Dual N- and C-terminal helices are required for endoplasmic reticulum and lipid droplet association of alcohol acetyltransferases in Saccharomyces cerevisiae

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Lin, Jyun Liang ^a   Wheeldon, Ian ^a  

^a University of California Riverside   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; ALCOHOL ACYLTRANSFERASE; FAT DROPLET; UNCLASSIFIED DRUG; ALCOHOL O-ACETYLTRANSFERASE; ATF2 PROTEIN, S CEREVISIAE; GREEN FLUORESCENT PROTEIN; PROTEIN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; ATF1 GENE; ATF2 GENE; CANTALOUPE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FUNGAL GENE; GENE SEQUENCE; KLUYVEROMYCES LACTIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PROTEIN DOMAIN; SACCHAROMYCES CEREVISIAE; TOMATO; WICKERHAMOMYCES ANOMALUS; AMINO ACID SEQUENCE; CELL MEMBRANE; CHEMISTRY; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; STRUCTURE ACTIVITY RELATION;

ACETYLTRANSFERASES; AMINO ACID SEQUENCE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEINS; LIPID DROPLETS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84905455199     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104141     Document Type: Article

References (58)

1. Yoshioka K, Hashimoto N (1981) Ester Formation by Alcohol Acetyltransferase from Brewers-Yeast. Agric Biol Chem 45: 2183-2190.
2. Mason AB, Dufour JP (2000) Alcohol acetyltransferases and the significance of ester synthesis in yeast. Yeast 16: 1287-1298.
3. Saerens SMG, Delvaux FR, Verstrepen KJ, Thevelein JM (2010) Production and biological function of volatile esters in Saccharomyces cerevisiae. Microb Biotechnol 3: 165-177.
4. Malcorps P, Dufour JP (1992) Short-Chain and Medium-Chain Aliphatic-Ester Synthesis in Saccharomyces-Cerevisiae. Eur J Biochem 210: 1015-1022. (Pubitemid 23015804)
5. Fujii T, Nagasawa N, Iwamatsu A, Bogaki T, Tamai W, et al. (1994) Molecular-Cloning, Sequence-Analysis, and Expression of the Yeast Alcohol Acetyltransferase Gene. Appl Environ Microbiol 60: 2786-2792. (Pubitemid 24242270)
6. Nagasawa N, Bogaki T, Iwamatsu A, Hamachi M, Kumagai C (1998) Cloning and nucleotide sequence of the alcohol acetyltransferase II gene (ATF2) from Saccharomyces cerevisiae Kyokai No. 7. Biosci Biotech and Bioch 62: 1852-1857. (Pubitemid 128473744)
7. Verstrepen KJ, Van Laere SDM, Vanderhaegen BMP, Derdelinckx G, Dufour JP, et al. (2003) Expression levels of the yeast alcohol acetyltransferase genes ATF1, Lg-ATF1, and ATF2 control the formation of a broad range of volatile esters. Appl Environ Microbiol 69: 5228-5237. (Pubitemid 37150744)
8. Lilly M, Lambrechts MG, Pretorius IS (2000) Effect of increased yeast alcohol acetyltransferase activity on flavor profiles of wine and distillates. Appl Environ Microbiol 66: 744-753. (Pubitemid 30082769)
9. Lilly M, Bauer FF, Lambrechts MG, Swiegers JH, Cozzolino D, et al. (2006) The effect of increased yeast alcohol acetyltransferase and esterase activity on the flavour profiles of wine and distillates. Yeast 23: 641-659. (Pubitemid 44210053)
10. Fujiwara D, Kobayashi O, Yoshimoto H, Harashima S, Tamai Y (1999) Molecular mechanism of the multiple regulation of the Saccharomyces cerevisiae ATF1 gene encoding alcohol acetyltransferase. Yeast 15: 1183-1197. (Pubitemid 29440631)
11. Fujii T, Kobayashi O, Yoshimoto H, Furukawa S, Tamai Y (1997) Effect of aeration and unsaturated fatty acids on expression of the Saccharomyces cerevisiae alcohol acetyltransferase gene. Appl Environ Microbiol 63: 910-915. (Pubitemid 27098471)
12. Saerens SMG, Delvaux F, Verstrepen KJ, Van Dijck P, Thevelein JM, et al. (2008) Parameters affecting ethyl ester production by Saccharomyces cerevisiae during fermentation. Appl Environ Microbiol 74: 454-461.
13. Plata C, Mauricio JC, Millan C, Ortega JM (2005) Influence of glucose and oxygen on the production of ethyl acetate and isoamyl acetate by a Saccharomyces cerevisiae strain during alcoholic fermentation. World J Microb Biot 21: 115-121. (Pubitemid 40172062)
14. Van Laere SDM, Saerens SMG, Verstrepen KJ, Van Dijck P, Thevelein JM, et al. (2008) Flavour formation in fungi: characterisation of KlAtf, the Kluyveromyces lactis orthologue of the Saccharomyces cerevisiae alcohol acetyltransferases Atf1 and Atf2. Appl Microbiol Biot 78: 783-792.
15. Galaz S, Morales-Quintana L, Moya-Leon MA, Herrera R (2013) Structural analysis of the alcohol acyltransferase protein family from Cucumismelo shows that enzyme activity depends on an essential solvent channel. Febs J 280: 1344-1357.
16. Aharoni A, Keizer LCP, Bouwmeester HJ, Sun ZK, Alvarez-Huerta M, et al. (2000) Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell 12: 647-661. (Pubitemid 30343579)
17. Howard D, Anderson RG (1976) Cell-Free Synthesis of Ethyl-Acetate by Extracts from Saccharomyces-Cerevisiae. J I Brewing 82: 70-71.
18. Verstrepen KJ, Van Laere SDM, Vercammen J, Derdelinckx G, Dufour JP, et al. (2004) The Saccharomyces cerevisiae alcohol acetyl transferase Atf1p is localized in lipid particles. Yeast 21: 367-376.
19. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691. (Pubitemid 37314307)
20. Cauet G, Degryse E, Ledoux C, Spagnoli R, Achstetter T (1999) Pregnenolone esterification in Saccharomyces cerevisiae - A potential detoxification mechanism. Eur J Biochem 261: 317-324. (Pubitemid 29166099)
21. Tiwari R, Koffel R, Schneiter R (2007) An acetylation/deacetylation cycle controls the export of sterols and steroids from S-cerevisiae. EMBO J 26: 5109-5119. (Pubitemid 350261287)
22. Goodman JM (2008) The gregarious lipid droplet. J Biol Chem 283: 28005-28009.
23. Walther TC, Farese RV (2012) Lipid Droplets and Cellular Lipid Metabolism. Annu Rev Biochem, 81: 687-714.
24. Chapman KD, Dyer JM, Mullen RT (2012) Biogenesis and functions of lipid droplets in plants. J Lipid Res 53: 215-226.
25. Athenstaedt K, Zweytick D, Jandrositz A, Kohlwein SD, Daum G (1999) Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J Bacteriol 181: 6441-6448. (Pubitemid 29512955)
26. Grillitsch K, Connerth M, Kofeler H, Arrey TN, Rietschel B, et al. (2011) Lipid particles/droplets of the yeast Saccharomyces cerevisiae revisited: Lipidome meets Proteome. Bba-Mol Cell Biol L 1811: 1165-1176.
27. Czabany T, Wagner A, Zweytick D, Lohner K, Leitner E, et al. (2008) Structural and biochemical properties of lipid particles from the yeast Saccharomyces cerevisiae. J Biol Chem 283: 17065-17074.
28. Ohsaki Y, Suzuki M, Fujimoto T (2014) Open Questions in Lipid Droplet Biology. Chem Biol 21: 86-96.
29. Wilfling F, Wang HJ, Haas JT, Krahmer N, Gould TJ, et al. (2013) Triacylglycerol Synthesis Enzymes Mediate Lipid Droplet Growth by Relocalizing from the ER to Lipid Droplets. Dev Cell 24: 384-399.
30. Sonnhammer EL, von Heijne G, Krogh A (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6: 175-182.
31. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 305: 567-580. (Pubitemid 33032862)
32. Combet C, Blanchet C, Geourjon C, Deleage G (2000) NPS@: network protein sequence analysis. Trends Biochem Sci 25: 147-150. (Pubitemid 30122428)
33. Gautier R, Douguet D, Antonny B, Drin G (2008) HELIQUEST: a web server to screen sequences with specific alpha-helical properties. Bioinformatics 24: 2101-2102.
34. Vadali RV, Bennett GN, San KY (2004) Applicability of CoA/acetyl-CoA manipulation system to enhance isoamyl acetate production in Escherichia coli. Metab Eng 6: 294-299. (Pubitemid 39379465)
35. Singh R, Vadlani PV, Harrison ML, Bennett GN, San KY (2008) Aerobic production of isoamyl acetate by overexpression of the yeast alcohol acetyltransferases AFT1 and AFT2 in Escherichia coli and using low-cost fermentation ingredients. Bioproc Biosyst Eng 31: 299-306. (Pubitemid 351713116)
36. Horton CE, Huang KX, Bennett GN, Rudolph FB (2003) Heterologous expression of the Saccharomyces cerevisiae alcohol acetyltransferase genes in Clostridium acetobutylicum and Escherichia coli for the production of isoamyl acetate. J Ind Microbiol Biotechnol 30: 427-432. (Pubitemid 37100325)
37. Horton CE, Bennett GN (2006) Ester production in E-coli and C-acetobutylicum. Enzyme Microb Tech 38: 937-943.
38. Rodriguez GM, Tashiro Y, Atsumi S (2014) Expanding ester biosynthesis in Escherichia coli. Nat Chem Biol 10: 259-265.
39. Abell BM, Holbrook LA, Abenes M, Murphy DJ, Hills MJ, et al. (1997) Role of the proline knot motif in oleosin endoplasmic reticulum topology and oil body targeting. Plant Cell 9: 1481-1493. (Pubitemid 28174124)
40. Ozeki S, Cheng J, Tauchi-Sato K, Hatano N, Taniguchi H, et al. (2005) Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J Cell Sci 118: 2601-2611. (Pubitemid 40932886)
41. Martin S, Driessen K, Nixon SJ, Zerial M, Parton RG (2005) Regulated localization of Rab18 to lipid droplets: effects of lipolytic stimulation and inhibition of lipid droplet catabolism. J Biol Chem 280: 42325-42335. (Pubitemid 43023204)
42. Drin G, Antonny B (2010) Amphipathic helices and membrane curvature. FEBS Lett 584: 1840-1847.
43. Hinson ER, Cresswell P (2009) The antiviral protein, viperin, localizes to lipid droplets via its N-terminal amphipathic alpha-helix. Proc Natl Acad Sci USA 106: 20452-20457.
44. Bouvet S, Golinelli-Cohen MP, Contremoulins V, Jackson CL (2013) Targeting of the Arf-GEF GBF1 to lipid droplets and Golgi membranes. J Cell Sci 126: 4794-4805.
45. Krahmer N, Guo Y, Wilfling F, Hilger M, Lingrell S, et al. (2011) Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP:phosphocholine cytidylyltransferase. Cell Metab 14: 504-515.
46. Boulant S, Montserret R, Hope RG, Ratinier M, Targett-Adams P, et al. (2006) Structural determinants that target the hepatitis C virus core protein to lipid droplets. J Biol Chem 281: 22236-22247. (Pubitemid 44181927)
47. McFie PJ, Banman SL, Kary S, Stone SJ (2011) Murine Diacylglycerol Acyltransferase-2 (DGAT2) Can Catalyze Triacylglycerol Synthesis and Promote Lipid Droplet Formation Independent of Its Localization to the Endoplasmic Reticulum. J Biol Chem 286: 28235-28246.
48. Zinser E, Daum G (1995) Isolation and Biochemical-Characterization of Organelles from the Yeast, Saccharomyces-Cerevisiae. Yeast 11: 493-536.
49. Leber R, Zinser E, Zellnig G, Paltauf F, Daum G (1994) Characterization of Lipid Particles of the Yeast, Saccharomyces-Cerevisiae. Yeast 10: 1421-1428. (Pubitemid 24347995)
50. Koffel R, Tiwari R, Falquet L, Schneiter R (2005) The Saccharomyces cerevisiae YLL012/YEH1, YLR020/YEH2, and TGL1 genes encode a novel family of membrane-anchored lipases that are required for steryl ester hydrolysis. Mol Cell Biol 25: 1655-1668. (Pubitemid 40280135)
51. Thurston PA, Quain DE, Tubb RS (1982) Lipid-Metabolism and the Regulation of Volatile Ester Synthesis in Saccharomyces-Cerevisiae. J I Brewing 88: 90-94.
52. Erdmann R, Blobel G (1995) Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J Cell Biol 128: 509-523.
53. Hoover DM, Lubkowski J (2002) DNAWorks: an automated method for designing oligonucleotides for PCR-based gene synthesis. Nucleic Acids Res 30: e43.
54. Binns D, Januszewski T, Chen Y, Hill J, Markin VS, et al. (2006) An intimate collaboration between peroxisomes and lipid bodies. J Cell Biol 173: 719-731. (Pubitemid 46165580)
55. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947-962. (Pubitemid 39206863)
56. Connerth M, Grillitsch K, Kofeler H, Daum G (2009) Analysis of lipid particles from yeast. Methods Mol Biol 579: 359-374.
57. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680. (Pubitemid 24354800)
58. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.