Vesicular trafficking systems impact TORC1-controlled transcriptional programs in Saccharomyces cerevisiae

G3: Genes, Genomes, Genetics

Volumn 6, Issue 3, 2016, Pages 641-652

  Kingsbury, Joanne M ^a   Cardenas, Maria E ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Golgi to endosome trafficking; Phosphate responsive network; Rapamycin mechanism of action; Ribosome biogenesis genes; Sulfur containing amino acid metabolism genes

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; METHIONINE; NITROGEN; PHOSPHATE; PROLINE; RAPAMYCIN; RIBOSOME PROTEIN; SULFUR; SULFUR AMINO ACID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SFP1; UNCLASSIFIED DRUG; AMINO ACID; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; SACCHAROMYCES CEREVISIAE PROTEIN; TARGET OF RAPAMYCIN KINASE;

AMINO ACID METABOLISM; ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENDOSOME; EUKARYOTE; GENE EXPRESSION; GOLGI COMPLEX; MICROARRAY ANALYSIS; NONHUMAN; RIBOSOME; SACCHAROMYCES CEREVISIAE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; PROTEIN TRANSPORT; TRANSPORT AT THE CELLULAR LEVEL; TRANSPORT VESICLE;

AMINO ACIDS; BIOLOGICAL TRANSPORT; ENDOSOMES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GOLGI APPARATUS; MULTIPROTEIN COMPLEXES; MUTATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION, GENETIC; TRANSPORT VESICLES;

EID: 84959472209     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.023911     Document Type: Article

References (87)

1. Amerik, A. Y., J. Nowak, S. Swaminathan, and M. Hochstrasser, 2000 The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol. Biol. Cell 11: 3365-3380.
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. Beck, T., and M. N. Hall, 1999 The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689-692.
5. Benito-Moreno, R.M.,M.Miaczynska, B. E. Bauer, R. J. Schweyen, and A. Ragnini, 1994 Mrs6p, the yeast homologue of the mammalian choroideraemia protein: immunological evidence for its function as the Ypt1p Rab escort protein. Curr. Genet. 27: 23-25.
6. Blaiseau, P. L., A. D. Isnard, Y. Surdin-Kerjan, and D. Thomas, 1997 Met31p and Met32p, two related zinc finger proteins, are involved in transcriptional regulation of yeast sulfur amino acid metabolism. Mol. Cell. Biol. 17: 3640-3648.
7. Boer, V. M., J. H. de Winde, J. T. Pronk, and M. D. Piper, 2003 The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur. J. Biol. Chem. 278: 3265-3274.
8. 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 PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
9. Buerger, C., B. DeVries, and V. Stambolic, 2006 Localization of Rheb to the endomembrane is critical for its signaling function. Biochem. Biophys. Res. Commun. 344: 869-880.
10. 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.
11. 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.
12. Causton, H. C., B. Ren, S. S. Koh, C. T. Harbison, E. Kanin et al., 2001 Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12: 323-337.
13. Chandrasekaran, S., and D. Skowyra, 2008 The emerging regulatory potential of SCFMet30 -mediated polyubiquitination and proteolysis of the Met4 transcriptional activator. Cell Div. 3: 11.
14. Cox, K. H., A. Kulkarni, J. J. Tate, and T. G. Cooper, 2004 Gln3 phosphorylation and intracellular localization in nutrient limitation and starvation differ from those generated by rapamycin inhibition of Tor1/2 in Saccharomyces cerevisiae. J. Biol. Chem. 279: 10270-10278.
15. Crespo, J. L., T. Powers, B. Fowler, and M. N. Hall, 2002 The TORcontrolled transcription activators GLN3, RTG1, and RTG3 are regulated in response to intracellular levels of glutamine. Proc. Natl. Acad. Sci. USA 99: 6784-6789.
16. 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.
17. Di Como, C. J., and Y. Jiang, 2006 The association of Tap42 phosphatase complexes with TORC1: another level of regulation in Tor signaling. Cell Cycle 5: 2729-2732.
18. Dilova, I., C. Y. Chen, and T. Powers, 2002 Mks1 in concert with TOR signaling negatively regulates RTG target gene expression in S. cerevisiae. Curr. Biol. 12: 389-395.
19. 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.
20. Fasolo, J., A. Sboner, M. G. Sun, H. Yu, R. Chen et al., 2011 Diverse protein kinase interactions identified by protein microarrays reveal novel connections between cellular processes. Genes Dev. 25: 767-778.
21. Fayyadkazan, M., J. J. Tate, F. Vierendeels, T. G. Cooper, E. Dubois et al., 2014 Components of Golgi-to-vacuole trafficking are required for nitrogen- and TORC1-responsive regulation of the yeast GATA factors. MicrobiologyOpen 3: 271-287.
22. 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.
23. 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.
24. 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.
25. Gasch, A. P., P. T. Spellman, C. M. Kao, O. Carmel-Harel, M. B. Eisen et al., 2000 Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11: 4241-4257.
26. 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.
27. 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.
28. Grigull, J., S. Mnaimneh, J. Pootoolal, M. D. Robinson, and T. R. Hughes, 2004 Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 24: 5534-5547.
29. Hardwick, J. S., F. G. Kuruvilla, J. K. Tong, A. F. Shamji, and S. L. Schreiber, 1999 Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the Tor proteins. Proc. Natl. Acad. Sci. USA 96: 14866-14870.
30. Huber, A., B. Bodenmiller, A. Uotila, M. Stahl, S. Wanka et al., 2009 Characterization of the rapamycin-sensitive phosphoproteome reveals that Sch9 is a central coordinator of protein synthesis. Genes Dev. 23: 1929-1943.
31. Huber, A., S. L. French, H. Tekotte, S. Yerlikaya, M. Stahl et al., 2011 Sch9 regulates ribosome biogenesis via Stb3, Dot6 and Tod6 and the histone deacetylase complex RPD3L. EMBO J. 30: 3052-3064.
32. Hughes Hallett, J. E., X. Luo, and A. P. Capaldi, 2014 State transitions in the TORC1 signaling pathway and information processing in Saccharomyces cerevisiae. Genetics 198: 773-786.
33. 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.
34. Jiang, Y., and S. Ferro-Novick, 1994 Identification of yeast component A: reconstitution of the geranylgeranyltransferase that modifies Ypt1p and Sec4p. Proc. Natl. Acad. Sci. USA 91: 4377-4381.
35. 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.
36. Kamada, Y., K. Yoshino, C. Kondo, T. Kawamata, N. Oshiro et al., 2010 Tor directly controls the Atg1 kinase complex to regulate autophagy. Mol. Cell. Biol. 30: 1049-1058.
37. Kingsbury, J. M., N. D. Sen, T. Maeda, J. Heitman, and M. E. Cardenas, 2014 Endolysosomal membrane trafficking complexes drive nutrient-dependent TORC1 signaling to control cell growth in Saccharomyces cerevisiae. Genetics 196: 1077-1089.
38. Kitamoto, K., K. Yoshizawa, Y. Ohsumi, and Y. Anraku, 1988 Mutants of Saccharomyces cerevisiae with defective vacuolar function. J. Bacteriol. 170: 2687-2691.
39. Kuras, L., H. Cherest, Y. Surdin-Kerjan, and D. Thomas, 1996 A heteromeric complex containing the centromere binding factor 1 and two basic leucine zipper factors, Met4 and Met28, mediates the transcription activation of yeast sulfur metabolism. EMBO J. 15: 2519-2529.
40. Kuras, L., R. Barbey, and D. Thomas, 1997 Assembly of a bZIP-bHLH transcription activation complex: formation of the yeast Cbf1-Met4-Met28 complex is regulated through Met28 stimulation of Cbf1 DNA binding. EMBO J. 16: 2441-2451.
41. Lee, T. A., P. Jorgensen, A. L. Bognar, C. Peyraud, D. Thomas et al., 2010 Dissection of combinatorial control by the Met4 transcriptional complex. Mol. Biol. Cell 21: 456-469.
42. Lempiainen, H., A. Uotila, J. Urban, I. Dohnal, G. Ammerer et al., 2009 Sfp1 interaction with TORC1 and Mrs6 reveals feedback regulation on TOR signaling. Mol. Cell 33: 704-716.
43. Liko, D., M. G. Slattery, and W. Heideman, 2007 Stb3 binds to ribosomal RNA processing element motifs that control transcriptional responses to growth in Saccharomyces cerevisiae. J. Biol. Chem. 282:26623-26628.
44. Lippman, S. I., and J. R. Broach, 2009 Protein kinase A and TORC1 activate genes for ribosomal biogenesis by inactivating repressors encoded by Dot6 and its homolog Tod6. Proc. Natl. Acad. Sci. USA 106: 19928-19933.
45. Loewith, R., and M. N. Hall, 2011 Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189: 1177-1201.
46. Marion, R. M., A. Regev, E. Segal, Y. Barash, D. Koller et al., 2004 Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression. Proc. Natl. Acad. Sci. USA 101: 14315-14322.
47. Martin, D. E., A. Soulard, and M. N. Hall, 2004 TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119: 969-979.
48. O'Neill, E. M., A. Kaffman, E. R. Jolly, and E. K. O'Shea, 1996 Regulation of PHO4 nuclear localization by the PHO80-PHO85 cyclin-CDK complex. Science 271: 209-212.
49. Ogawa, N., J. DeRisi, and P. O. Brown, 2000 New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Mol. Biol. Cell 11: 4309-4321.
50. Ouni, I., K. Flick, and P. Kaiser, 2011 Ubiquitin and transcription: The SCF/Met4 pathway, a (protein-) complex issue. Transcription 2: 135-139.
51. Ozcan, S., and M. Johnston, 1999 Function and regulation of yeast hexose transporters. Microbiol. Mol. Biol. Rev. 63: 554-569.
52. Panchaud, N., M. P. Peli-Gulli, and C. De Virgilio, 2013 Amino acid deprivation inhibits TORC1 through a GTPase-activating protein complex for the Rag family GTPase Gtr1. Sci. Signal. 6: ra42.
53. 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.
54. 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.
55. Ptacek, J., G. Devgan, G. Michaud, H. Zhu, X. Zhu et al., 2005 Global analysis of protein phosphorylation in yeast. Nature 438: 679-684.
56. Puria, R., and M. E. Cardenas, 2008 Rapamycin bypasses vesicle-mediated signaling events to activate Gln3 in Saccharomyces cerevisiae. Commun. Integr. Biol. 1: 23-25.
57. Puria, R., S. A. Zurita-Martinez, and M. E. Cardenas, 2008 Nuclear translocation of Gln3 in response to nutrient signals requires Golgi-toendosome trafficking in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 105: 7194-7199.
58. 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.
59. Rudra, D., Y. Zhao, and J. R. Warner, 2005 Central role of Ifh1p-Fhl1p interaction in the synthesis of yeast ribosomal proteins. EMBO J. 24: 533-542.
60. Saito, K., R. Ohtomo, Y. Kuga-Uetake, T. Aono, and M. Saito, 2005 Direct labeling of polyphosphate at the ultrastructural level in Saccharomyces cerevisiae by using the affinity of the polyphosphate binding domain of Escherichia coli exopolyphosphatase. Appl. Environ. Microbiol. 71: 5692-5701.
61. 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.
62. Sancak, Y, L. Bar-Peled, R. Zoncu, A. L. Markhard, S. Nada, and D. M. Sabatini, 2010 Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141:290-303.
63. Santhanam, A., A. Hartley, K. Duvel, J. R. Broach, and S. Garrett, 2004 PP2A phosphatase activity is required for stress and Tor kinase regulation of yeast stress response factor Msn2p. Eukaryot. Cell 3: 1261-1271.
64. Schawalder, S. B., M. Kabani, I. Howald, U. Choudhury, M. Werner et al., 2004 Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1. Nature 432: 1058-1061.
65. Secco, D., C. Wang, H. Shou, and J. Whelan, 2012 Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain-containing proteins. FEBS Lett. 586: 289-295.
66. Sherman, F., G. R. Fink, and C. W. Lawrence, 1974 Methods in Yeast Genetics, Cold Spring Harbor Laboratory, Cold Spring Harbor.
67. Shin, C. S., S. Y. Kim, and W. K. Huh, 2009 TORC1 controls degradation of the transcription factor Stp1, a key effector of the SPS amino-acid-sensing pathway in Saccharomyces cerevisiae. J. Cell Sci. 122: 2089-2099.
68. Singh, J., and M. Tyers, 2009 A Rab escort protein integrates the secretion system with TOR signaling and ribosome biogenesis. Genes Dev. 23:1944-1958.
69. Springer, M., D. D. Wykoff, N. Miller, and E. K. O'Shea, 2003 Partially phosphorylated Pho4 activates transcription of a subset of phosphateresponsive genes. PLoS Biol. 1: E28.
70. 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.
71. 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.
72. Takahara, T., and T. Maeda, 2012 Transient sequestration of TORC1 into stress granules during heat stress. Mol. Cell 47: 242-252.
73. Tate, J. J., A. Feller, E. Dubois, and T. G. Cooper, 2006 Saccharomyces cerevisiae Sit4 phosphatase is active irrespective of the nitrogen source provided, and Gln3 phosphorylation levels become nitrogen source-responsive in a sit4-deleted strain. J. Biol. Chem. 281: 37980-37992.
74. Thedieck, K., B. Holzwarth, M. T. Prentzell, C. Boehlke, K. Klasener et al., 2013 Inhibition of mTORC1 by astrin and stress granules prevents apoptosis in cancer cells. Cell 154: 859-874.
75. Thomas, M. R., and E. K. O'Shea, 2005 An intracellular phosphate buffer filters transient fluctuations in extracellular phosphate levels. Proc. Natl. Acad. Sci. USA 102: 9565-9570.
76. Upadhya, R., J. Lee, and I. M. Willis, 2002 Maf1 is an essential mediator of diverse signals that repress RNA polymerase III transcription. Mol. Cell 10: 1489-1494.
77. 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.
78. Urech, K., M. Durr, T. Boller, A. Wiemken, and J. Schwencke, 1978 Localization of polyphosphate in vacuoles of Saccharomyces cerevisiae. Arch. Microbiol. 116: 275-278.
79. Verwaal, R., J. W. Paalman, A. Hogenkamp, A. J. Verkleij, C. T. Verrips et al., 2002 HXT5 expression is determined by growth rates in Saccharomyces cerevisiae. Yeast 19: 1029-1038.
80. Wang, S., Z. Y. Tsun, R. L. Wolfson, K. Shen, G. A. Wyant et al., 2015 Metabolism. Lysosomal amino acid transporter SLC38A9 signals arginine sufficiency to mTORC1. Science 347: 188-194.
81. Warner, J. R., 1999 The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24: 437-440.
82. Wedaman, K. P., A. Reinke, S. Anderson, J. Yates, 3rd, J. M. McCaffery et al., 2003 Tor kinases are in distinct membrane-associated protein complexes in Saccharomyces cerevisiae. Mol. Biol. Cell 14: 1204-1220.
83. Wippich, F., B. Bodenmiller, M. G. Trajkovska, S. Wanka, R. Aebersold et al., 2013 Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell 152: 791-805.
84. Yan, G., X. Shen, and Y. Jiang, 2006 Rapamycin activates Tap42-associated phosphatases by abrogating their association with Tor complex 1. EMBO J. 25: 3546-3555.
85. Yan, G., Y. Lai, and Y. Jiang, 2012 The TOR complex 1 is a direct target of Rho1 GTPase. Mol. Cell 45: 743-753.
86. Zoncu, R., L. Bar-Peled, A. Efeyan, S. Wang, Y. Sancak et al., 2011 mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H-ATPase. Science 334: 678-683.
87. 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.