Compartment-specific synthesis of phosphatidylethanolamine is required for normal heavy metal resistance

Molecular Biology of the Cell

Volumn 21, Issue 3, 2010, Pages 443-455

  Gulshan, Kailash ^a   Shahi, Puja ^a   Moye Rowley, W Scott ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; CADMIUM; CARRIER PROTEIN; HEAVY METAL; MEMBRANE PHOSPHOLIPID; MEMBRANE PROTEIN; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE DECARBOXYLASE; PROTEIN PDR17; PROTEIN YCF1; UNCLASSIFIED DRUG;

ARTICLE; ENDOSOME; ENZYME ANALYSIS; LIPID COMPOSITION; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE;

ATP-BINDING CASSETTE TRANSPORTERS; CADMIUM; CARBOXY-LYASES; CELL MEMBRANE; ENDOSOMES; ISOENZYMES; MEMBRANE LIPIDS; MITOCHONDRIA; PHOSPHATIDYLETHANOLAMINES; PHOSPHOLIPID TRANSFER PROTEINS; R-SNARE PROTEINS; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VACUOLES;

SACCHAROMYCES CEREVISIAE;

EID: 76049118071     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-06-0519     Document Type: Article

References (75)

1. Achleitner, G., Zweytick, D., Trotter, P. J., Voelker, D. R., and Daum, G. (1995). Synthesis and intracellular transport of aminoglycerophospholipids in permeabilized cells of the yeast, Saccharomyces cerevisiae. J. Biol. Chem. 270, 29836-29842.
2. Bagnat, M., Keränen, S., Shevchenko, A., Shevchenko, A., and Simons, K. (2000). Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. USA 97, 3254-3259.
3. Balzi, E., Wang, M., Leterme, S., Van Dyck, L., and Goffeau, A. (1994). PDR5: a novel yeast multidrug resistance transporter controlled by the transcription regulator PDR1. J. Biol. Chem. 269, 2206-2214.
4. Becherer, K. A., Rieder, S. E., Emr, S. D., and Jones, E. W. (1996). Novel syntaxin homologue, Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast. Mol. Biol. Cell 7, 579-594.
5. Birner, R., Burgermeister, M., Schneiter, R., and Daum, G. (2001). Roles of phosphatidylethanolamine and of its several biosynthetic pathways in Saccharomyces cerevisiae. Mol. Biol. Cell 12, 997-1007.
6. Bissinger, P. H., and Kuchler, K. (1994). Molecular cloning and expression of the S. cerevisiae STS1 gene product. J. Biol. Chem. 269, 4180-4186.
7. Bligh, E. G., and Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917.
8. Bogdanov, M., Heacock, P. N., and Dowhan, W. (2002). A polytopic membrane protein displays a reversible topology dependent on membrane lipid composition. EMBO J. 21, 2107-2116.
9. Bogdanov, M., Umeda, M., and Dowhan, W. (1999). Phospholipid-assisted refolding of an integral membrane protein. Minimum structural features for phosphatidylethanolamine to act as a molecular chaperone. J. Biol. Chem. 274, 12339-12345.
10. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
11. Carman, G. M., and Han, G. S. (2009). Regulation of phospholipid synthesis in yeast. J Lipid Res. 50(suppl), S69-S73.
12. Chalvardjian, A., and Rudnicki, E. (1970). Determination of lipid phosphorus in the nanomolar range. Anal. Biochem. 36, 225-226.
13. Chaudhuri, B., Ingavale, S., and Bachhawat, A. K. (1997). apd1+, a gene required for red pigment formation in ade6 mutants of Schizosaccharomyces pombe, encodes an enzyme required for glutathione biosynthesis: a role for glutathione and a glutathione-conjugate pump. Genetics 145, 75-83.
14. Chen, C. Y., Ingram, M. F., Rosal, P. H., and Graham, T. R. (1999). Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J. Cell Biol. 147, 1223-1236.
15. Chen, S., Wang, J., Muthusamy, B. P., Liu, K., Zare, S., Andersen, R. J., and Graham, T. R. (2006). Roles for the Drs2p-Cdc50p complex in protein transport and phosphatidylserine asymmetry of the yeast plasma membrane. Traffic 7, 1503-1517.
16. Clancey, C. J., Chang, S. C., and Dowhan, W. (1993). Cloning of a gene (PSD1) encoding phosphatidylserine decarboxylase from Saccharomyces cerevisiae by complementation of an Escherichia coli mutant. J. Biol. Chem. 268, 24580-24590.
17. Daum, G., Lees, N. D., Bard, M., and Dickson, R. (1998). Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast 14, 1471-1510.
18. Dowhan, W., and Bogdanov, M. (2009). Lipid-dependent membrane protein topogenesis. Annu. Rev. Biochem. 78, 515-540.
19. Dupre, S., and Haguenauer-Tsapis, R. (2003). Raft partitioning of the yeast uracil permease during trafficking along the endocytic pathway. Traffic 4, 83-96.
20. Furuta, N., Fujimura-Kamada, K., Saito, K., Yamamoto, T., and Tanaka, K. (2007). Endocytic recycling in yeast is regulated by putative phospholipid translocases and the Ypt31p/32p-Rcy1p pathway. Mol. Biol. Cell 18, 295-312.
21. Gerrard, S. R., Levi, B. P., and Stevens, T. H. (2000). Pep12p is a multifunctional yeast syntaxin that controls entry of biosynthetic, endocytic and retrograde traffic into the prevacuolar compartment. Traffic 1, 259-269.
22. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003). Global analysis of protein expression in yeast. Nature 425, 737-741.
23. Griac, P. (2007). Sec14 related proteins in yeast. Biochim. Biophys. Acta 1771, 737-745.
24. Gueldry, O., Lazard, M., Delort, F., Dauplais, M., Grigoras, I., Blanquet, S., and Plateau, P. (2003). Ycf1p-dependent Hg(II) detoxification in Saccharomyces cerevisiae. Eur. J. Biochem. 270, 2486-2496.
25. Gulshan, K., Schmidt, J., Shahi, P., and Moye-Rowley, W. S. (2008). Evidence for the bifunctional nature of mitochondrial phosphatidylserine decarboxylase: role in Pdr3-dependent retrograde regulation of PDR5 expression. Mol. Cell. Biol. 28, 5851-5864.
26. Gurunathan, S., Chapman-Shimshoni, D., Trajkovic, S., and Gerst, J. E. (2000). Yeast exocytic v-SNAREs confer endocytosis. Mol. Biol. Cell 11, 3629-3643.
27. Hakizimana, P., Masureel, M., Gbaguidi, B., Ruysschaert, J. M., and Govaerts, C. (2008). Interactions between phosphatidylethanolamine headgroup and LmrP, a multidrug transporter: a conserved mechanism for proton gradient sensing? J. Biol. Chem. 283, 9369-9376.
28. Hearn, J. D., Lester, R. L., and Dickson, R. C. (2003). The uracil transporter Fur4p associates with lipid rafts. J. Biol. Chem. 278, 3679-3686.
29. Hirata, D., Yano, K., Miyahara, K., and Miyakawa, T. (1994). Saccharomyces cerevisiae YDR1, which encodes a member of the ATP-binding cassette (ABC) superfamily, is required for multidrug resistance. Curr. Genet. 26, 285-294.
30. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., and O'Shea, E. K. (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691.
31. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
32. Kama, R., Robinson, M., and Gerst, J. E. (2007). Btn2, a Hook1 ortholog and potential Batten disease-related protein, mediates late endosome-Golgi protein sorting in yeast. Mol. Cell. Biol. 27, 605-621.
33. Katzmann, D. J., Epping, E. A., and Moye-Rowley, W. S. (1999). Mutational disruption of plasma membrane trafficking of Saccharomyces cerevisiae Yor1p, a homologue of mammalian multidrug resistance protein. Mol. Cell. Biol. 19, 2998-3009.
34. Katzmann, D. J., Hallstrom, T. C., Voet, M., Wysock, W., Golin, J., Volckaert, G., and Moye-Rowley, W. S. (1995). Expression of an ATP-binding cassette transporter encoding gene (YOR1) is required for oligomycin resistance in Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 6875-6883.
35. Kitamura, H., Wu, W. I., and Voelker, D. R. (2002). The C2 domain of phosphatidylserine decarboxylase 2 is not required for catalysis but is essential for in vivo function. J. Biol. Chem. 277, 33720-33726.
36. Klein, M., Mamnun, Y. M., Eggmann, T., Schuller, C., Wolfger, H., Martinoia, E., and Kuchler, K. (2002). The ATP-binding cassette (ABC) transporter Bpt1p mediates vacuolar sequestration of glutathione conjugates in yeast. FEBS Lett. 520, 63-67.
37. Kolaczkowski, M., van der Rest, M., Cybularz-Kolaczkowski, A., Soumillion, J.-P., Konings, W. N., and Goffeau, A. (1996). Anticancer drugs, ionophoric peptides and steroids as substrates of the yeast multidrug transporter Pdr5p. J. Biol. Chem. 271, 31543-31548.
38. Krogan, N. J., et al. (2006). Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643.
39. Kuge, O., Saito, K., Kojima, M., Akamatsu, Y., and Nishijima, M. (1996). Post-translational processing of the phosphatidylserine decarboxylase gene product in Chinese hamster ovary cells. Biochem. J. 319, 33-38.
40. Lewis, M. J., Nichols, B. J., Prescianotto-Baschong, C., Riezman, H., and Pelham, H. R. (2000). Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol. Biol. Cell 11, 23-38.
41. Li, Q. X., and Dowhan, W. (1990). Studies on the mechanism of formation of the pyruvate prosthetic group of phosphatidylserine decarboxylase from Escherichia coli. J. Biol. Chem. 265, 4111-4115.
42. Li, Z.-S., Szczypka, M., Lu, Y.-P., Thiele, D. J., and Rea, P. A. (1996). The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J. Biol. Chem. 271, 6509-6517.
43. Longtine, M. S., McKenzie, A., Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
44. Manolson, M. F., Proteau, D., Preston, R. A., Stenbit, A., Roberts, B. T., Hoyt, M. A., Preuss, D., Mulholland, J., Botstein, D., and Jones, E. W. (1992). The VPH1 gene encodes a 95-kDa integral membrane polypeptide required for in vivo assembly and activity of the yeast vacuolar H+-ATPase. J. Biol. Chem. 267, 14294-14303.
45. Maxfield, F. R., and Tabas, I. (2005). Role of cholesterol and lipid organization in disease. Nature 438, 612-621.
46. Nerlich, A., von Orlow, M., Rontein, D., Hanson, A. D., and Dormann, P. (2007). Deficiency in phosphatidylserine decarboxylase activity in the psd1 psd2 psd3 triple mutant of Arabidopsis affects phosphatidylethanolamine accumulation in mitochondria. Plant Physiol. 144, 904-914.
47. Opekarova, M., Malinska, K., Novakova, L., and Tanner, W. (2005). Differential effect of phosphatidylethanolamine depletion on raft proteins: further evidence for diversity of rafts in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1711, 87-95.
48. Rose, M. D., Misra, L. M., and Vogel, J. P. (1989). KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57, 1211-1221.
49. Schuiki, I., and Daum, G. (2009). Phosphatidylserine decarboxylases, key enzymes of lipid metabolism. IUBMB Life 61, 151-162.
50. 2+-ATPases. Nature 319, 689-693.
51. Sharma, K. G., Mason, D. L., Liu, G., Rea, P. A., Bachhawat, A. K., and Michaelis, S. (2002). Localization, regulation, and substrate transport properties of Bpt1p, a Saccharomyces cerevisiae MRP-type ABC transporter. Eukaryot. Cell 1, 391-400.
52. Sherman, F., Fink, G., and Hicks, J. (1979). Methods in Yeast Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
53. Singer-Kruger, B., Frank, R., Crausaz, F., and Riezman, H. (1993). Partial purification and characterization of early and late endosomes from yeast. Identification of four novel proteins. J. Biol. Chem. 268, 14376-14386.
54. Smirnov, M. N., Smirnov, V. N., Budowsky, E. I., Inge-Vechtomov, S. G., and Serebrjakov, N. G. (1967). Red pigment of adenine-deficient yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 27, 299-304.
55. Sturley, S. L. (2000). Conservation of eukaryotic sterol homeostasis: new insights from studies in budding yeast. Biochim. Biophys. Acta 1529, 155-163.
56. Szczypka, M. S., Wemmie, J. A., Moye-Rowley, W. S., and Thiele, D. J. (1994). A yeast metal resistance protein similar to human CFTR and multidrug resistance-associated protein. J. Biol. Chem. 269, 22853-22857.
57. Tommasini, R., Evers, R., Vogt, E., Mornet, C., Zaman, G.J.R., Schinkel, A. H., Borst, P., and Martinoia, E. (1996). The human multidrug resistance-associated protein functionally complements the yeast cadmium factor 1. Proc. Natl. Acad. Sci. USA 93, 6743-6748.
58. Trotter, P. J., Pedretti, J., and Voelker, D. R. (1993). Phosphatidylserine decarboxylase from Saccharomyces cerevisiae. Isolation of mutants, cloning of the gene, and creation of a null allele. J. Biol. Chem. 268, 21416-21424.
59. Trotter, P. J., Pedretti, J., Yates, R., and Voelker, D. R. (1995). Phosphatidylserine decarboxylase 2 of Saccharomyces cerevisiae. Cloning and mapping of the gene, heterologous expression, and creation of the null allele. J. Biol. Chem. 270, 6071-6080.
60. Trotter, P. J., and Voelker, D. R. (1995). Identification of a non-mitochondrial phosphatidylserine decarboxylase activity (PSD2) in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 270, 6062-6070.
61. Umebayashi, K., and Nakano, A. (2003). Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. J. Cell Biol. 161, 1117-1131.
62. van den Hazel, H. B., Pichler, H., do Valle Matta, M. A., Leitner, E., Goffeau, A., and Daum, G. (1999). PDR16 and PDR17, two homologous genes of Saccharomyces cerevisiae, affect lipid biosynthesis and resistance to multiple drugs. J. Biol. Chem. 274, 1934-1941.
63. van Meer, G. (2005). Cellular lipidomics. EMBO J. 24, 3159-3165.
64. Vance, J. E. (2003). Molecular and cell biology of phosphatidylserine and phosphatidylethanolamine metabolism. Prog Nucleic Acid Res Mol Biol 75, 69-111.
65. Vida, T. A., and Emr, S. D. (1995). A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779-792.
66. Vida, T. A., Graham, T. R., and Emr, S. D. (1990). In vitro reconstitution of intercompartmental protein transport to the yeast vacuole. J. Cell Biol. 111, 2871-2884.
67. Voelker, D. R. (1997). Phosphatidylserine decarboxylase. Biochim. Biophys. Acta 1348, 236-244.
68. Wang, X., Bogdanov, M., and Dowhan, W. (2002). Topology of polytopic membrane protein subdomains is dictated by membrane phospholipid composition. EMBO J. 21, 5673-5681.
69. Wemmie, J. A., and Moye-Rowley, W. S. (1997). Mutational analysis of the Saccharomyces cerevisiae ATP-binding cassette transporter protein Ycf1p. Mol. Microbiol. 25, 683-694.
70. Wemmie, J. A., Szczypka, M. S., Thiele, D. J., and Moye-Rowley, W. S. (1994). Cadmium tolerance mediated by the yeast AP-1 protein requires the presence of an ATP-binding cassette transporter-encoding gene, YCF1. J. Biol. Chem. 269, 32592-32597.
71. Wu, W. I., Routt, S., Bankaitis, V. A., and Voelker, D. R. (2000). A new gene involved in the transport-dependent metabolism of phosphatidylserine, PSTB2/PDR17, shares sequence similarity with the gene encoding the phosphatidylinositol/ phosphatidylcholine transfer protein, SEC14. J. Biol. Chem. 275, 14446-14456.
72. Wu, W. I., and Voelker, D. R. (2001). Characterization of phosphatidylserine transport to the locus of phosphatidylserine decarboxylase 2 in permeabilized yeast. J. Biol. Chem. 276, 7114-7121.
73. Yamashiro, C. T., Kane, P. M., Wolczyk, D. F., Preston, R. A., and Stevens, T. H. (1990). Role of vacuolar acidification in protein sorting and zymogen activation: a genetic analysis of the yeast vacuolar proton-translocating ATPase. Mol. Cell. Biol. 10, 3737-3749.
74. Zhang, W., Bogdanov, M., Pi, J., Pittard, A. J., and Dowhan, W. (2003). Reversible topological organization within a polytopic membrane protein is governed by a change in membrane phospholipid composition. J. Biol. Chem. 278, 50128-50135.
75. o component of the mitochondrial ATPase. J. Biol. Chem. 276, 47844-47852.