Phospholipid flippases Lem3p-Dnf1p and Lem3p-Dnf2p are involved in the sorting of the tryptophan permease Tat2p in yeast

Journal of Biological Chemistry

Volumn 288, Issue 5, 2013, Pages 3594-3608

  Hachiro, Takeru ^a   Yamamoto, Takaharu ^a   Nakano, Kenji ^a   Tanaka, Kazuma ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC PHOSPHOLIPIDS; ALANINE SUBSTITUTION; ATPASES; CYTOPLASMIC LEAFLET; CYTOPLASMIC REGIONS; INTRACELLULAR MEMBRANES; LOW LEVEL; MEMBRANE PHOSPHOLIPIDS; MISLOCALIZATION; MODEL-BASED OPC; P-TYPE; PHOSPHATIDYLSERINE; TERMINAL REGIONS; TRANS-GOLGI NETWORK; UBIQUITINATION;

CELL MEMBRANES; LIPOSOMES; MACHINERY; MEMBRANES; MOLECULAR BIOLOGY; PHOSPHOLIPIDS;

AMINO ACIDS;

ADENOSINE TRIPHOSPHATASE; ALANINE; LEM3P DNF1P; LEM3P DNF2P; LIPOSOME; LYSINE; PERMEASE; PHOSPHATIDYLSERINE; PHOSPHOLIPID; TRYPTOPHAN; TRYTOPHAN PERMEASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; ENDOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; TRANS GOLGI NETWORK; UBIQUITINATION; YEAST CELL;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; AMINO ACID TRANSPORT SYSTEMS; ATP-BINDING CASSETTE TRANSPORTERS; CELL MEMBRANE; ENDOCYTOSIS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHATIDYLSERINES; PHOSPHOLIPID TRANSFER PROTEINS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-GOLGI NETWORK; TRYPTOPHAN; UBIQUITINATION; VACUOLES;

EID: 84873308688     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.416263     Document Type: Article

References (79)

1. Devaux, P. F., López-Montero, I., and Bryde, S. (2006) Proteins involved in lipid translocation in eukaryotic cells. Chem. Phys. Lipids 141, 119-132
2. Daleke, D. L. (2007) Phospholipid flippases. J. Biol. Chem. 282, 821-825
3. Lenoir, G., Williamson, P., and Holthuis, J. C. (2007) On the origin of lipid asymmetry. The flip side of ion transport. Curr. Opin. Chem. Biol. 11, 654-661
4. Tanaka, K., Fujimura-Kamada, K., and Yamamoto, T. (2011) Functions of phospholipid flippases. J. Biochem. 149, 131-143
5. Sebastian, T. T., Baldridge, R. D., Xu, P., and Graham, T. R. (2012) Phospholipid flippases. Building asymmetric membranes and transport vesicles. Biochim. Biophys. Acta 1821, 1068-1077
6. Saito, K., Fujimura-Kamada, K., Furuta, N., Kato, U., Umeda, M., and Tanaka, K. (2004) Cdc50p, a protein required for polarized growth, associates with the Drs2p P-type ATPase implicated in phospholipid translocation in Saccharomyces cerevisiae. Mol. Biol. Cell 15, 3418-3432
7. 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 Ypt31pβ2p-Rcy1p pathway. Mol. Biol. Cell 18, 295-312
8. Lenoir, G., Williamson, P., Puts, C. F., and Holthuis, J. C. (2009) Cdc50p plays a vital role in the ATPase reaction cycle of the putative aminophospholipid transporter Drs2p. J. Biol. Chem. 284, 17956-17967
9. Takahashi, Y., Fujimura-Kamada, K., Kondo, S., and Tanaka, K. (2011) Isolation and characterization of novel mutations in CDC50, the noncatalytic subunit of the Drs2p phospholipid flippase. J. Biochem. 149, 423-432
10. Jacquot, A., Montigny, C, Hennrich, H., Barry, R., Le Maire, M., Jaxel, C, Holthuis, J., Champeil, P., and Lenoir, G. (2012) Phosphatidylserine stimulation of Drs2p·Cdc50p lipid translocase dephosphorylation is controlled by phosphatidylinositol 4-phosphate. J. Biol. Chem. 287, 13249-13261
11. Natarajan, P., Wang, J., Hua, Z., and Graham, T. R. (2004) Drs2p-coupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc. Natl. Acad. Sci. U. S. A. 101, 10614-10619
12. Alder-Baerens, N, Lisman, Q., Luong, L., Pomorski, T., and Holthuis, J. C. (2006) Loss of P4 ATPases Drs2p and Dnf3p disrupts aminophospholipid transport and asymmetry in yeast post-Golgi secretory vesicles. Mol. Biol. Cell 17, 1632-1642
13. Hua, Z., Fatheddin, P., and Graham, T. R. (2002) An essential subfamily of Drs2p-related P-type ATPases is required for protein trafficking between Golgi complex and endosomal/vacuolar system. Mol. Biol. Cell 13, 3162-3177
14. Pomorski, T., Lombardi, R., Riezman, H., Devaux, P. F., Van Meer, G., and Holthuis, J. C. (2003) Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol. Biol. Cell 14, 1240-1254
15. Nakano, K., Yamamoto, T., Kishimoto, T., Noji, T., and Tanaka, K. (2008) Protein kinases Fpk1p and Fpk2p are novel regulators of phospholipid asymmetry. Mol. Biol. Cell 19, 1783-1797
16. Devaux, P. F., Herrmann, A., Ohlwein, N, and Kozlov, M. M. (2008) How lipid flippases can modulate membrane structure. Biochim. Biophys. Acta 1778, 1591-1600
17. Graham, T. R., and Kozlov, M. M. (2010) Interplay of proteins and lipids in generating membrane curvature. Curr. Opin. Cell Biol. 22, 430-436
18. Saito, K., Fujimura-Kamada, K., Hanamatsu, H., Kato, U., Umeda, M., Kozminski, K. G., and Tanaka, K. (2007) Transbilayer phospholipid flipping regulates Cdc42p signaling during polarized cell growth via Rga GTPase-activating proteins. Dev. Cell 13, 743-751
19. Das, A., Slaughter, B. D., Unruh, J. R., Bradford, W. D., Alexander, R., Rubinstein, B., and Li, R. (2012) Flippase-mediated phospholipid asymmetry promotes fast Cdc42 recycling in dynamic maintenance of cell polarity. Nat. Cell Biol. 14, 304-310
20. 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
21. Lauwers, E., Erpapazoglou, Z., Haguenauer-Tsapis, R., and André, B. (2010) The ubiquitin code of yeast permease trafficking. Trends Cell Biol. 20, 196-204
22. Beck, T., Schmidt, A., and Hall, M. (1999) Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J. Cell Biol. 146, 1227-1238
23. Nakamura, H., Miura, K., Fukuda, Y., Shibuya, I., Ohta, A., and Takagi, M. (2000) Phosphatidylserine synthesis required for the maximal tryptophan transport activity in Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 64, 167-172
24. Rodríguez-Vargas, S., Sánchez-García, A., Martínez-Rivas, J. M., Prieto, J. A., and Randez-Gil, F. (2007) Fluidization of membrane lipids enhances the tolerance of Saccharomyces cerevisiae to freezing and salt stress. Appl. Environ. Microbiol. 73, 110-116
25. Rose, M. D., Winston, F., and Hieter, P. (1990) Methods in Yeast Genetics: A Laboratory Course Manual, pp. 177-186, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
26. Guthrie, C, and Fink, G. R. (eds) (1991) Guide to Yeast Genetics and Molecular Biology, Vol 194, Academic Press, San Diego
27. Elble, R. (1992) A simple and efficient procedure for transformation of yeasts. BioTechniques 13, 18-20
28. Gietz, R. D., and Woods, R. A. (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96
29. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., and Boeke, J. D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C. A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132
30. Longtine, M. S., McKenzie, A., 3rd, 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
31. Goldstein, A. L., and McCusker, J. H. (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553
32. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K., and Pease, L. R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59
33. Valdivia, R. H., and Schekman, R. (2003) The yeasts Rho1p and Pkc1p regulate the transportof chitin synthase III (Chs3p) from internal stores to the plasma membrane. Proc. Natl. Acad. Sci. U. S. A. 100, 10287-10292
34. Misu, K., Fujimura-Kamada, K., Ueda, T., Nakano, A., Katoh, H., and Tanaka, K. (2003) Cdc50p, a conserved endosomal membrane protein, controls polarized growth in Saccharomyces cerevisiae. Mol. Biol. Cell 14, 730-747
35. Bigay, J., Casella, J. F., Drin, G., Mesmin, B., and Antonny, B. (2005) Arf-GAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO J. 24, 2244-2253
36. Heitman, J., Koller, A., Kunz, J., Henriquez, R., Schmidt, A., Movva, N. R., and Hall, M. N. (1993) The immunosuppressant FK506 inhibits amino acid import in Saccharomyces cerevisiae. Mol. Cell. Biol. 13, 5010-5019
37. Mochida, J., Yamamoto, T., Fujimura-Kamada, K., and Tanaka, K. (2002) The novel adaptor protein, Mti1p, and Vrp1p, a homolog of Wiskott-Aldrich syndrome protein-interacting protein (WIP), may antagonistically regulate type I myosins in Saccharomyces cerevisiae. Genetics 160, 923-934
38. Braus, G. H. (1991) Aromatic amino acid biosynthesis in the yeast Saccharomyces cerevisiae. A model system for the regulation of a eukaryotic biosynthetic pathway. Microbiol. Rev. 55, 349-370
39. Schmidt, A., Hall, M. N., and Koller, A. (1994) Two FK506 resistanceconferring genes in Saccharomyces cerevisiae, TAT1 and TAT2, encode amino acid permeases mediating tyrosine and tryptophan uptake. Mol. Cell. Biol. 14, 6597-6606
40. Roelants, F. M., Baltz, A. G., Trott, A. E., Fereres, S., and Thorner, J. (2010) A protein kinase network regulates the function of aminophospholipid flippases. Proc. Natl. Acad. Sci. U. S. A. 107, 34-39
41. Zubenko, G. S., Park, F. J., and Jones, E. W. (1982) Genetic properties of mutations at the PEP4 locus in Saccharomyces cerevisiae. Genetics 102, 679-690
42. Jones, E. W., Zubenko, G. S., and Parker, R. R. (1982) PEP4 gene function is required for expression of several vacuolar hydrolases in Saccharomyces cerevisiae. Genetics 102, 665-677
43. Liu, K., Hua, Z., Nepute, J. A., and Graham, T. R. (2007) Yeast P4-ATPases Drs2p and Dnf1p are essential cargos of the NPFXD/Sla1p endocytic pathway. Mol. Biol. Cell 18, 487-500
44. Takagi, K., Iwamoto, K., Kobayashi, S., Horiuchi, H., Fukuda, R., and Ohta, A. (2012) Involvement of Golgi-associated retrograde protein complex in the recycling of the putative Dnf aminophospholipid flippases in yeast. Biochem. Biophys. Res. Commun. 417, 490-494
45. Vater, C. A., Raymond, C. K., Ekena, K., Howald-Stevenson, I., and Stevens, T. H. (1992) The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, isa GTPase with two functionally separable domains. J. Cell Biol. 119, 773-786
46. Bensen, E. S., Costaguta, G., and Payne, G. S. (2000) Synthetic genetic interactions with temperature-sensitive clathrin in Saccharomyces cerevisiae. Roles for synaptojanin-like Inp53p and dynamin-related Vps1p in clathrin-dependent protein sorting at the trans-Golgi network. Genetics 154, 83-97
47. Dell'Angelica, E. C, Puertollano, R., Mullins, C, Aguilar, R. C, Vargas, J. D., Hartnell, L. M., and Bonifacino, J. S. (2000) GGAs. A family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J. Cell Biol. 149, 81-94
48. Hirst, J., Lui, W. W., Bright, N. A., Totty, N., Seaman, M. N., and Robinson, M. S. (2000) A family of proteins with 7-adaptin and VHS domains that facilitate trafficking between the trans-Golgi network and the vacuole/lysosome. J. Cell Biol. 149, 67-80
49. Nothwehr, S. F., Conibear, E., and Stevens, T. H. (1995) Golgi and vacuolar membrane proteins reach the vacuole in vps1 mutant yeast cells via the plasma membrane. J. Cell Biol. 129, 35-46
50. Costaguta, G., Stefan, C. J., Bensen, E. S., Emr, S. D., and Payne, G. S. (2001) Yeast Gga coat proteins function with clathrin in Golgi to endosome transport. Mol. Biol. Cell 12, 1885-1896
51. Scott, P. M., Bilodeau, P. S., Zhdankina, O., Winistorfer, S. C., Hauglund, M. J., Allaman, M. M., Kearney, W. R., Robertson, A. D., Boman, A. L., and Piper, R. C. (2004) GGA proteins bind ubiquitin to facilitate sorting at the trans-Golgi network. Nat Cell Biol. 6, 252-259
52. 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
53. 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
54. Bilodeau, P. S., Winistorfer, S. C., Kearney, W. R., Robertson, A. D., and Piper, R. C. (2003) Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J. Cell Biol. 163, 237-243
55. Piper, R. C., Cooper, A. A., Yang, H., and Stevens, T. H. (1995) VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. J. Cell Biol. 131, 603-617
56. Katzmann, D. J., Stefan, C. J., Babst, M., and Emr, S. D. (2003) Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162, 413-423
57. Franzusoff, A., Redding, K., Crosby, J., Fuller, R. S., and Schekman, R. (1991) Localization of components involved in protein transport and processing through the yeast Golgi apparatus. J. Cell Biol. 112, 27-37
58. Tang, H. Y., Munn, A., and Cai, M. (1997) EH domain proteins Pan1p and End3p are components of a complex that plays a dual role in organization of the cortical actin cytoskeleton and endocytosis in Saccharomyces cerevisiae. Mol. Cell. Biol. 17, 4294-4304
59. Vaduva, G., Martin, N. C, and Hopper, A. K. (1997) Actin-binding verprolin is a polarity development protein required for the morphogenesis and function of the yeast actin cytoskeleton. J. Cell Biol. 139, 1821-1833
60. Raths, S., Rohrer, J., Crausaz, F., and Riezman, H. (1993) end3 and end4. Two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J. Cell Biol. 120, 55-65
61. Munn, A. L., Stevenson, B. J., Geli, M. I., and Riezman, H. (1995) end5, end6, and end7. Mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell 6, 1721-1742
62. Takagi, K., Iwamoto, K., Kobayashi, S., Horiuchi, H., Fukuda, R., and Ohta, A. (2012) Involvement of Golgi-associated retrograde protein complex in the recycling of the putative Dnf aminophospholipid flippases in yeast. Biochem. Biophys. Res. Commun. 417, 490-494
63. Risinger, A. L., and Kaiser, C A. (2008) Different ubiquitin signals act at the Golgi and plasma membrane to direct GAP1 trafficking. Mol. Biol. Cell 19, 2962-2972
64. Kato, U., Emoto, K., Fredriksson, C, Nakamura, H., Ohta, A., Kobayashi, T., Murakami-Murofushi, K., Kobayashi, T., and Umeda, M. (2002) A novel membrane protein, Ros3p, is required for phospholipid translocation across the plasma membrane in Saccharomyces cerevisiae. J. Biol. Chem. 277, 37855-37862
65. Nagayama, A., Kato, C, and Abe, F. (2004) The N-and C-terminal mutations in tryptophan permease Tat2 confer cell growth in Saccharomyces cerevisiae under high pressure and low-temperature conditions. Extremophiles 8, 143-149
66. Surma, M. A., Klose, C, and Simons, K. (2012) Lipid-dependent protein sorting at the trans-Golgi network. Biochim. Biophys. Acta 1821, 1059-1067
67. Klemm, R. W., Ejsing, C. S., Surma, M. A., Kaiser, H. J., Gerl, M. J., Sampaio, J. L., De Robillard, Q., Ferguson, C, Proszynski, T. J., Shevchenko, A., and Simons, K. (2009) Segregation of sphingolipids and sterols during formation of secretory vesicles at the trans-Golgi network. J. Cell Biol. 185, 601-612
68. Bauer, B. E., Rossington, D., Mollapour, M., Mamnun, Y., Kuchler, K., and Piper, P. W. (2003) Weak organic acid stress inhibits aromatic amino acid uptake by yeast, causing a strong influence of amino acid auxotrophies on the phenotypes of membrane transporter mutants. Eur. J. Biochem. 270, 3189-3195
69. +/H+ exchanger. EMBOJ. 30, 679-691
70. Krishna, A. G., Menon, S. T., Terry, T. J., and Sakmar, T. P. (2002) Evidence that helix 8 of rhodopsin acts as a membrane-dependent conformational switch. Biochemistry 41, 8298-8309
71. McLaughlin, S., Smith, S. O., Hayman, M. J., and Murray, D. (2005) An electrostatic engine model for autoinhibition and activation of the epidermal growth factor receptor (EGFR/ErbB) family. J. Gen. Physiol. 126, 41-53
72. Stevens, H. C., Malone, L., and Nichols, J. W. (2008) The putative aminophospholipid translocases, DNF1 and DNF2, are not required for 7-nitrobenz-2-oxa-1, 3-diazol-4-yl-phosphatidylserine flip across the plasma membrane of Saccharomyces cerevisiae. J. Biol. Chem. 283, 35060-35069
73. Baldridge, R. D., and Graham, T. R. (2012) Identification of residues defining phospholipid flippase substrate specificity of type IV P-type ATPases. Proc. Natl. Acad. Sci. U. S. A. 109, E290-E298
74. Parsons, A. B., Lopez, A., Givoni, I. E., Williams, D. E., Gray, C. A., Porter, J., Chua, G., Sopko, R., Brost, R. L., Ho, C. H., Wang, J., Ketela, T., Brenner, C., Brill, J. A., Fernandez, G. E., Lorenz, T. C., Payne, G. S., Ishihara, S., Ohya, Y., Andrews, B., Hughes, T. R., Frey, B. J., Graham, T. R., Andersen, R. J., and Boone, C. (2006) Exploring the mode-of-action ofbioactive compounds by chemical-genetic profiling in yeast. Cell 126, 611-625
75. Guo, Y., Au, W. C., Shakoury-Elizeh, M., Protchenko, O., Basrai, M., Prinz, W. A., and Philpott, C. C. (2010) Phosphatidylserine is involved in the ferrichrome-induced plasma membrane trafficking of Arn1 in Saccharomyces cerevisiae. J. Biol. Chem. 285, 39564-39573
76. Gietz, R. D., and Sugino, A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitromutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534
77. Kikyo, M., Tanaka, K., Kamei, T., Ozaki, K., Fujiwara, T., Inoue, E., Takita, Y., Ohya, Y., and Takai, Y. (1999) An FH domain-containing Bnr1p is a multifunctional protein interacting with a variety of cytoskeletal proteins in Saccharomyces cerevisiae. Oncogene 18, 7046-7054
78. Abe, F., and Iida, H. (2003) Pressure-induced differential regulation of the two tryptophan permeases Tat1 and Tat2 by ubiquitin ligase Rsp5 and its binding proteins, Bul1 and Bul2. Mol. Cell. Biol. 23, 7566-7584
79. Abe, F., and Horikoshi, K. (2000) Tryptophan permease gene TAT2 confers high pressure growth in Saccharomyces cerevisiae. Mol. Cell. Biol. 20, 8093-8102