevenson BJ, Pichler H, Riezman H. Specific sterols required for the internalization step of endocytosis in yeast. Mol Biol Cell 1999; 10:3943-57; PMID:10564282.
22. Thevissen K, Ayscough KR, Aerts AM, Du W, De Brucker K, Meert EM, et al. Miconazole induces changes in actin cytoskeleton prior to reactive oxygen species induction in yeast. J Biol Chem 2007; 282:21592-7; PMID:17553796; http://dx.doi.org/10.1074/jbc.M608505200.
23. Lindstrom DL, Leverich CK, Henderson KA, Gottschling DE. Replicative age induces mitotic recombination in the ribosomal RNA gene cluster of Saccharomyces cerevisiae. PLoS Genet 2011; 7:1002015; PMID:21436897; http://dx.doi.org/10. 1371/journal.pgen.1002015.
24. Tang F, Peng Y, Nau JJ. Kauffman EJ, Weisman LS. Vac8p, an armadillo repeat protein, co-ordinates vacuole inheritance with multiple vacuolar processes. Traffic 2006; 7:1368-77; PMID:16824055; http://dx.doi.org/10.1111/j. 1600-0854.2006.00458.x.
25. Peng Y, Tang F, Weisman LS. Palmitoylation plays a role in targeting Vac8p to specific membrane subdomains. Traffic 2006; 7:1378-87; PMID:16978392; http://dx.doi.org/10.1111/j.1600-0854.2006.00472.x.
26. Aronova S, Wedaman K, Anderson S, Yates J, 3rd, Powers T. Probing the membrane environment of the TOR kinases reveals functional interactions between TORC1, actin and membrane trafficking in Saccharomyces cerevisiae. Mol Biol Cell 2007; 18:2779-94; PMID:17507646; http://dx.doi.org/10.1091/mbc.E07-03-0274.
27. Kozminski KG, Alfaro G, Dighe S, Beh CT. Homologues of oxysterol-binding proteins affect Cdc42p- and Rho1p-mediated cell polarization in Saccharomyces cerevisiae. Traffic 2006; 7:1224-42; PMID:17004323; http://dx.doi.org/10.1111/j. 1600-0854.2006.00467.x.
28. Plank M, Wuttke D, van Dam S, Clarke SA, de Magalhães JP. A meta-analysis of caloric restriction gene expression profiles to infer common signatures and regulatory mechanisms. Mol Biosyst 2012; 8:1339-49; PMID:22327899; http://dx.doi.org/10.1039/c2mb05255e.
29. te Welscher YM, Jones L, van Leeuwen MR, Dijksterhuis J, de Kruijff B, Eitzen G, et al. Natamycin inhibits vacuole fusion at the priming phase via a specific interaction with ergosterol. Antimicrob Agents Chemother 2010; 54:2618-25; PMID:20385867; http://dx.doi.org/10.1128/AAC.01794-09.
30. Smotrys JE, Schoenfish MJ, Stutz MA, Linder ME. The vacuolar DHHC-CRD protein Pfa3p is a protein acyltransferase for Vac8p. J Cell Biol 2005; 170:1091-9; PMID:16186255; http://dx.doi.org/10.1083/jcb.200507048.
31. Strasser B, Iwaszkiewicz J, Michielin O, Mayer A. The V-ATPase proteolipid cylinder promotes the lipid-mixing stage of SNARE-dependent fusion of yeast vacuoles. EMBO J 2011; 30:4126-41; PMID:21934648; http://dx.doi.org/10. 1038/emboj.2011.335.
32. Brett CL, Kallay L, Hua Z, Green R, Chyou A, Zhang Y, et al. Genome-wide analysis reveals the vacuolar pH-stat of Saccharomyces cerevisiae. PLoS ONE 2011; 6:17619; PMID:21423800; http://dx.doi.org/10.1371/journal.pone.0017619.
33. Zhang YQ, Gamarra S, Garcia-Effron G, Park S, Perlin DS, Rao R. Requirement for ergosterol in V-ATPase function underlies antifungal activity of azole drugs. PLoS Pathog 2010; 6:1000939; PMID:20532216; http://dx.doi.org/10. 1371/journal.ppat.1000939.
34. Zurita-Martinez SA, Puria R, Pan X, Boeke JD, Cardenas ME. Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae. Genetics 2007; 176:2139-50; PMID:17565946; http://dx.doi.org/10. 1534/genetics.107.072835.
35. Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen J. Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 2001; 294:1942-5; PMID:11729323; http://dx.doi.org/10.1126/science.1066015.
36. Sturgill TW, Cohen A, Diefenbacher M, Trautwein M, Martin DE, Hall MN. TOR1 and TOR2 have distinct locations in live cells. Eukaryot Cell 2008; 7:1819-30; PMID:18723607; http://dx.doi.org/10.1128/EC.00088-08.
37. Tedrick K, Trischuk T, Lehner R, Eitzen G. Enhanced membrane fusion in sterol-enriched vacuoles bypasses the Vrp1p requirement. Mol Biol Cell 2004; 15:4609-21; PMID:15254266; http://dx.doi.org/10.1091/mbc.E04-03-0194.