Identification of dosage-sensitive genes in Saccharomyces cerevisiae using the genetic tug-of-war method

Genome Research

Volumn 23, Issue 2, 2013, Pages 300-311

  Makanae, Koji ^a   Kintaka, Reiko ^a   Makino, Takashi ^b   Kitano, Hiroaki ^c,d,e   Moriya, Hisao ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

^c SONY COMPUTER SCIENCE LABORATORIES INC   (Japan)

^d Systems Biology Institute   (Japan)

^e OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; GENE DOSAGE; GENE IDENTIFICATION; GENE ISOLATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC PROCEDURES; GENETIC TUG OF WAR METHOD; INTRACELLULAR TRANSPORT; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

GENE DOSAGE; GENE EXPRESSION; GENE REGULATORY NETWORKS; GENES, FUNGAL; GENOME, FUNGAL; MOLECULAR SEQUENCE ANNOTATION; OPEN READING FRAMES; PROTEIN INTERACTION MAPS; SACCHAROMYCES CEREVISIAE;

EID: 84873345436     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.146662.112     Document Type: Article

References (48)

1. Abruzzi KC, SmithA,ChenW, Solomon F. 2002. Protection from free b-tubulin by the b-tubulin binding protein Rbl2p. Mol Cell Biol 22: 138-147.
2. Akada R, Yamamoto J, Yamashita I. 1997. Screening and identification of yeast sequences that cause growth inhibition when overexpressed. Mol Gen Genet 254: 267-274.
3. Alon U, Surette MG, Barkai N, Leibler S. 1999. Robustness in bacterial chemotaxis. Nature 397: 168-171.
4. Amberg DC, Burke D, Strathern JN. 2005. Methods in yeast genetics: A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor Laboratory Press, New York.
5. Boyer J, Badis G, Fairhead C, Talla E, Hantraye F, Fabre E, Fischer G, Hennequin C, Koszul R, Lafontaine I, et al. 2004. Large-scale exploration of growth inhibition caused by overexpression of genomic fragments in Saccharomyces cerevisiae. Genome Biol 5: R72.
6. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. 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.
7. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
8. Clotet J, Garí E, Aldea M, Arino J. 1999. The yeast ser/thr phosphatases sit4 and ppz1 play opposite roles in regulation of the cell cycle. Mol Cell Biol 19: 2408-2415.
9. Cormack BP, Bertram G, Egerton M, Gow NA, Falkow S, Brown AJ. 1997. Yeast-enhanced green fluorescent protein (yEGFP): A reporter of gene expression in Candida albicans. Microbiology 143: 303-311.
10. Dekel E, Alon U. 2005. Optimality and evolutionary tuning of the expression level of a protein. Nature 436: 588-592.
11. de Nadal E, Clotet J, Posas F, Serrano R, Gomez N, Arino J. 1998. The yeast halotolerance determinant Hal3p is an inhibitory subunit of the Ppz1p Ser/Thr protein phosphatase. Proc Natl Acad Sci 95: 7357-7362.
12. Espinet C, de la Torre MA, Aldea M, Herrero E. 1995. An efficient method to isolate yeast genes causing overexpression-mediated growth arrest. Yeast 11: 25-32.
13. Gelperin DM, White MA, Wilkinson ML, Kon Y, Kung LA, Wise KJ, Lopez-Hoyo N, Jiang L, Piccirillo S, Yu H, et al. 2005. Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev 19: 2816-2826.
14. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK,Weissman JS. 2003. Global analysis of protein expression in yeast. Nature 425: 737-741.
15. Jones GM, Stalker J, Humphray S,West A, Cox T, Rogers J, Dunham I, Prelich G. 2008. A systematic library for comprehensive overexpression screens in Saccharomyces cerevisiae. Nat Methods 5: 239-241.
16. Jungbluth M, Renicke C, Taxis C. 2010. Targeted protein depletion in Saccharomyces cerevisiae by activation of a bidirectional degron. BMC Syst Biol 4: 176.
17. Kaizu K, Moriya H, KitanoH. 2010. Fragilities caused by dosage imbalance in regulation of the budding yeast cell cycle. PLoS Genet 6: e1000919.
18. Krantz M, Ahmadpour D, Ottosson LG, Warringer J, Waltermann C, Nordlander B, Klipp E, Blomberg A, Hohmann S, Kitano H. 2009. Robustness and fragility in the yeast high osmolarity glycerol (HOG) signal-transduction pathway. Mol Syst Biol 5: 281.
19. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: An information aesthetic for comparative genomics. Genome Res 19: 1639-1645.
20. Little JW, Shepley DP, Wert DW. 1999. Robustness of a gene regulatory circuit. EMBO J 18: 4299-4307.
21. Liu H, Krizek J, Bretscher A. 1992. Construction of a GAL1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes lethality in yeast. Genetics 132: 665-673.
22. Makino T, McLysaght A. 2010. Ohnologs in the human genome are dosage balanced and frequently associated with disease. Proc Natl Acad Sci 107: 9270-9274.
23. Mazón MJ, Behrens MM, Morgado E, Portillo F. 1993. Low activity of the yeast cAMP-dependent protein kinase catalytic subunit Tpk3 is due to the poor expression of the TPK3 gene. Eur J Biochem 213: 501-506.
24. Moriya H, Shimizu-Yoshida Y, Kitano H. 2006. In vivo robustness analysis of cell division cycle genes in Saccharomyces cerevisiae. PLoS Genet 2: e111.
25. Moriya H,Chino A, Kapuy O, Csika'sz-Nagy A, Nova'k B. 2011. Overexpression limits of fission yeast cell-cycle regulators in vivo and in silico. Mol Syst Biol 7: 556.
26. Moriya H, Makanae K, Watanabe K, Chino A, Shimizu-Yoshida Y. 2012. Robustness analysis of cellular systems using the genetic tug-of-war method. Mol Biosyst 8: 2513-2522.
27. Nehlin JO, Carlberg M, Ronne H. 1992. Yeast SKO1 gene encodes a bZIP protein that binds to the CRE motif and acts as a repressor of transcription. Nucleic Acids Res 20: 5271-5278.
28. NiuW, Li Z, ZhanW, Iyer VR, Marcotte EM. 2008. Mechanisms of cell cycle control revealed by a systematic and quantitative overexpression screen in S. cerevisiae. PLoS Genet 4: e1000120.
29. Oldenburg KR, Vo KT, Michaelis S, Paddon C. 1997. Recombinationmediated PCR-directed plasmid construction in vivo in yeast. Nucleic Acids Res 25: 451-452.
30. Ortiz D, Medkova M,Walch-Solimena C, Novick P. 2002. Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J Cell Biol 157: 1005-1015.
31. Palmer LK, Baptiste BA, Fester JC, Perkins JC, Keil RL. 2009. RRD1, a component of the TORC1 signalling pathway, affects anaesthetic response in Saccharomyces cerevisiae. Yeast 26: 655-661.
32. Papp B, Pál C, Hurst LD. 2003. Dosage sensitivity and the evolution of gene families in yeast. Nature 424: 194-197.
33. Park JE, Park CJ, Sakchaisri K, Karpova T, Asano S, McNally J, Sunwoo Y, Leem SH, Lee KS. 2004. Novel functional dissection of the localization-specific roles of budding yeast polo kinase Cdc5p. Mol Cell Biol 24: 9873-9886.
34. Partow S, Siewers V, Bjørn S, Nielsen J, Maury J. 2010. Characterization of different promoters for designing a new expression vector in Saccharomyces cerevisiae. Yeast 27: 955-964.
35. Sheltzer JM, Amon A. 2011. The aneuploidy paradox: Costs and benefits of an incorrect karyotype. Trends Genet 27: 446-453.
36. Sopko R, Huang D, Preston N, Chua G, Papp B, Kafadar K, Snyder M, Oliver SG, Cyert M, Hughes TR, et al. 2006. Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell 21: 319-330.
37. Stevens RC, Davis TN. 1998. Mlc1p is a light chain for the unconventional myosin Myo2p in Saccharomyces cerevisiae. J Cell Biol 142: 711-722.
38. Stevenson LF, Kennedy BK, Harlow E. 2001. A large-scale overexpression screen in Saccharomyces cerevisiae identifies previously uncharacterized cell cycle genes. Proc Natl Acad Sci 98: 3946-3951.
39. Stoebel DM, Dean AM, Dykhuizen DE. 2008. The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178: 1653-1660.
40. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, Dunham MJ, Amon A. 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916-924.
41. Vavouri T, Semple JI, Garcia-Verdugo R, Lehner B. 2009. Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell 138: 198-208.
42. Veitia RA, Birchler JA. 2010. Dominance and gene dosage balance in health and disease: Why levels matter! J Pathol 220: 174-185.
43. Veitia RA, Bottani S, Birchler JA. 2008. Cellular reactions to gene dosage imbalance: Genomic, transcriptomic and proteomic effects. Trends Genet 24: 390-397.
44. von Dassow G, Meir E, Munro EM, Odell GM. 2000. The segment polarity network is a robust developmental module. Nature 406: 188-192.
45. Wagner A. 2005. Energy constraints on the evolution of gene expression. Mol Biol Evol 22: 1365-1374.
46. Weinstein B, Solomon F. 1990. Phenotypic consequences of tubulin overproduction in Saccharomyces cerevisiae: Differences between a-tubulin and b-tubulin. Mol Cell Biol 10: 5295-5304.
47. Yoshikawa K, Tanaka T, Ida Y, Furusawa C, Hirasawa T, Shimizu H. 2011. Comprehensive phenotypic analysis of single-gene deletion and overexpression strains of Saccharomyces cerevisiae. Yeast 28: 349-361.
48. Zaslaver A, Mayo AE, Rosenberg R, Bashkin P, Sberro H, Tsalyuk M, Surette MG, Alon U. 2004. Just-in-time transcription program in metabolic pathways. Nat Genet 36: 486-491.