Gene-nutrient interaction markedly influences yeast chronological lifespan

Experimental Gerontology

Volumn 86, Issue , 2016, Pages 113-123

  Smith, Daniel L ^a,b   Maharrey, Crystal H ^c   Carey, Christopher R ^c   White, Richard A ^d   Hartman, John L ^a,b,c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Aging; Chronological lifespan (CLS); Gene nutrient interaction; Genome wide screen; Longevity; Quantitative high throughput cell array phenotyping; Saccharomyces cerevisiae; Yeast gene deletion strain library

Indexed keywords

ARTICLE; AUXOTROPHY; BIOLOGY; BUDDING YEAST; CELL AGING; CHRONOLOGICAL LIFESPAN; CHRONOLOGY; FUNGAL STRAIN; GENE DELETION; GENE IDENTIFICATION; GENE INTERACTION; GENE NUTRIENT INTERACTION; GENE ONTOLOGY; GENE REPLICATION; GENETIC SCREENING; GENETIC VARIABILITY; LIFESPAN; MODIFIER GENE; NONHUMAN; PLOIDY; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; STRAIN IDENTIFICATION; AGING; CULTURE MEDIUM; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE ENVIRONMENT INTERACTION; LONGEVITY; PHENOTYPE;

CULTURE MEDIUM;

AGING; CULTURE MEDIA; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENE-ENVIRONMENT INTERACTION; GENOME-WIDE ASSOCIATION STUDY; LONGEVITY; PHENOTYPE; SACCHAROMYCES CEREVISIAE;

EID: 84971634920     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2016.04.012     Document Type: Article

References (56)

1. Ben-Shitrit, T., Yosef, N., Shemesh, K., Sharan, R., Ruppin, E., Kupiec, M., Systematic identification of gene annotation errors in the widely used yeast mutation collections. Nat. Methods 9 (2012), 373–378.
2. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P., Boeke, J.D., 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 (1998), 115–132.
3. Burtner, C.R., Murakami, C.J., Kaeberlein, M., A genomic approach to yeast chronological aging. Methods Mol. Biol. 548 (2009), 101–114.
4. Burtner, C.R., Murakami, C.J., Kennedy, B.K., Kaeberlein, M., A molecular mechanism of chronological aging in yeast. Cell Cycle 8 (2009), 1256–1270.
5. Burtner, C.R., Murakami, C.J., Olsen, B., Kennedy, B.K., Kaeberlein, M., A genomic analysis of chronological longevity factors in budding yeast. Cell Cycle 10 (2011), 1385–1396.
6. Cherry, J.M., Hong, E.L., Amundsen, C., Balakrishnan, R., Binkley, G., Chan, E.T., Christie, K.R., Costanzo, M.C., Dwight, S.S., Engel, S.R., Fisk, D.G., Hirschman, J.E., Hitz, B.C., Karra, K., Krieger, C.J., Miyasato, S.R., Nash, R.S., Park, J., Skrzypek, M.S., Simison, M., Weng, S., Wong, E.D., Saccharomyces genome database: the genomics resource of budding yeast. Nucleic Acids Res. 40 (2012), D700–D705.
7. Costanzo, M., Baryshnikova, A., Bellay, J., Kim, Y., Spear, E.D., Sevier, C.S., Ding, H., Koh, J.L., Toufighi, K., Mostafavi, S., Prinz, J., St Onge, R.P., VanderSluis, B., Makhnevych, T., Vizeacoumar, F.J., Alizadeh, S., Bahr, S., Brost, R.L., Chen, Y., Cokol, M., Deshpande, R., Li, Z., Lin, Z.Y., Liang, W., Marback, M., Paw, J., San Luis, B.J., Shuteriqi, E., Tong, A.H., van Dyk, N., Wallace, I.M., Whitney, J.A., Weirauch, M.T., Zhong, G., Zhu, H., Houry, W.A., Brudno, M., Ragibizadeh, S., Papp, B., Pal, C., Roth, F.P., Giaever, G., Nislow, C., Troyanskaya, O.G., Bussey, H., Bader, G.D., Gingras, A.C., Morris, Q.D., Kim, P.M., Kaiser, C.A., Myers, C.L., Andrews, B.J., Boone, C., The genetic landscape of a cell. Science 327 (2010), 425–431.
8. Curran, S.P., Ruvkun, G., Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet., 3, 2007, e56.
9. Delaney, J.R., Murakami, C., Chou, A., Carr, D., Schleit, J., Sutphin, G.L., An, E.H., Castanza, A.S., Fletcher, M., Goswami, S., Higgins, S., Holmberg, M., Hui, J., Jelic, M., Jeong, K.S., Kim, J.R., Klum, S., Liao, E., Lin, M.S., Lo, W., Miller, H., Moller, R., Peng, Z.J., Pollard, T., Pradeep, P., Pruett, D., Rai, D., Ros, V., Schuster, A., Singh, M., Spector, B.L., Wende, H.V., Wang, A.M., Wasko, B.M., Olsen, B., Kaeberlein, M., Dietary restriction and mitochondrial function link replicative and chronological aging in Saccharomyces cerevisiae. Exp. Gerontol. 48 (2013), 1006–1013.
10. Fabrizio, P., Wei, M., Conserved role of medium acidification in chronological senescence of yeast and mammalian cells. Aging (Albany NY) 3 (2011), 1127–1129.
11. Fabrizio, P., Pozza, F., Pletcher, S.D., Gendron, C.M., Longo, V.D., Regulation of longevity and stress resistance by Sch9 in yeast. Science 292 (2001), 288–290.
12. Fabrizio, P., Battistella, L., Vardavas, R., Gattazzo, C., Liou, L.L., Diaspro, A., Dossen, J.W., Gralla, E.B., Longo, V.D., Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J. Cell Biol. 166 (2004), 1055–1067.
13. Fabrizio, P., Hoon, S., Shamalnasab, M., Galbani, A., Wei, M., Giaever, G., Nislow, C., Longo, V.D., Genome-wide screen in Saccharomyces cerevisiae identifies vacuolar protein sorting, autophagy, biosynthetic, and tRNA methylation genes involved in life span regulation. PLoS Genet., 6, 2010, e1001024.
14. Ghirardi, O., Cozzolino, R., Guaraldi, D., Giuliani, A., Within- and between-strain variability in longevity of inbred and outbred rats under the same environmental conditions. Exp. Gerontol. 30 (1995), 485–494.
15. Giaever, G., Nislow, C., The yeast deletion collection: a decade of functional genomics. Genetics 197 (2014), 451–465.
16. Giaever, G., Chu, A.M., Ni, L., Connelly, C., Riles, L., Veronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., Andre, B., Arkin, A.P., Astromoff, A., El-Bakkoury, M., Bangham, R., Benito, R., Brachat, S., Campanaro, S., Curtiss, M., Davis, K., Deutschbauer, A., Entian, K.D., Flaherty, P., Foury, F., Garfinkel, D.J., Gerstein, M., Gotte, D., Guldener, U., Hegemann, J.H., Hempel, S., Herman, Z., Jaramillo, D.F., Kelly, D.E., Kelly, S.L., Kotter, P., LaBonte, D., Lamb, D.C., Lan, N., Liang, H., Liao, H., Liu, L., Luo, C., Lussier, M., Mao, R., Menard, P., Ooi, S.L., Revuelta, J.L., Roberts, C.J., Rose, M., Ross-Macdonald, P., Scherens, B., Schimmack, G., Shafer, B., Shoemaker, D.D., Sookhai-Mahadeo, S., Storms, R.K., Strathern, J.N., Valle, G., Voet, M., Volckaert, G., Wang, C.Y., Ward, T.R., Wilhelmy, J., Winzeler, E.A., Yang, Y., Yen, G., Youngman, E., Yu, K., Bussey, H., Boeke, J.D., Snyder, M., Philippsen, P., Davis, R.W., Johnston, M., Functional profiling of the Saccharomyces cerevisiae genome. Nature 418 (2002), 387–391.
17. Hamilton, B., Dong, Y., Shindo, M., Liu, W., Odell, I., Ruvkun, G., Lee, S.S., A systematic RNAi screen for longevity genes in C. elegans. Genes Dev. 19 (2005), 1544–1555.
18. Hansen, M., Hsu, A.L., Dillin, A., Kenyon, C., New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet. 1 (2005), 119–128.
19. Harrison, D.E., Strong, R., Allison, D.B., Ames, B.N., Astle, C.M., Atamna, H., Fernandez, E., Flurkey, K., Javors, M.A., Nadon, N.L., Nelson, J.F., Pletcher, S., Simpkins, J.W., Smith, D., Wilkinson, J.E., Miller, R.A., Acarbose, 17-alpha-estradiol, and nordihydroguaiaretic acid extend mouse lifespan preferentially in males. Aging Cell 13 (2014), 273–282.
20. Hartman, J.L. IV, Buffering of deoxyribonucleotide pool homeostasis by threonine metabolism. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 11700–11705.
21. Hartman, J.L. IV, Tippery, N.P., Systematic quantification of gene interactions by phenotypic array analysis. Genome Biol., 5, 2004, R49.
22. Hartman, J.L. IV, Stisher, C., Outlaw, D.A., Guo, J., Shah, N.A., Tian, D., Santos, S.M., Rodgers, J.W., White, R.A., Yeast phenomics: an experimental approach for modeling gene interaction networks that buffer disease. Genes 6 (2015), 24–45.
23. Hughes, T.R., Roberts, C.J., Dai, H., Jones, A.R., Meyer, M.R., Slade, D., Burchard, J., Dow, S., Ward, T.R., Kidd, M.J., Friend, S.H., Marton, M.J., Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25 (2000), 333–337.
24. Irizarry, R.A., Ooi, S.L., Wu, Z., Boeke, J.D., Use of mixture models in a microarray-based screening procedure for detecting differentially represented yeast mutants. Stat. Appl. Genet. Mol. Biol., 2(Article1), 2003.
25. Jiang, J.C., Jaruga, E., Repnevskaya, M.V., Jazwinski, S.M., An intervention resembling caloric restriction prolongs life span and retards aging in yeast. FASEB J. 14 (2000), 2135–2137.
26. Johnson, J.E., Johnson, F.B., Methionine restriction activates the retrograde response and confers both stress tolerance and lifespan extension to yeast, mouse and human cells. PLoS ONE, 9, 2014, e97729.
27. Kaeberlein, M., Powers, R.W. 3rd, Steffen, K.K., Westman, E.A., Hu, D., Dang, N., Kerr, E.O., Kirkland, K.T., Fields, S., Kennedy, B.K., Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310 (2005), 1193–1196.
28. Kennedy, B.K., The genetics of ageing: insight from genome-wide approaches in invertebrate model organisms. J. Intern. Med. 263 (2008), 142–152.
29. Kennedy, B.K., Smith, E.D., Kaeberlein, M., The enigmatic role of Sir2 in aging. Cell 123 (2005), 548–550.
30. Longo, V.D., Shadel, G.S., Kaeberlein, M., Kennedy, B., Replicative and chronological aging in Saccharomyces cerevisiae. Cell Metab. 16 (2012), 18–31.
31. Louie, R.J., Guo, J., Rodgers, J.W., White, R., Shah, N., Pagant, S., Kim, P., Livstone, M., Dolinski, K., McKinney, B.A., Hong, J., Sorscher, E.J., Bryan, J., Miller, E.A., Hartman, J.L. IV, A yeast phenomic model for the gene interaction network modulating CFTR-∆F508 protein biogenesis. Genome Med., 4, 2012, 103.
32. Mani, R., St Onge, R.P., Hartman, J.L. IV, Giaever, G., Roth, F.P., Defining genetic interaction. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 3461–3466.
33. Matecic, M., Smith, D.L., Pan, X., Maqani, N., Bekiranov, S., Boeke, J.D., Smith, J.S., A microarray-based genetic screen for yeast chronological aging factors. PLoS Genet., 6, 2010, e1000921.
34. McCormick, M.A., Delaney, J.R., Tsuchiya, M., Tsuchiyama, S., Shemorry, A., Sim, S., Chou, A.C., Ahmed, U., Carr, D., Murakami, C.J., Schleit, J., Sutphin, G.L., Wasko, B.M., Bennett, C.F., Wang, A.M., Olsen, B., Beyer, R.P., Bammler, T.K., Prunkard, D., Johnson, S.C., Pennypacker, J.K., An, E., Anies, A., Castanza, A.S., Choi, E., Dang, N., Enerio, S., Fletcher, M., Fox, L., Goswami, S., Higgins, S.A., Holmberg, M.A., Hu, D., Hui, J., Jelic, M., Jeong, K.S., Johnston, E., Kerr, E.O., Kim, J., Kim, D., Kirkland, K., Klum, S., Kotireddy, S., Liao, E., Lim, M., Lin, M.S., Lo, W.C., Lockshon, D., Miller, H.A., Moller, R.M., Muller, B., Oakes, J., Pak, D.N., Peng, Z.J., Pham, K.M., Pollard, T.G., Pradeep, P., Pruett, D., Rai, D., Robison, B., Rodriguez, A.A., Ros, B., Sage, M., Singh, M.K., Smith, E.D., Snead, K., Solanky, A., Spector, B.L., Steffen, K.K., Tchao, B.N., Ting, M.K., Vander Wende, H., Wang, D., Welton, K.L., Westman, E.A., Brem, R.B., Liu, X.G., Suh, Y., Zhou, Z., Kaeberlein, M., Kennedy, B.K., A comprehensive analysis of replicative lifespan in 4698 single-gene deletion strains uncovers conserved mechanisms of aging. Cell Metab. 22 (2015), 895–906.
35. Mirisola, M.G., Longo, V.D., Acetic acid and acidification accelerate chronological and replicative aging in yeast. Cell Cycle 11 (2012), 3532–3533.
36. Murakami, C., Kaeberlein, M., Quantifying Yeast Chronological Life Span by Outgrowth of Aged Cells. (J Vis Exp), 2009.
37. Murakami, C.J., Burtner, C.R., Kennedy, B.K., Kaeberlein, M., A method for high-throughput quantitative analysis of yeast chronological life span. J. Gerontol. A Biol. Sci. Med. Sci. 63 (2008), 113–121.
38. Murakami, C.J., Wall, V., Basisty, N., Kaeberlein, M., Composition and acidification of the culture medium influences chronological aging similarly in vineyard and laboratory yeast. PLoS ONE, 6, 2011, e24530.
39. Murakami, C., Delaney, J.R., Chou, A., Carr, D., Schleit, J., Sutphin, G.L., An, E.H., Castanza, A.S., Fletcher, M., Goswami, S., Higgins, S., Holmberg, M., Hui, J., Jelic, M., Jeong, K.S., Kim, J.R., Klum, S., Liao, E., Lin, M.S., Lo, W., Miller, H., Moller, R., Peng, Z.J., Pollard, T., Pradeep, P., Pruett, D., Rai, D., Ros, V., Schuster, A., Singh, M., Spector, B.L., VanderWende, H., Wang, A.M., Wasko, B.M., Olsen, B., Kaeberlein, M., pH neutralization protects against reduction in replicative lifespan following chronological aging in yeast. Cell Cycle 11 (2012), 3087–3096.
40. Ocampo, A., Liu, J., Schroeder, E.A., Shadel, G.S., Barrientos, A., Mitochondrial respiratory thresholds regulate yeast chronological life span and its extension by caloric restriction. Cell Metab. 16 (2012), 55–67.
41. Ooi, S.L., Shoemaker, D.D., Boeke, J.D., DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat. Genet. 35 (2003), 277–286.
42. Orentreich, N., Matias, J.R., DeFelice, A., Zimmerman, J.A., Low methionine ingestion by rats extends life span. J. Nutr. 123 (1993), 269–274.
43. Pan, Y., Schroeder, E.A., Ocampo, A., Barrientos, A., Shadel, G.S., Regulation of yeast chronological life span by TORC1 via adaptive mitochondrial ROS signaling. Cell Metab. 13 (2011), 668–678.
44. Polymenis, M., Kennedy, B.K., Chronological and replicative lifespan in yeast: do they meet in the middle?. Cell Cycle 11 (2012), 3531–3532.
45. Powers, R.W. 3rd, Kaeberlein, M., Caldwell, S.D., Kennedy, B.K., Fields, S., Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 20 (2006), 174–184.
46. Rodgers, J., Guo, J., Hartman, J.L. IV, Phenomic assessment of genetic buffering by kinetic analysis of cell arrays. Methods Mol. Biol. 1205 (2014), 187–208.
47. Shah, N.A., Laws, R.J., Wardman, B., Zhao, L.P., Hartman, J.L. IV, Accurate, precise modeling of cell proliferation kinetics from time-lapse imaging and automated image analysis of agar yeast culture arrays. BMC Syst. Biol., 1, 2007, 3.
48. Smith, E.D., Kennedy, B.K., Kaeberlein, M., Genome-wide identification of conserved longevity genes in yeast and worms. Mech. Ageing Dev. 128 (2007), 106–111.
49. Smith, E.D., Tsuchiya, M., Fox, L.A., Dang, N., Hu, D., Kerr, E.O., Johnston, E.D., Tchao, B.N., Pak, D.N., Welton, K.L., Promislow, D.E., Thomas, J.H., Kaeberlein, M., Kennedy, B.K., Quantitative evidence for conserved longevity pathways between divergent eukaryotic species. Genome Res. 18 (2008), 564–570.
50. Strong, R., Miller, R.A., Astle, C.M., Floyd, R.A., Flurkey, K., Hensley, K.L., Javors, M.A., Leeuwenburgh, C., Nelson, J.F., Ongini, E., Nadon, N.L., Warner, H.R., Harrison, D.E., Nordihydroguaiaretic acid and aspirin increase lifespan of genetically heterogeneous male mice. Aging Cell 7 (2008), 641–650.
51. Troen, A.M., French, E.E., Roberts, J.F., Selhub, J., Ordovas, J.M., Parnell, L.D., Lai, C.Q., Lifespan modification by glucose and methionine in Drosophila melanogaster fed a chemically defined diet. Age (Dordr) 29 (2007), 29–39.
52. Wei, M., Madia, F., Longo, V.D., Studying age-dependent genomic instability using the S. cerevisiae chronological lifespan model. J. Vis. Exp, 2011.
53. Wickerham, L.J., A critical evaluation of the nitrogen assimilation tests commonly used in the classification of yeasts. J. Bacteriol. 52 (1946), 293–301.
54. Wierman, M.B., Matecic, M., Valsakumar, V., Li, M., Smith, D.L. Jr., Bekiranov, S., Smith, J.S., Functional genomic analysis reveals overlapping and distinct features of chronologically long-lived yeast populations. Aging (Albany NY) 7 (2015), 177–194.
55. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J.D., Bussey, H., Chu, A.M., Connelly, C., Davis, K., Dietrich, F., Dow, S.W., El Bakkoury, M., Foury, F., Friend, S.H., Gentalen, E., Giaever, G., Hegemann, J.H., Jones, T., Laub, M., Liao, H., Davis, R.W., et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285 (1999), 901–906.
56. Yuan, D.S., Pan, X., Ooi, S.L., Peyser, B.D., Spencer, F.A., Irizarry, R.A., Boeke, J.D., Improved microarray methods for profiling the yeast knockout strain collection. Nucleic Acids Res., 33, 2005, e103.