A stable yeast strain efficiently producing cholesterol instead of ergosterol is functional for tryptophan uptake, but not weak organic acid resistance

Metabolic Engineering

Volumn 13, Issue 5, 2011, Pages 555-569

  Souza, Cleiton M ^a   Schwabe, Tatjana M E ^a   Pichler, Harald ^b,c   Ploier, Birgit ^b,c   Leitner, Erich ^b   Guan, Xue Li ^d   Wenk, Markus R ^d   Riezman, Isabelle ^a   Riezman, Howard ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^c AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Campesterol; Cholesterol; DHCR24; DHCR7; Ergosterol; Lipid engineering; Membranes; Tryptophan transport; Weak organic acid transport; Yeast

Indexed keywords

CAMPESTEROL; DHCR24; DHCR7; ERGOSTEROL; TRYPTOPHAN TRANSPORT; WEAK ORGANIC ACIDS;

ACID RESISTANCE; AMINO ACIDS; CHOLESTEROL; LIPIDS; STRAIN; YEAST;

ALCOHOLS;

ARGININE; CARBOXYLIC ACID; CHOLESTA 5,24(25) DIENOL; CHOLESTA 5,7 DIENOL; CHOLESTA 5,7,24(25) TRIENOL; CHOLESTA 7,24(25) DIENOL; CHOLESTA 8,24(25) DIENOL; CHOLESTA TETRAENOL; CHOLESTEROL; DEHYDROCHOLESTEROL 24 REDUCTASE; DEHYDROCHOLESTEROL 7 REDUCTASE; ERGOSTEROL; LIPID; MULTIDRUG RESISTANCE PROTEIN; PDR12P PROTEIN; STEROL; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ARTICLE; CHEMICAL STRUCTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; YEAST;

ATP-BINDING CASSETTE TRANSPORTERS; CHOLESTEROL; ERGOSTEROL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRYPTOPHAN;

EUKARYOTA;

EID: 80052033032     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2011.06.006     Document Type: Article

References (63)

1. Anderson R.G., Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 2002, 296:1821-1825.
2. Bagnat M., Chang A., Simons K. Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast. Mol. Biol. Cell 2001, 12:4129-4138.
3. Bagnat M., Keranen S., Shevchenko A., Simons K. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. U S A 2000, 97:3254-3259.
4. Baudry K., Swain E., Rahier A., Germann M., Batta A., Rondet S., Mandala S., Henry K., Tint G.S., Edlind T., Kurtz M., Nickels J.T. The effect of the erg26-1 mutation on the regulation of lipid metabolism in Saccharomyces cerevisiae. J. Biol. Chem. 2001, 276:12702-12711.
5. Bottema C.D., Rodriguez R.J., Parks L.W. Influence of sterol structure on yeast plasma membrane properties. Biochim. Biophys. Acta 1985, 813:313-320.
6. Callera G.E., Montezano A.C., Yogi A., Tostes R.C., Touyz R.M. Vascular signaling through cholesterol-rich domains: implications in hypertension. Curr. Opin. Nephrol. Hypertens. 2007, 16:90-104.
7. Carvalho M., Schwudke D., Sampaio J.L., Palm W., Riezman I., Dey G., Gupta G.D., Mayor S., Riezman H., Shevchenko A., Kurzchalia T.V., Eaton S. Survival strategies of a sterol auxotroph. Development 2010, 137:3675-3685.
8. Castillon G.A., Watanabe R., Taylor M., Schwabe T.M., Riezman H. Concentration of GPI-anchored proteins upon ER exit in yeast. Traffic 2009, 10:186-200.
9. Chazal N., Gerlier D. Virus entry, assembly, budding, and membrane rafts. Microbiol. Mol. Biol. Rev. 2003, 67:226-237. table of contents.
10. Clayton P.T. Disorders of cholesterol biosynthesis. Arch. Dis. Child. 1998, 78:185-189.
11. Eisenkolb M., Zenzmaier C., Leitner E., Schneiter R. A specific structural requirement for ergosterol in long-chain fatty acid synthesis mutants important for maintaining raft domains in yeast. Mol. Biol. Cell 2002, 13:4414-4428.
12. Gaber R.F., Copple D.M., Kennedy B.K., Vidal M., Bard M. The yeast gene ERG6 is required for normal membrane function but is not essential for biosynthesis of the cell-cycle-sparking sterol. Mol. Cell. Biol. 1989, 9:3447-3456.
13. Gimpl G., Burger K., Fahrenholz F. Cholesterol as modulator of receptor function. Biochemistry 1997, 36:10959-10974.
14. Gimpl G., Fahrenholz F. Cholesterol as stabilizer of the oxytocin receptor. Biochim. Biophys. Acta 2002, 1564:384-392.
15. Grossmann G., Malinsky J., Stahlschmidt W., Loibl M., Weig-Meckl I., Frommer W.B., Opekarovã¡ M., Tanner W. Plasma membrane microdomains regulate turnover of transport proteins in yeast. J. Cell Biol. 2008, 183:1075-1088.
16. Guan X.L., Riezman I., Wenk M.R., Riezman H. Yeast lipid analysis and quantification by mass spectrometry. Methods Enzymol. 2010, 470:369-391.
17. Guan X.L., Souza C.M., Pichler H., Dewhurst G., Schaad O., Kajiwara K., Wakabayashi H., Ivanova T., Castillon G.A., Piccolis M., Abe F., Loewith R., Funato K., Wenk M.R., Riezman H. Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Mol. Biol. Cell 2009, 20:2083-2095.
18. Guan X.L., Wenk M.R. Mass spectrometry-based profiling of phospholipids and sphingolipids in extracts from Saccharomyces cerevisiae. Yeast 2006, 23:465-477.
19. Hapala I., Klobucnikova V., Mazanova K., Kohut P. Two mutants selectively resistant to polyenes reveal distinct mechanisms of antifungal activity by nystatin and amphotericin B. Biochem. Soc. Trans. 2005, 33:1206-1209.
20. Heese-Peck A., Pichler H., Zanolari B., Watanabe R., Daum G., Riezman H. Multiple functions of sterols in yeast endocytosis. Mol. Biol. Cell 2002, 13:2664-2680.
21. Hein C., Andre B. A C-terminal di-leucine motif and nearby sequences are required for NH4(+)-induced inactivation and degradation of the general amino acid permease, Gap1p, of Saccharomyces cerevisiae. Mol. Microbiol. 1997, 24:607-616.
22. Holyoak C.D., Bracey D., Piper P.W., Kuchler K., Coote P.J. The Saccharomyces cerevisiae weak-acid-inducible ABC transporter Pdr12 transports fluorescein and preservative anions from the cytosol by an energy-dependent mechanism. J. Bacteriol. 1999, 181:4644-4652.
23. Kresnowati M.T., Suarez-Mendez C.M., van Winden W.A., van Gulik W.M., Heijnen J.J. Quantitative physiological study of the fast dynamics in the intracellular pH of Saccharomyces cerevisiae in response to glucose and ethanol pulses. Metab. Eng. 2008, 10:39-54.
24. Kurzchalia T.V., Ward S. Why do worms need cholesterol?. Nat. Cell Biol. 2003, 5:684-688.
25. Lichtenberg D., Goni F.M., Heerklotz H. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem. Sci. 2005, 30:430-436.
26. Longtine M.S., McKenzie A., Demarini D.J., Shah N.G., Wach A., Brachat A., Philippsen P., Pringle J.R. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
27. Lucero H.A., Robbins P.W. Lipid rafts-protein association and the regulation of protein activity. Arch. Biochem. Biophys. 2004, 426:208-224.
28. Malinska K., Malinsky J., Opekarova M., Tanner W. Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol. Biol. Cell 2003.
29. Malinska K., Malinsky J., Opekarova M., Tanner W. Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J. Cell Sci. 2004, 117:6031-6041.
30. Mayor S., Sabharanjak S., Maxfield F.R. Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO J. 1998, 17:4626-4638.
31. Michel V., Bakovic M. Lipid rafts in health and disease. Biol. Cell 2007, 99:129-140.
32. Mollapour M., Fong D., Balakrishnan K., Harris N., Thompson S., Schuller C., Kuchler K., Piper P.W. Screening the yeast deletant mutant collection for hypersensitivity and hyper-resistance to sorbate, a weak organic acid food preservative. Yeast 2004, 21:927-946.
33. Mullner H., Daum G. Dynamics of neutral lipid storage in yeast. Acta Biochim. Pol. 2004, 51:323-347.
34. Mullner H., Deutsch G., Leitner E., Ingolic E., Daum G. YEH2/YLR020c encodes a novel steryl ester hydrolase of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 2005, 280:13321-13328.
35. Mumberg D., Muller R., Funk M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 1995, 156:119-122.
36. Nicolaou S.A., Gaida S.M., Papoutsakis E.T. A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: from biofuels and chemicals, to biocatalysis and bioremediation. Metab. Eng. 2010, 12:307-331.
37. Opekarova M., Robl I., Tanner W. Phosphatidyl ethanolamine is essential for targeting the arginine transporter Can1p to the plasma membrane of yeast. Biochim. Biophys. Acta 2002, 1564:9-13.
38. Opekarova M., Tanner W. Specific lipid requirements of membrane proteins-a putative bottleneck in heterologous expression. Biochim. Biophys. Acta 2003, 1610:11-22.
39. Parks L.W., Crowley J.H., Leak F.W., Smith S.J., Tomeo M.E. Use of sterol mutants as probes for sterol functions in the yeast, Saccharomyces cerevisiae. Crit. Rev. Biochem. Mol. Biol. 1999, 34:399-404.
40. Parks L.W., Smith S.J., Crowley J.H. Biochemical and physiological effects of sterol alterations in yeast-a review. Lipids 1995, 30:227-230.
41. Petschnigg J., Wolinski H., Kolb D., Zellnig G., Kurat C.F., Natter K., Kohlwein S.D. Good fat-essential cellular requirements for triacylglycerol synthesis to maintain membrane homeostasis in yeast. J. Biol. Chem. 2009.
42. Pichler H., Riezman H. Where sterols are required for endocytosis. Biochim. Biophys. Acta 2004, 1666:51-61.
43. Pike, L.J., 2006. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 47, 1597-1598.
44. Pinto W.J., Lozano R., Nes W.R. Inhibition of sterol biosynthesis by ergosterol and cholesterol in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1985, 836:89-95.
45. Piper P., Calderon C.O., Hatzixanthis K., Mollapour M. Weak acid adaptation: the stress response that confers yeasts with resistance to organic acid food preservatives. Microbiology 2001, 147:2635-2642.
46. Regenberg B., During-Olsen L., Kielland-Brandt M.C., Holmberg S. Substrate specificity and gene expression of the amino-acid permeases in Saccharomyces cerevisiae. Curr. Genet. 1999, 36:317-328.
47. Reina C., Padoani G., Carotti C., Merico A., Tripodi G., Ferrari P., Popolo L. Expression of the alpha3/beta1 isoform of human Na,K-ATPase in the methylotrophic yeast Pichia pastoris. FEMS Yeast Res. 2007, 7:585-594.
48. Rockwell N.C., Wolfger H., Kuchler K., Thorner J. ABC transporter Pdr10 regulates the membrane microenvironment of Pdr12 in Saccharomyces cerevisiae. J. Membr. Biol. 2009, 229:27-52.
49. Roncero C., Valdivieso M.H., Ribas J.C., Duran A. Isolation and characterization of Saccharomyces cerevisiae mutants resistant to Calcofluor white. J. Bacteriol. 1988, 170:1950-1954.
50. Sharp P.M., Li W.H. The codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987, 15:1281-1295.
51. Shiba Y., Paradise E.M., Kirby J., Ro D.K., Keasling J.D. Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae for high-level production of isoprenoids. Metab. Eng. 2007, 9:160-168.
52. Shivapurkar R., Souza C.M., Jeannerat D., Riezman H. An efficient method for the production of isotopically enriched cholesterol for NMR. J. Lipid Res. 2011, 52:1062-1065.
53. Simons K., Ikonen E. Functional rafts in cell membranes. Nature 1997, 387:569-572.
54. Smith S.J., Crowley J.H., Parks L.W. Transcriptional regulation by ergosterol in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 1996, 16:5427-5432.
55. Souza C.M., Pichler H. Lipid requirements for endocytosis in yeast. Biochim. Biophys. Acta 2007, 1771:442-454.
56. te Welscher Y.M., ten Napel H.H., Balague M.M., Souza C.M., Riezman H., de Kruijff B., Breukink E. Natamycin blocks fungal growth by binding specifically to ergosterol without permeabilizing the membrane. J. Biol. Chem. 2008, 283:6393-6401.
57. Umebayashi K., Nakano A. Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. J. Cell Biol. 2003, 161:1117-1131.
58. Waterham H.R., Koster J., Romeijn G.J., Hennekam R.C., Vreken P., Andersson H.C., FitzPatrick D.R., Kelley R.I., Wanders R.J. Mutations in the 3beta-hydroxysterol Delta24-reductase gene cause desmosterolosis, an autosomal recessive disorder of cholesterol biosynthesis. Am. J. Hum. Genet. 2001, 69:685-694. Epub 2001 Aug 22.
59. Wickerham L.J. A critical evaluation of the nitrogen assimilation tests commonly used in the classification of yeasts. J. Bacteriol. 1946, 52:293-301.
60. Wolfman L., Sachs B.A. Separation of cholesterol and demosterol by thin-layer chromatography. J. Lipid Res. 1964, 15:127-128.
61. Xu S.H., Nes W.D. Biosynthesis of cholesterol in the yeast mutant erg6. Biochem. Biophys. Res. Commun. 1988, 155:509-517.
62. Xu X., Bittman R., Duportail G., Heissler D., Vilcheze C., London E. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. J. Biol. Chem. 2001, 276:33540-33546.
63. Ziman M., Chuang J.S., Schekman R.W. Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway. Mol. Biol. Cell 1996, 7:1909-1919.