Endolysosomal membrane trafficking complexes drive nutrient-dependent TORC1 signaling to control cell growth in Saccharomyces cerevisiae

Genetics

Volumn 196, Issue 4, 2014, Pages 1077-1089

  Kingsbury, Joanne M ^a   Sen, Neelam D ^a,c   Maeda, Tatsuya ^b   Heitman, Joseph ^a   Cardenas, Maria E ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; GUANOSINE TRIPHOSPHATASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN P70; RAPAMYCIN; ANTIFUNGAL AGENT; SACCHAROMYCES CEREVISIAE PROTEIN; TORC1 PROTEIN COMPLEX, S CEREVISIAE; TRANSCRIPTION FACTOR; VESICULAR TRANSPORT PROTEIN;

ALLELE; AMINO ACID METABOLISM; ARTICLE; CELL GROWTH; CELL MEMBRANE; COMPLEX FORMATION; GENOTYPE; LYSOSOME; MAMMAL; MINIMUM INHIBITORY CONCENTRATION; MUTANT; NONHUMAN; NUTRIENT; ORTHOLOGY; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; YEAST; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; SIGNAL TRANSDUCTION;

AMINO ACIDS; ANTIFUNGAL AGENTS; CELL PROLIFERATION; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SIROLIMUS; TRANSCRIPTION FACTORS; VESICULAR TRANSPORT PROTEINS;

EID: 84901319212     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.161646     Document Type: Article

References (70)

1. Alarcon, C. M., M. E. Cardenas, and J. Heitman, 1996 Mammalian RAFT1 kinase domain provides rapamycin-sensitive TOR function in yeast. Genes Dev. 10: 279-288.
2. Araki, T., Y. Uesono, T. Oguchi, and E. A. Toh, 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.
3. Banta, L. M., J. S. Robinson, D. J. Klionsky, and S. D. Emr, 1988 Organelle assembly in yeast: characterization of yeast mutants defective in vacuolar biogenesis and protein sorting. J. Cell Biol. 107: 1369-1383.
4. Berchtold, D., and T. C. Walther, 2009 TORC2 plasma membrane localization is essential for cell viability and restricted to a distinct domain. Mol. Biol. Cell 20: 1565-1575.
5. Binda, M., M. P. Peli-Gulli, G. Bonfils, N. Panchaud, J. Urban et al., 2009 The Vam6 GEF controls TORC1 by activating the EGO complex. Mol. Cell 35: 563-573.
6. Bonfils, G., M. Jaquenoud, S. Bontron, C. Ostrowicz, C. Ungermann et al., 2012 Leucyl-tRNA synthetase controls TORC1 via the EGO complex. Mol. Cell 46: 105-110.
7. Brachmann, C. B., A. Davies, G. J. Cost, E. Caputo, J. Li et al., 1998 Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCRmediated gene disruption and other applications. Yeast 14: 115-132.
8. Cardenas, M. E., and J. Heitman, 1995 FKBP12-rapamycin target TOR2 is a vacuolar protein with an associated phosphatidylinositol-4 kinase activity. EMBO J. 14: 5892-5907.
9. Cardenas, M. E., N. S. Cutler, M. C. Lorenz, C. J. Di Como, and J. Heitman, 1999 The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev. 13: 3271-3279.
10. Di Como, C. J., and K. T. Arndt, 1996 Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 10: 1904-1916.
11. Dubouloz, F., O. Deloche, V. Wanke, E. Cameroni, and C. De Virgilio, 2005 The TOR and EGO protein complexes orchestrate microautophagy in yeast. Mol. Cell 19: 15-26.
12. Duvel, K., A. Santhanam, S. Garrett, L. Schneper, and J. R. Broach, 2003 Multiple roles of Tap42 in mediating rapamycin-induced transcriptional changes in yeast. Mol. Cell 11: 1467-1478.
13. Epp, N., R. Rethmeier, L. Kramer, andC. Ungermann, 2011 Membrane dynamics and fusion at late endosomes and vacuoles-Rab regulation, multisubunit tethering complexes and SNAREs. Eur. J. Cell Biol. 90: 779-785.
14. Flinn, R. J., and J. M. Backer, 2010 mTORC1 signals from late endosomes: taking a TOR of the endocytic system. Cell Cycle 9: 1869-1870.
15. Flinn, R. J., Y. Yan, S. Goswami, P. J. Parker, and J. M. Backer, 2010 The late endosome is essential for mTORC1 signaling. Mol. Biol. Cell 21: 833-841.
16. Gao, M., and C. A. Kaiser, 2006 A conserved GTPase-containing complex is required for intracellular sorting of the general amino-acid permease in yeast. Nat. Cell Biol. 8: 657-667.
17. Garipler, G., and C. D. Dunn, 2013 Defects associated with mitochondrial DNA damage can be mitigated by increased vacuolar pH in Saccharomyces cerevisiae. Genetics 194: 285-290.
18. Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles et al., 2002 Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
19. Gietz, R. D., R. H. Schiestl, A. R. Willems, and R. A. Woods, 1995 Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355-360.
20. Goldstein, A. L., and J. H. McCusker, 1999 Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
21. Heitman, J., N. R. Movva, and M. N. Hall, 1991 Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253: 905-909.
22. Hickey, C. M., C. Stroupe, and W. Wickner, 2009 The major role of the Rab Ypt7p in vacuole fusion is supporting HOPS membrane association. J. Biol. Chem. 284: 16118-16125.
23. +-translocating adenosine triphosphatase from vacuolar membranes of Saccharomyces cerevisiae. J. Biol. Chem. 265: 6726-6733.
24. Hughes, A. L., and D. E. Gottschling, 2012 An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492: 261-265.
25. Huh, W. K., J. V. Falvo, L. C. Gerke, A. S. Carroll, R. W. Howson et al., 2003 Global analysis of protein localization in budding yeast. Nature 425: 686-691.
26. +-ATPase assembly. J. Biol. Chem. 272: 25928-25934.
27. Jorgensen, P., I. Rupes, J. R. Sharom, L. Schneper, J. R. Broach et al., 2004 A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev. 18: 2491-2505.
28. Kane, P. M., 2006 The where, when, and how of organelle acidification by the yeast vacuolar H+-ATPase. Microbiol. Mol. Biol. Rev. 70: 177-191.
29. Kitamoto, K., K. Yoshizawa, Y. Ohsumi, and Y. Anraku, 1988a Dynamic aspects of vacuolar and cytosolic amino acid pools of Saccharomyces cerevisiae. J. Bacteriol. 170: 2683-2686.
30. Kitamoto, K., K. Yoshizawa, Y. Ohsumi, and Y. Anraku, 1988b Mutants of Saccharomyces cerevisiae with defective vacuolar function. J. Bacteriol. 170: 2687-2691.
31. Klionsky, D. J., 2005 The molecular machinery of autophagy: unanswered questions. J. Cell Sci. 118: 7-18.
32. Liang, C., J. S. Lee, K. S. Inn, M. U. Gack, Q. Li et al., 2008 Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 10: 776-787.
33. Loewith, R., and M. N. Hall, 2011 Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189: 1177-1201.
34. Loewith, R., E. Jacinto, S. Wullschleger, A. Lorberg, J. L. Crespo et al., 2002 Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10: 457-468.
35. Nakashima, N., N. Hayashi, E. Noguchi, and T. Nishimoto, 1996 Putative GTPase Gtr1p genetically interacts with the RanGTPase cycle in Saccharomyces cerevisiae. J. Cell Sci. 109 (Pt 9): 2311-2318.
36. Nakashima, N., E. Noguchi, and T. Nishimoto, 1999 Saccharomyces cerevisiae putative G protein, Gtr1p, which forms complexes with itself and a novel protein designated as Gtr2p, negatively regulates the Ran/Gsp1p G protein cycle through Gtr2p. Genetics 152: 853-867.
37. Nickerson, D. P., C. L. Brett, and A. J. Merz, 2009 Vps-C complexes: gatekeepers of endolysosomal traffic. Curr. Opin. Cell Biol. 21: 543-551.
38. Oldenburg, K. R., K. T. Vo, S. Michaelis, and C. Paddon, 1997 Recombination-mediated PCR-directed plasmid construction in vivo in yeast. Nucleic Acids Res. 25: 451-452.
39. Onodera, J., and Y. Ohsumi, 2005 Autophagy is required for maintenance of amino acid levels and protein synthesis under nitrogen starvation. J. Biol. Chem. 280: 31582-31586.
40. Ostrowicz, C. W., C. Brocker, F. Ahnert, M. Nordmann, J. Lachmann et al., 2010 Defined subunit arrangement and Rab interactions are required for functionality of the HOPS tethering complex. Traffic 11: 1334-1346.
41. Peplowska, K., D. F. Markgraf, C. W. Ostrowicz, G. Bange, and C. Ungermann, 2007 The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endolysosomal biogenesis. Dev. Cell 12: 739-750.
42. Peterson, M. R., and S. D. Emr, 2001 The class C Vps complex functions at multiple stages of the vacuolar transport pathway. Traffic 2: 476-486.
43. Powers, T., and P. Walter, 1999 Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol. Biol. Cell 10: 987-1000.
44. Puria, R., S. A. Zurita-Martinez, and M. E. Cardenas, 2008 Nuclear translocation of Gln3 in response to nutrient signals requires Golgi-to-endosome trafficking in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 105: 7194-7199.
45. Raymond, C. K., I. Howald-Stevenson, C. A. Vater, and T. H. Stevens, 1992 Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3: 1389-1402.
46. Reinke, A., S. Anderson, J. M. McCaffery, J. Yates, III, S. Aronova et al., 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.
47. Rohde, J. R., R. Bastidas, R. Puria, and M. E. Cardenas, 2008 Nutritional control via Tor signaling in Saccharomyces cerevisiae. Curr. Opin. Microbiol. 11: 153-160.
48. Rothman, J.H., I. Howald, andT. H. Stevens, 1989a Characterization of genes required for protein sorting and vacuolar function in the yeast Saccharomyces cerevisiae. EMBO J. 8: 2057-2065.
49. +-ATPase are deficient in two yeast mutants that fail to sort vacuolar proteins. J. Cell Biol. 109: 93-100.
50. Russnak, R., D. Konczal, and S. L. McIntire, 2001 A family of yeast proteins mediating bidirectional vacuolar amino acid transport. J. Biol. Chem. 276: 23849-23857.
51. Sambade, M., M. Alba, A. M. Smardon, R. W. West, and P. M. Kane, 2005 A genomic screen for yeast vacuolar membrane ATPase mutants. Genetics 170: 1539-1551.
52. Sancak, Y., T. R. Peterson, Y. D. Shaul, R. A. Lindquist, C. C. Thoreen et al., 2008 The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320: 1496-1501.
53. Sancak, Y., L. Bar-Peled, R. Zoncu, A. L. Markhard, S. Nada et al., 2010 Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141: 290-303.
54. Schauer, A., H. Knauer, C. Ruckenstuhl, H. Fussi, M. Durchschlag et al., 2009 Vacuolar functions determine the mode of cell death. Biochim. Biophys. Acta 1793: 540-545.
55. Schmidt, A., J. Kunz, and M. N. Hall, 1996 TOR2 is required for organization of the actin cytoskeleton in yeast. Proc. Natl. Acad. Sci. USA 93: 13780-13785.
56. Sherman, F., G. R. Fink, and C. W. Lawrence, 1974 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. Srivastava, A., C. A. Woolford, and E. W. Jones, 2000 Pep3p/Pep5p complex: a putative docking factor at multiple steps of vesicular transport to the vacuole of Saccharomyces cerevisiae. Genetics 156: 105-122.
58. Stroupe, C., K. M. Collins, R. A. Fratti, and W. Wickner, 2006 Purification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p. EMBO J. 25: 1579-1589.
59. Sturgill, T. W., A. Cohen, M. Diefenbacher, M. Trautwein, D. E. Martin et al., 2008 TOR1 and TOR2 have distinct locations in live cells. Eukaryot. Cell 7: 1819-1830.
60. Takahara, T., and T. Maeda, 2012 Transient sequestration of TORC1 into stress granules during heat stress. Mol. Cell 47: 242-252.
61. te Welscher, Y. M., L. Jones, M. R. van Leeuwen, J. Dijksterhuis, B. de Kruijff et al., 2010 Natamycin inhibits vacuole fusion at the priming phase via a specific interaction with ergosterol. Antimicrob. Agents Chemother. 54: 2618-2625.
62. Urban, J., A. Soulard, A. Huber, S. Lippman, D. Mukhopadhyay et al., 2007 Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol. Cell 26: 663-674.
63. Wach, A., A. Brachat, R. Pohlmann, and P. Philippsen, 1994 New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793-1808.
64. Wang, Y., Y. Kurihara, T. Sato, H. Toh, H. Kobayashi et al., 2009 Gtr1p differentially associates with Gtr2p and Ego1p. Gene 437: 32-38.
65. Wedaman, K. P., A. Reinke, S. Anderson, J. Yates, III, J. M. McCaffery et al., 2003 Tor kinases are in distinct membrane-associated protein complexes in Saccharomyces cerevisiae. Mol. Biol. Cell 14: 1204-1220.
66. Wiemken, A., and M. Durr, 1974 Characterization of amino acid pools in the vacuolar compartment of Saccharomyces cerevisiae. Arch. Microbiol. 101: 45-57.
67. Wullschleger, S., R. Loewith, W. Oppliger, and M. N. Hall, 2005 Molecular organization of target of rapamycin complex 2. J. Biol. Chem. 280: 30697-30704.
68. Wullschleger, S., R. Loewith, and M. N. Hall, 2006 TOR signaling in growth and metabolism. Cell 124: 471-484.
69. +-ATPase. Science 334: 678-683.
70. Zurita-Martinez, S. A., R. Puria, X. Pan, J. D. Boeke, and M. E. Cardenas, 2007 Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae. Genetics 176: 2139-2150.