TORC2 plasma membrane localization is essential for cell viability and restricted to a distinct domain

Molecular Biology of the Cell

Volumn 20, Issue 5, 2009, Pages 1565-1575

  Berchtold, Doris ^a   Walther, Tobias C ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN; PROTEIN TORC1; PROTEIN TORC2; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL VIABILITY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE;

BINDING SITES; CARRIER PROTEINS; CELL MEMBRANE; CELL SURVIVAL; GREEN FLUORESCENT PROTEINS; INTRACELLULAR MEMBRANES; LIPID METABOLISM; MEMBRANE PROTEINS; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; VACUOLES;

SACCHAROMYCES CEREVISIAE;

EID: 63749117393     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-10-1001     Document Type: Article

References (65)

1. Araki, T., Uesono, Y., Oguchi, T., and Toh, E. A. (2005). LAS24/KOG1, a component of the TOR complex 1 (TORC1), is needed for resistance to local anesthetic tetracaine and normal distribution of actin cytoskeleton in yeast. Genes Genet. Syst. 80, 325-343.
2. Aronova, S., Wedaman, K., Anderson, S., Yates, J., 3rd, and Powers, T. (2007). Probing the membrane environment of the TOR kinases reveals functional interactions between TORC1, actin, and membrane trafficking in Saccharomyces cerevisiae. Mol. Biol. Cell. 18, 2779-2794.
3. Aronova, S., Wedaman, K., Aronov, P. A., Fontes, K., Ramos, K., Hammock, B. D., and Powers, T. (2008). Regulation of ceramide biosynthesis by TOR complex 2. Cell Metab. 7, 148-158.
4. Audhya, A., Loewith, R., Parsons, A. B., Gao, L., Tabuchi, M., Zhou, H., Boone, C., Hall, M. N., and Emr, S. D. (2004). Genome-wide lethality screen identifies new PI4,5P2 effectors that regulate the actin cytoskeleton. EMBO J. 23, 3747-3757.
5. Bagnat, M., Keranen, 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.
6. Bagnat, M., and Simons, K. (2002). Lipid rafts in protein sorting and cell polarity in budding yeast Saccharomyces cerevisiae. Biol. Chem. 383,1475-1480.
7. Beeler, T., Bacikova, D., Gable, K., Hopkins, L., Johnson, C., Slife, H., and Dunn, T. (1998). The Saccharomyces cerevisiae TSC10/YBR265w gene encoding 3-ketosphinganine reductase is identified in a screen for temperature-sensitive suppressors of the Ca2+-sensitive csg2Delta mutant. J. Biol. Chem. 273, 30688-30694.
8. Brickner, J. H., and Walter, P. (2004). Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 2, e342.
9. Cardenas, M. E., and Heitman, J. (1995). FKBP12-rapamycin target TOR2 is a vacuolar protein with an associated phosphatidylinositol-4 kinase activity. EMBO J. 14, 5892-5907.
10. Casamayor, A., Torrance, P. D., Kobayashi, T., Thorner, J., and Alessi, D. R. (1999). Functional counterparts of mammalian protein kinases PDK1 and SGK in budding yeast. Curr. Biol. 9, 186-197.
11. Chen, E. J., and Kaiser, C. A. (2003). LST8 negatively regulates amino acid biosynthesis as a component of the TOR pathway. J. Cell Biol. 161, 333-347.
12. Daquinag, A., Fadri, M., Jung, S. Y., Qin, J., and Kunz, J. (2007). The yeast PH domain proteins Slm1 and Slm2 are targets of sphingolipid signaling during the response to heat stress. Mol. Cell. Biol. 27, 633-650.
13. De Virgilio, C., and Loewith, R. (2006). Cell growth control: little eukaryotes make big contributions. Oncogene 25, 6392-6415.
14. deHart, A. K., Schnell, J. D., Allen, D. A., Tsai, J. Y., and Hicke, L. (2003). Receptor internalization in yeast requires the Tor2-Rho1 signaling pathway. Mol. Biol. Cell. 14, 4676-4684.
15. Fadri, M., Daquinag, A., Wang, S., Xue, T., and Kunz, J. (2005). The pleckstrin homology domain proteins Slm1 and Slm2 are required for actin cytoskeleton organization in yeast and bind phosphatidylinositol-4,5- bisphosphate and TORC2. Mol. Biol. Cell. 16, 1883-1900.
16. Friant, S., Lombardi, R., Schmelzle, T., Hall, M. N., and Riezman, H. (2001). Sphingoid base signaling via Pkh kinases is required for endocytosis in yeast. EMBO J. 20, 6783-6792.
17. Grossmann, G., Opekarova, M., Malinsky, J., Weig-Meckl, I., and Tanner, W. (2007). Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J. 26,1-8.
18. Grossmann, G., Opekarova, M., Novakova, L., Stolz, J., and Tanner, W. (2006). Lipid raft-based membrane compartmentation of a plant transport protein expressed in Saccharomyces cerevisiae. Eukaryot. Cell 5, 945-953.
19. Heitman, J., Movva, N. R., and Hall, M. N. (1991). Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253, 905-909.
20. 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.
21. Inagaki, M., Schmelzle, T., Yamaguchi, K., Irie, K., Hall, M. N., and Matsumoto, K. (1999). PDK1 homologs activate the Pkc1-mitogen-activated protein kinase pathway in yeast. Mol. Cell. Biol. 19, 8344-8352.
22. Jacinto, E., Loewith, R., Schmidt, A., Lin, S., Ruegg, M. A., Hall, A., and Hall, M. N. (2004). Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat. Cell Biol. 6, 1122-1128.
23. Janke, C., 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.
24. Joglekar, A. P., Salmon, E. D., and Bloom, K. S. (2008). Counting kinetochore protein numbers in budding yeast using genetically encoded fluorescent proteins. Methods Cell Biol. 85, 127-151.
25. Jorgensen, P., Rupes, I., Sharom, J. R., Schneper, L., Broach, J. R., and Tyers, M. (2004). A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev. 18, 2491-2505.
26. Kaksonen, M., Sun, Y., and Drubin, D. G. (2003). A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115, 475-487.
27. Kaksonen, M., Toret, C. P., and Drubin, D. G. (2005). A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305-320.
28. Kamada, Y., Fujioka, Y., Suzuki, N. N., Inagaki, F., Wullschleger, S., Loewith, R., Hall, M. N., and Ohsumi, Y. (2005). Tor2 directlyphosphorylates the AGC kinase Ypk2 to regulate actin polarization. Mol. Cell. Biol. 25, 7239-7248.
29. Kim,D. H.,Sarbassov,D. D.,Ali,S. M.,Latek,R. R.,Guntur,K. V.,ErdjumentBromage, H., Tempst, P., and Sabatini, D. M. (2003). GbetaL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol. Cell 11, 895-904.
30. Kunz, J., Schneider, U., Howald, I., Schmidt, A., and Hall, M. N. (2000). HEAT repeats mediate plasma membrane localization of Tor2p in yeast. J. Biol. Chem. 275, 37011-37020.
31. Lee, M. C., Hamamoto, S., and Schekman, R. (2002). Ceramide biosynthesis is required for the formation of the oligomeric H+-ATPase Pma1p in the yeast endoplasmic reticulum. J. Biol. Chem. 277, 22395-22401.
32. Lee, S., Comer, F. I., Sasaki, A., McLeod, I. X., Duong, Y., Okumura, K., Yates, J. R., 3rd, Parent, C. A., and Firtel, R. A. (2005). TOR complex 2 integrates cell movement during chemotaxis and signal relay in Dictyostelium. Mol. Biol. Cell. 16, 4572-4583.
33. Lemmon, M. A. (2008). Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111.
34. Liu, K., Zhang, X., Sumanasekera, C., Lester, R. L., and Dickson, R. C. (2005). Signalling functions for sphingolipid long-chain bases in Saccharomyces cerevisiae. Biochem. Soc. Trans. 33, 1170-1173.
35. Loewith, R., Jacinto, E., Wullschleger, S., Lorberg, A., Crespo, J. L., Bonenfant, D., Oppliger, W., Jenoe, P., and Hall, M. N. (2002). Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10, 457-468.
36. Malinska, K., Malinsky, J., Opekarova, M., and Tanner, W. (2003). Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol. Biol. Cell 14, 4427-4436.
37. Malinska,K.,Malinsky,J.,Opekarova,M.,and Tanner,W. (2004). Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J. Cell Sci. 117, 6031-6041.
38. Narayan, K., and Lemmon, M. A. (2006). Determining selectivity of phosphoi- nositide-binding domains. Methods 39, 122-133.
39. Odorizzi, G., Babst, M., and Emr, S. D. (2000). Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem. Sci. 25, 229-235.
40. Onken, B., Wiener, H., Philips, M. R., and Chang, E. C. (2006). Compartmentalized signaling of Ras in fission yeast. Proc. Natl. Acad. Sci. USA 103, 9045-9050.
41. Puria, R., Zurita-Martinez, S. A., and Cardenas, M. E. (2008). Nuclear trans- location of Gln3 in response to nutrient signals requires Golgi-to-endosome trafficking in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 105, 7194-7199.
42. Reiling, J. H., and Sabatini, D. M. (2006). Stress and mTORture signaling. Oncogene 25, 6373-6383.
43. Reinke, A., Anderson, S., McCaffery, J. M., Yates, J., 3rd, Aronova, S., Chu, S., Fairclough, S., Iverson, C., Wedaman, K. P., and Powers, T. (2004). TOR complex 1 includes a novel component, Tco89p (YPL180w), and cooperates with Ssd1p to maintain cellular integrity in Saccharomyces cerevisiae. J. Biol. Chem. 279, 14752-14762.
44. Sarbassov, D. D., Ali, S. M., Kim, D. H., Guertin, D. A., Latek, R. R., Erdjument- Bromage, H., Tempst, P., and Sabatini, D. M. (2004). Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14, 1296-1302.
45. Sarbassov, D. D., Guertin, D. A., Ali, S. M., and Sabatini, D. M. (2005). Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101.
46. Schmidt, A., Beck, T., Koller, A., Kunz, J., and Hall, M. N. (1998). The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J. 17, 6924-6931.
47. Schmidt, A., Bickle, M., Beck, T., and Hall, M. N. (1997). The yeast phosphatidylinositol kinase homolog TOR2 activates RHO1 and RHO2 via the exchange factor ROM2. Cell 88, 531-542.
48. Schroder, W. A., Buck, M., Cloonan, N., Hancock, J. F., Suhrbier, A., Sculley, T., and Bushell, G. (2007). Human Sin1 contains Ras-binding and pleckstrin homology domains and suppresses Ras signalling. Cell Signal. 19, 1279-1289.
49. Schwartz, M. A., and Madhani, H. D. (2006). Control of MAPK signaling specificity by a conserved residue in the MEK-binding domain of the yeast scaffold protein Ste5. Curr. Genet. 49, 351-363.
50. Simons, K., and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
51. Smith, F. D., Langeberg, L. K., and Scott, J. D. (2006). The where's and when's of kinase anchoring. Trends Biochem. Sci. 31, 316-323.
52. Sturgill, T. W., Cohen, A., Diefenbacher, M., Trautwein, M., Martin, D., and Hall, M. N. (2008). TOR1 and TOR2 have distinct locations in live cells. Eukaryot. Cell 10, 1819-1830.
53. Sun, Y., Taniguchi, R., Tanoue, D., Yamaji, T., Takematsu, H., Mori, K., Fujita, T., Kawasaki, T., and Kozutsumi, Y. (2000). Sli2 (Ypk1), a homologue of mammalian protein kinase SGK, is a downstream kinase in the sphingolipid- mediated signaling pathway of yeast. Mol. Cell. Biol. 20, 4411-4419.
54. Tabuchi, M., Audhya, A., Parsons, A. B., Boone, C., and Emr, S. D. (2006). The phosphatidylinositol 4,5-biphosphate and TORC2 binding proteins Slm1 and Slm2 function in sphingolipid regulation. Mol. Cell. Biol. 26, 5861-5875.
55. Toshima, J. Y., Toshima, J., Kaksonen, M., Martin, A. C., King, D. S., and Drubin, D. G. (2006). Spatial dynamics of receptor-mediated endocytic trafficking in budding yeast revealed by using fluorescent alpha-factor derivatives. Proc. Natl. Acad. Sci. USA 103, 5793-5798.
56. Tsang, C. K., and Zheng, X. F. (2007). TOR-in(g) the nucleus. Cell Cycle 6, 25-29.
57. Urban, J., et al. (2007). Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol. Cell. 26, 663-674.
58. van Meer, G., and Lisman, Q. (2002). Sphingolipid transport: rafts and translocators. J. Biol. Chem. 277, 25855-25858.
59. Walther, T. C., Aguilar, P. S., Frohlich, F., Chu, F., Moreira, K., Burlingame, A. L., and Walter, P. (2007). Pkh-kinases control eisosome assembly and organization. EMBO J. 26, 4946-4955.
60. Walther, T. C., Brickner, J. H., Aguilar, P. S., Bernales, S., Pantoja, C., and Walter, P. (2006). Eisosomes mark static sites of endocytosis. Nature 439, 998-1003.
61. Wedaman, K. P., Reinke, A., Anderson, S., Yates, J., 3rd, McCaffery, J. M., and Powers, T. (2003). Tor kinases are in distinct membrane-associated protein complexes in Saccharomyces cerevisiae. Mol. Biol. Cell. 14, 1204-1220.
62. Wullschleger, S., Loewith, R., and Hall, M. N. (2006). TOR signaling in growth and metabolism. Cell 124, 471-484.
63. Wullschleger, S., Loewith, R., Oppliger, W., and Hall, M. N. (2005). Molecular organization of target of rapamycin complex 2. J. Biol. Chem. 280, 30697-30704.
64. Zacharias, D. A., Violin, J. D., Newton, A. C., and Tsien, R. Y. (2002). Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913-916.
65. Zurita-Martinez, S. A., Puria, R., Pan, X., Boeke, J. D., and Cardenas, M. E. (2007). Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae. Genetics 176, 2139-2150.