Budding yeast SSD1-V regulates transcript levels of many longevity genes and extends chronological life span in purified quiescent cells

Molecular Biology of the Cell

Volumn 20, Issue 17, 2009, Pages 3851-3864

  Li, Lihong ^a   Lu, Yong ^b,e   Qin, Li Xuan ^c   Bar Joseph, Ziv ^b   Werner Washburne, Margaret ^d   Breeden, Linda L ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b Carnegie Mellon University   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF NEW MEXICO   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SSD1; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE REGULATION; CELL SURVIVAL; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; YEAST CELL;

CELL CYCLE; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; LONGEVITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMORPHISM, GENETIC; PROTEIN ISOFORMS; RIBOSOMAL PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 70349318536     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-04-0347     Document Type: Article

References (104)

1. Allen, C., et al. (2006). Isolation of quiescent and nonquiescent cells from yeast stationary-phase cultures. J. Cell Biol. 174, 89-100. (Pubitemid 43992899)
2. Alvers, A. L., Fishwick, L. K., Wood, M. S., Hu, D., Chung, H. S., Dunn, W. A., Jr., and Aris, J. P. (2009). Autophagy and amino acid homeostasis are required for chronological longevity in Saccharomyces cerevisiae. Aging Cell 8, 353-369.
3. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. (2003). Current Protocols in Molecular Biology, New York: Wiley Interscience, 13.13.13.
4. Bar-Joseph, Z., Gerber, G., Simon, I., Gifford, D. K., and Jaakkola, T. S. (2003). Comparing the continuous representation of time-series expression profiles to identify differentially expressed genes. Proc. Natl. Acad. Sci. USA 100, 10146-10151.
5. Boeke, J., Lacroute, F., and Fink, G. (1984). A positive selection for mutants lacking orotidine-5′ phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197, 345-346.
6. Boer, V. M., Amini, S., and Botstein, D. (2008). Influence of genotype and nutrition on survival and metabolism of starving yeast. Proc. Natl. Acad. Sci. USA 105, 6930-6935.
7. Brauer, M. J., Yuan, J., Bennett, B. D., Lu, W., Kimball, E., Botstein, D., and Rabinowitz, J. D. (2006). Conservation of the metabolomic response to starvation across two divergent microbes. Proc. Natl. Acad. Sci. USA 103, 19302-19307.
8. Breeden, L. L. (1997). Alpha factor synchronization of budding yeast. Methods Enzymol. 283, 332-341.
9. Briand, J. F., Navarro, F., Rematier, P., Boschiero, C., Labarre, S., Werner, M., Shpakovski, G. V., and Thuriaux, P. (2001). Partners of Rpb8p, a small subunit shared by yeast RNA polymerases I, II and III. Mol. Cell. Biol. 21, 6056-6065.
10. Burtner, C. R., Murakami, C. J., Kennedy, B. K., and Kaeberlein, M. (2009). A molecular mechanism of chronological aging in yeast. Cell Cycle 8, 1256-1270.
11. Cheong, H., and Klionsky, D. J. (2008). Dual role of Atg1 in regulation of autophagy-specific PAS assembly in Saccharomyces cerevisiae. Autophagy 4, 724-726.
12. Cheong, H., Nair, U., Geng, J., and Klionsky, D. J. (2008). The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae. Mol. Biol. Cell 19, 668-681.
13. Chiocchetti, A., et al. (2007). Ribosomal proteins Rpl10 and Rps6 are potent regulators of yeast replicative life span. Exp. Gerontol. 42, 275-286.
14. Collins, S. R., et al. (2007). Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446, 806-810.
15. Cvrckova, F., and Nasmyth, K. (1993). Yeast G1 cyclins CLN1 and CLN2 and a GAP-like protein have a role in bud formation. EMBO J. 12, 5277-5286.
16. de Lichtenberg, U., Jensen, L. J., Fausboll, A., Jensen, T. S., Bork, P. and Brunak, S. (2005). Comparison of computational methods for the identification of cell cycle-regulated genes. Bioinformatics 21, 1164-1171. (Pubitemid 40467941)
17. Dequard-Chablat, M., Riva, M., Carles, C., and Sentenac, A. (1991). RPC19, the gene for a subunit common to yeast RNA polymerases A (I) and C (III). J. Biol. Chem. 266, 15300-15307. (Pubitemid 21907648)
18. Diaz-Troya, S., Perez-Perez, M. E., Florencio, F. J., and Crespo, J. L. (2008). The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 4, 851-865.
19. Du, L. L., and Novick, P. (2002). Pag1p, a novel protein associated with protein kinase Cbk1p, is required for cell morphogenesis and proliferation in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 503-514.
20. Fabrizio, P., Liou, L. L., Moy, V. N., Diaspro, A., Valentine, J. S., Gralla, E. B., and Longo, V. D. (2003). SOD2 functions downstream of Sch9 to extend longevity in yeast. Genetics 163, 35-46. (Pubitemid 36222651)
21. Fabrizio, P., and Longo, V. D. (2003). The chronological life span of Saccharomyces cerevisiae. Aging Cell 2, 73-81.
22. Fabrizio, P., Pletcher, S. D., Minois, N., Vaupel, J. W., and Longo, V. D. (2004). Chronological aging-independent replicative life span regulation by Msn2/Msn4 and Sod2 in Saccharomyces cerevisiae. FEBS Lett. 557, 136-142.
23. Fabrizio, P., Pozza, F., Pletcher, S. D., Gendron, C. M., and Longo, V. D. (2001). Regulation of longevity and stress resistance by Sch9 in yeast. Science 292, 288-290. (Pubitemid 32295387)
24. Gank, K. D., Yeaman, M. R., Kojima, S., Yount, N. Y., Park, H., Edwards, J. E., Jr., Filler, S. G., and Fu, Y. (2008). SSD1 is integral to host defense peptide resistance in Candida albicans. Eukaryot. Cell 7, 1318-1327.
25. Garneau, N. L., Wilusz, J., and Wilusz, C. J. (2007). The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8, 113-126.
26. Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D., and Brown, P. O. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11, 4241-4257.
27. Goldstrohm, A. C., Hook, B. A., Seay, D. J., and Wickens, M. (2006). PUF proteins bind Pop2p to regulate messenger RNAs. Nat. Struct. Mol. Biol. 13, 533-539.
28. Goldstrohm, A. C., Seay, D. J., Hook, B. A., and Wickens, M. (2007). PUF protein-mediated deadenylation is catalyzed by Ccr4p. J. Biol. Chem. 282, 109-114.
29. Gomes, P., Sampaio-Marques, B., Ludovico, P., Rodrigues, F., and Leao, C. (2007). Low auxotrophy-complementing amino acid concentrations reduce yeast chronological life span. Mech. Ageing Dev. 128, 383-391.
30. Harbison, C. T., et al. (2004). Transcriptional regulatory code of a eukaryotic genome. Nature 431, 99-104.
31. Hellauer, K., Akache, B., MacPherson, S., Sirard, E., and Turcotte, B. (2002). Zinc cluster protein Rdr1p is a transcriptional repressor of the PDR5 gene encoding a multidrug transporter. J. Biol. Chem. 277, 17671-17676.
32. Henry, S. A. (1973). Death resulting from fatty acid starvation in yeast. J. Bacteriol. 116, 1293-1303.
33. Herker, E., Jungwirth, H., Lehmann, K. A., Maldener, C., Frohlich, K. U., Wissing, S., Buttner, S., Fehr, M., Sigrist, S., and Madeo, F. (2004). Chronological aging leads to apoptosis in yeast. J. Cell Biol. 164, 501-507. (Pubitemid 38233311)
34. Hogan, D. J., Riordan, D. P., Gerber, A. P., Herschlag, D., and Brown, P. O. (2008). Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol. 6, e255.
35. Holstege, F. C., Jennings, E. G., Wyrick, J. J., Lee, T. I., Hengartner, C. J., Green, M. R., Golub, T. R., Lander, E. S., and Young, R. A. (1998). Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95, 717-728.
36. Hong, E. L., et al. (2008). Gene Ontology annotations at SGD: new data sources and annotation methods. Nucleic Acids Res. 36, D577-D581.
37. Hughes, J. D., Estep, P. W., Tavazoie, S., and Church, G. M. (2000). Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. J. Mol. Biol. 296, 1205-1214.
38. Ibeas, J. I., Yun, D. J., Damsz, B., Narasimhan, M. L., Uesono, Y., Ribas, J. C., Lee, H., Hasegawa, P. M., Bressan, R. A., and Pardo, J. M. (2001). Resistance to the plant PR-5 protein osmotin in the model fungus Saccharomyces cerevisiae is mediated by the regulatory effects of SSD1 on cell wall composition. Plant J. 25, 271-280.
39. Jiang, J. C., Kirchman, P. A., Allen, M., and Jazwinski, S. M. (2004). Suppressor analysis points to the subtle role of the LAG1 ceramide synthase gene in determining yeast longevity. Exp. Gerontol. 39, 999-1009.
40. Jiang, J. C., Wawryn, J., Shantha Kumara, H. M., and Jazwinski, S. M. (2002). Distinct roles of processes modulated by histone deacetylases Rpd3p, Hda1p, and Sir2p in life extension by caloric restriction in yeast. Exp. Gerontol. 37, 1023-1030.
41. Jorgensen, P., Nelson, B., Robinson, M. D., Chen, Y., Andrews, B., Tyers, M., and Boone, C. (2002). High-resolution genetic mapping with ordered arrays of Saccharomyces cerevisiae deletion mutants. Genetics 162, 1091-1099.
42. Kaeberlein, M., Andalis, A. A., Fink, G. R., and Guarente, L. (2002). High osmolarity extends life span in Saccharomyces cerevisiae by a mechanism related to calorie restriction. Mol. Cell. Biol. 22, 8056-8066.
43. Kaeberlein, M., Andalis, A. A., Liszt, G. B., Fink, G. R., and Guarente, L. (2004). Saccharomyces cerevisiae SSD1-V confers longevity by a Sir2p-independent mechanism. Genetics 166, 1661-1672. (Pubitemid 38621050)
44. Kaeberlein, M., and Guarente, L. (2002). Saccharomyces cerevisiae MPT5 and SSD1 function in parallel pathways to promote cell wall integrity. Genetics 160, 83-95.
45. Kaeberlein, M., Kirkland, K. T., Fields, S., and Kennedy, B. K. (2005a). Genes determining yeast replicative life span in a long-lived genetic background. Mech. Ageing Dev. 126, 491-504.
46. Kaeberlein, M., McVey, M., and Guarente, L. (1999). The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 13, 2570-2580.
47. Kaeberlein, M., Powers, R. W., 3rd, Steffen, K. K., Westman, E. A., Hu, D., Dang, N., Kerr, E. O., Kirkland, K. T., Fields, S., and Kennedy, B. K. (2005b). Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310, 1193-1196.
48. Kennedy, B. K., Austriaco, N. R., Jr., Zhang, J., and Guarente, L. (1995). Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae. Cell 80, 485-496.
49. Kikuchi, Y., Oka, Y., Kobayashi, M., Uesono, Y., Toh-e, A., and Kikuchi, A. (1994). A new yeast gene, HTR1, required for growth at high temperature, is needed for recovery from mating pheromone-induced G1 arrest. Mol. Gen. Genet. 245, 107-116.
50. Kosodo, Y., Imai, K., Hirata, A., Noda, Y., Takatsuki, A., Adachi, H., and Yoda, K. (2001). Multicopy suppressors of the sly1 temperature-sensitive mutation in the ER-Golgi vesicular transport in Saccharomyces cerevisiae. Yeast 18, 1003-1014.
51. Li, B., and Warner, J. R. (1996). Mutation of the Rab6 homologue of Saccharomyces cerevisiae, YPT6, inhibits both early Golgi function and ribosome biosynthesis. J. Biol. Chem. 271, 16813-16819.
52. Li, L., Bagley, D., Ward, D. M., and Kaplan, J. (2008). Yap5 is an iron-responsive transcriptional activator that regulates vacuolar iron storage in yeast. Mol. Cell. Biol. 28, 1326-1337.
53. Lin, S. J., Kaeberlein, M., Andalis, A. A., Sturtz, L. A., Defossez, P. A., Culotta, V. C., Fink, G. R., and Guarente, L. (2002). Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 418, 344-348.
54. Longo, V. D. (2003). The Ras and Sch9 pathways regulate stress resistance and longevity. Exp. Gerontol. 38, 807-811.
55. Longtine, M. S., McKenzie, A., III, 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.
56. Lu, Y., Mahony, S., Panayiotis, V. B., Rosenfeld, R., Simon, I., Breeden, L. L., and Bar-Joseph, Z. (2007). Combined analysis reveals a core set of cycling transcripts. Genome Biol. 8, R146-R157. (Pubitemid 351903191)
57. Luukkonen, B. G., and Seraphin, B. (1999). A conditional U5 snRNA mutation affecting pre-mRNA splicing and nuclear pre-mRNA retention identifies SSD1/SRK1 as a general splicing mutant suppressor. Nucleic Acids Res. 27, 3455-3465.
58. Maddock, J. R., Weidenhammer, E. M., Adams, C. C., Lunz, R. L., and Woolford, J. L., Jr. (1994). Extragenic suppressors of Saccharomyces cerevisiae prp4 mutations identify a negative regulator of PRP genes. Genetics 136, 833-847.
59. Martin, D. E., Soulard, A., and Hall, M. N. (2004). TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119, 969-979. (Pubitemid 40037610)
60. Mazanka, E., Alexander, J., Yeh, B. J., Charoenpong, P., Lowery, D. M., Yaffe, M., and Weiss, E. L. (2008). The NDR/LATS family kinase Cbk1 directly controls transcriptional asymmetry. PLoS Biol. 6, e203.
61. Mazzoni, C., Mancini, P., Verdone, L., Madeo, F., Serafini, A., Herker, E., and Falcone, C. (2003). A truncated form of KlLsm4p and the absence of factors involved in mRNA decapping trigger apoptosis in yeast. Mol. Biol. Cell 14, 721-729.
62. McInerny, C. J., Partridge, J. F., Mikesell, G. E., Creemer, D. P., and Breeden, L. L. (1997). A novel Mcm1-dependent element in the SWI4, CLN3, CDC6, and CDC47 promoters activates M/G1-specific transcription. Genes Dev. 11, 1277-1288.
63. Mir, S. S., Fiedler, D., and Cashikar, A. G. (2009). Ssd1 is required for thermotolerance and Hsp104-mediated protein disaggregation in Saccharomyces cerevisiae. Mol. Cell. Biol. 29, 187-200.
64. Moehle, C. M., and Hinnebusch, A. G. (1991). Association of RAP1 binding sites with stringent control of ribosomal protein gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 11, 2723-2735.
65. Moriya, H., and Isono, K. (1999). Analysis of genetic interactions between DHH1, SSD1 and ELM1 indicates their involvement in cellular morphology determination in Saccharomyces cerevisiae. Yeast 15, 481-496.
66. Mortimer, R. K., and Johnston, J. R. (1959). Life span of individual yeast cells. Nature 183, 1751-1752.
67. Ohkuni, K., Okuda, A., and Kikuchi, A. (2003). Yeast Nap1-binding protein Nbp2p is required for mitotic growth at high temperatures and for cell wall integrity. Genetics 165, 517-529. (Pubitemid 37337621)
68. Onda, M., Ota, K., Chiba, T., Sakaki, Y., and Ito, T. (2004). Analysis of gene network regulating yeast multidrug resistance by artificial activation of transcription factors: involvement of Pdr3 in salt tolerance. Gene 332, 51-59. (Pubitemid 38624250)
69. Parsons, A. B., Brost, R. L., Ding, H., Li, Z., Zhang, C., Sheikh, B., Brown, G. W., Kane, P. M., Hughes, T. R., and Boone, C. (2004). Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat. Biotechnol. 22, 62-69.
70. Phatnani, H. P., and Greenleaf, A. L. (2006). Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20, 2922-2936.
71. Powers, R. W., 3rd, Kaeberlein, M., Caldwell, S. D., Kennedy, B. K., and Fields, S. (2006). Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 20, 174-184.
72. Pramila, T., Miles, S., GuhaThakurta, D., Jemilo, D., and Breeden, L. L. (2002). Conserved homeodomain proteins interact with MADS box protein Mcm1 to restrict ECB-dependent transcription to the M/G1 phase of the cell cycle. Genes Dev. 16, 3034-3045. (Pubitemid 35424191)
73. Pramila, T., Wu, W., Miles, S., Noble, W. S., and Breeden, L. L. (2006). The Forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle. Genes Dev. 20, 2266-2278. (Pubitemid 44244527)
74. Ptacek, J., et al. (2005). Global analysis of protein phosphorylation in yeast. Nature 438, 679-684. (Pubitemid 41740579)
75. Qin, H., and Lu, M. (2006). Natural variation in replicative and chronological life spans of Saccharomyces cerevisiae. Exp. Gerontol. 41, 448-456.
76. Qin, L. X., and Self, S. G. (2006). The clustering of regression models method with applications to gene expression data. Biometrics 62, 526-533. (Pubitemid 43926658)
77. Racki, W. J., Becam, A. M., Nasr, F., and Herbert, C. J. (2000). Cbk1p, a protein similar to the human myotonic dystrophy kinase, is essential for normal morphogenesis in Saccharomyces cerevisiae. EMBO J. 19, 4524-4532.
78. Raisner, R. M., and Madhani, H. D. (2008). Genomewide screen for negative regulators of sirtuin activity in Saccharomyces cerevisiae reveals 40 loci and links to metabolism. Genetics 179, 1933-1944.
79. Reguly, T., et al. (2006). Comprehensive curation and analysis of global interaction networks in Saccharomyces cerevisiae. J. Biol. 5, 1-28.
80. 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.
81. Rudra, D., Zhao, Y., and Warner, J. R. (2005). Central role of Ifh1p-Fhl1p interaction in the synthesis of yeast ribosomal proteins. EMBO J. 24, 533-542. (Pubitemid 40343255)
82. Rundlett, S. E., Carmen, A. A., Kobayashi, R., Bavykin, S., Turner, B. M., and Grunstein, M. (1996). HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc. Natl. Acad. Sci. USA 93, 14503-14508.
83. Saldanha, A. J., Brauer, M. J., and Botstein, D. (2004). Nutritional homeostasis in batch and steady-state culture of yeast. Mol. Biol. Cell 15, 4089-4104.
84. Scherer, S., and Davis, R. W. (1979). Replacement of chromosome segments with altered DNA sequences constructed in vitro. Proc. Natl. Acad. Sci. USA 76, 4951-4955.
85. Sikorski, R. S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
86. Spingola, M., Grate, L., Haussler, D., and Ares, M., Jr. (1999). Genome-wide bioinformatic and molecular analysis of introns in Saccharomyces cerevisiae. RNA 5, 221-234.
87. Stettler, S., Chiannilkulchai, N., Hermann-Le Denmat, S., Lalo, D., Lacroute, F., Sentenac, A., and Thuriaux, P. (1993). A general suppressor of RNA polymerase I, II and III mutations in Saccharomyces cerevisiae. Mol. Gen. Genet. 239, 169-176.
88. Sutton, A., Immanuel, D., and Arndt, K. T. (1991). The SIT4 protein phosphatase functions in late G1 for progression into S phase. Mol. Cell. Biol. 11, 2133-2148.
89. Tanaka, S., et al. (2007). Saccharomyces cerevisiae SSD1 orthologues are essential for host infection by the ascomycete plant pathogens Colletotrichum lagenarium and Magnaporthe grisea. Mol. Microbiol. 64, 1332-1349. (Pubitemid 46849021)
90. Tarassov, K., Messier, V., Landry, C. R., Radinovic, S., Molina, M. M., Shames, I., Malitskaya, Y., Vogel, J., Bussey, H., and Michnick, S. W. (2008). An in vivo map of the yeast protein interactome. Science 320, 1465-1470. (Pubitemid 351929421)
91. Tong, A. H., et al. (2001). Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368.
92. Tong, A. H., et al. (2004). Global mapping of the yeast genetic interaction network. Science 303, 808-813. (Pubitemid 38174652)
93. Uesono, Y., Fujita, A., Toh-e, A., and Kikuchi, Y. (1994). The MCS1/SSD1/SRK1/SSL1 gene is involved in stable maintenance of the chromosome in yeast. Gene 143, 135-138. (Pubitemid 24182079)
94. Uesono, Y., Toh-e, A., and Kikuchi, Y. (1997). Ssd1p of Saccharomyces cerevisiae associates with RNA. J. Biol. Chem. 272, 16103-16109.
95. Vannier, D., Damay, P., and Shore, D. (2001). A role for Sds3p, a component of the Rpd3p/Sin3p deacetylase complex, in maintaining cellular integrity in Saccharomyces cerevisiae. Mol. Genet. Genom. 265, 560-568. (Pubitemid 32397644)
96. Vellai, T. (2009). Autophagy genes and ageing. Cell Death Differ. 16, 94-102.
97. Warner, J. R. (1999). The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24, 437-440.
98. Wei, M., Fabrizio, P., Hu, J., Ge, H., Cheng, C., Li, L., and Longo, V. D. (2008). Life span extension by calorie restriction depends on Rim15 and transcription factors downstream of Ras/PKA, Tor, and Sch9. PLoS Genet. 4, e13. (Pubitemid 351230881)
99. Weinberger, M., Feng, L., Paul, A., Smith, D. L., Jr., Hontz, R. D., Smith, J. S., Vujcic, M., Singh, K. K., Huberman, J. A., and Burhans, W. C. (2007). DNA replication stress is a determinant of chronological lifespan in budding yeast. PLoS ONE 2, e748. (Pubitemid 351338868)
100. Wheeler, R. T., Kupiec, M., Magnelli, P., Abeijon, C., and Fink, G. R. (2003). A Saccharomyces cerevisiae mutant with increased virulence. Proc. Natl. Acad. Sci. USA 100, 2766-2770.
101. Wijnen, H., and Futcher, B. (1999). Genetic analysis of the shared role of CLN3 and BCK2 at the G1-S transition in Saccharomyces cerevisiae. Genetics 153, 1131-1143.
102. Yamaguchi-Iwai, Y., Dancis, A., and Klausner, R. D. (1995). AFT1, a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J. 14, 1231-1239.
103. Wilson, R. B., Brenner, A. A., White, T. B., Engler, M. J., Gaughran, J. P., and Tatchell, K. (1991). The Saccharomyces cerevisiae SRK1 gene, a suppressor of bcy1 and ins1, may be involved in protein phosphatase function. Mol. Cell. Biol. 11, 3369-3373.
104. Zanelli, C. F., and Valentini, S. R. (2005). Pkc1 acts through Zds1 and Gic1 to suppress growth and cell polarity defects of a yeast eIF5A mutant. Genetics 171, 1571-1581.