Chromosome-specific and global effects of aneuploidy in Saccharomyces cerevisiae

Genetics

Volumn 202, Issue 4, 2016, Pages 1395-1409

  Dodgson, Stacie E ^a,b   Kim, Sharon ^a,b   Costanzo, Michael ^c   Baryshnikova, Anastasia ^d   Morse, Darcy L ^b   Kaiser, Chris A ^b   Boone, Charles ^c   Amon, Angelika ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d PRINCETON UNIVERSITY   (United States)

Author keywords

Aneuploidy; Dosage imbalance; Protein transport; Synthetic lethality

Indexed keywords

FUNGAL PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ANEUPLOIDY; ARTICLE; CHROMOSOME; DISOMY; FUNGAL CELL WALL; FUNGAL GENE; FUNGAL STRAIN; GENE DELETION; GENE DOSAGE; GENETIC ANALYSIS; KARYOTYPE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SYNTHETIC GENE ARRAY; GENE EXPRESSION PROFILING; GENETICS; LETHAL MUTATION; METABOLISM; PROCEDURES; REPRODUCTIVE FITNESS;

ANEUPLOIDY; CHROMOSOMES, FUNGAL; GENE DELETION; GENE DOSAGE; GENE EXPRESSION PROFILING; GENETIC FITNESS; KARYOTYPE; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SYNTHETIC LETHAL MUTATIONS;

EID: 84979901324     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.185660     Document Type: Article

References (74)

1. Abe, F., K. Usui, and T. Hiraki, 2009 Fluconazole modulates membrane rigidity, heterogeneity, and water penetration into the plasma membrane in Saccharomyces cerevisiae. Biochemistry 48: 8494–8504.
2. Baryshnikova, A., and B. Andrews, 2012 Neighboring-gene effect: a genetic uncertainty principle. Nat. Methods 9: 341–343.
3. Baryshnikova, A., M. Costanzo, Y. Kim, H. Ding, J. Koh et al., 2010 Quantitative analysis of fitness and genetic interactions in yeast on a genome scale. Nat. Methods 7: 1017–1024.
4. Baryshnikova, A., B. VanderSluis, M. Costanzo, C. L. Myers, R. S. Cha et al., 2013 Global linkage map connects meiotic centromere function to chromosome size in budding yeast. G3 (Bethesda) 3: 1741–1751.
5. Baxter, B. K., and E. A. Craig, 1998 Isolation of UBP3, encoding a de-ubiquitinating enzyme, as a multicopy suppressor of a heat-shock mutant strain of S. cerevisiae. Curr. Genet. 33: 412–419.
6. Bell, W., P. Klaassen, M. Ohnacker, T. Boller, M. Herweijer et al., 1992 Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation. Eur. J. Biochem. 209: 951–959.
7. Ben-Shitrit, T., N. Yosef, K. Shemesh, R. Sharan, E. Ruppin et al., 2012 Systematic identification of gene annotation errors in the widely used yeast mutation collections. Nat. Methods 9: 373–378.
8. Beroukhim, R., C. H. Mermel, D. Porter, G. Wei, S. Raychaudhuri et al., 2010 The landscape of somatic copy-number alteration across human cancers. Nature 463: 899–905.
9. Biggins, S., F. F. Severin, N. Bhalla, I. Sassoon, A. A. Hyman et al., 1999 The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev. 13: 532–544.
10. Blank, H. M., J. M. Sheltzer, C. M. Meehl, and A. Amon, 2015 Mitotic entry in the presence of DNA damage is a widespread property of aneuploidy in yeast. Mol. Biol. Cell 26: 1440–1451.
11. Bonney, M. E., H. Moriya, and A. Amon, 2015 Aneuploid proliferation defects in yeast are not driven by copy number changes of a few dosage-sensitive genes. Genes Dev. 29: 898–903.
12. Castrejon, F., A. Gomez, M. Sanz, A. Durán, and C. Roncero, 2006 The RIM101 pathway contributes to yeast cell wall assembly and its function becomes essential in the absence of mitogen-activated protein kinase Slt2p. Eukaryot. Cell 5: 507–517.
13. Chan, C. S., and D. Botstein, 1993 Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast. Genetics 135: 677–691.
14. Chen, G., W. D. Bradford, C. W. Seidel, and R. Li, 2012 Hsp90 stress potentiates rapid cellular adaptation through induction of aneuploidy. Nature 482: 246–250.
15. Chen, G., W. A. Mulla, A. Kucharavy, H.-J. Tsai, B. Rubinstein et al., 2015 Targeting the adaptability of heterogeneous aneuploids. Cell 160: 771–784.
16. Cohen, M., F. Stutz, N. Belgareh, R. Haguenauer-Tsapis, and C. Dargemont, 2003 Ubp3 requires a cofactor, Bre5, to specifically de-ubiquitinate the COPII protein, Sec23. Nat. Cell Biol. 5: 661–667.
17. Costanzo, M., A. Baryshnikova, J. Bellay, Y. Kim, E. D. Spear et al., 2010 The genetic landscape of a cell. Science 327: 425–431.
18. D’Amore, T., R. Crumplen, and G. G. Stewart, 1991 The involvement of trehalose in yeast stress tolerance. J. Ind. Microbiol. 7: 191–196.
19. Dephoure, N., S. Hwang, C. O’Sullivan, S. E. Dodgson, S. P. Gygi et al., 2014 Quantitative proteomic analysis reveals posttranslational responses to aneuploidy in yeast. eLife 3: e03023.
20. Dinter, A., and E. G. Berger, 1998 Golgi-disturbing agents. Histochem. Cell Biol. 109: 571–590.
21. Dulic, V., M. Egerton, I. Elguindi, S. Raths, B. Singer et al., 1991 Yeast endocytosis assays. Methods Enzymol. 194: 697–710.
22. Duncan, M. C., M. J. Cope, B. L. Goode, B. Wendland, and D. G. Drubin, 2001 Yeast Eps15-like endocytic protein, Pan1p, activates the Arp2/3 complex. Nat. Cell Biol. 3: 687–690.
23. Fotso, P., Y. Koryakina, O. Pavliv, A. B. Tsiomenko, and V. V. Lupashin, 2005 Cog1p plays a central role in the organization of the yeast conserved oligomeric Golgi complex. J. Biol. Chem. 280: 27613–27623.
24. Gagny, B., A. Wiederkehr, P. Dumoulin, B. Winsor, H. Riezman et al., 2000 A novel EH domain protein of Saccharomyces cerevisiae, Ede1p, involved in endocytosis. J. Cell Sci. 113(Pt 18): 3309–3319.
25. Giaever, G., and C. Nislow, 2014 The yeast deletion collection: a decade of functional genomics. Genetics 197: 451–465.
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. Goode, B. L., J. A. Eskin, and B. Wendland, 2015 Actin and endocytosis in budding yeast. Genetics 199: 315–358.
28. Gordon, D. J., B. Resio, and D. Pellman, 2012 Causes and consequences of aneuploidy in cancer. Nat. Rev. Genet. 13: 189–203.
29. Grade, M., H. Becker, T. Liersch, T. Ried, and B. M. Ghadimi, 2006 Molecular cytogenetics: genomic imbalances in colorectal cancer and their clinical impact. Cell. Oncol. 28: 71–84.
30. Hughes, T. R., C. J. Roberts, H. Dai, A. R. Jones, M. R. Meyer et al., 2000 Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25: 333–337.
31. Jorgensen, P., B. Nelson, M. D. Robinson, Y. Chen, B. Andrews et al., 2002 High-resolution genetic mapping with ordered arrays of Saccharomyces cerevisiae deletion mutants. Genetics 162: 1091–1099.
32. Jovanovic, P., M. Mihajlovic, J. Djordjevic-Jocic, S. Vlajkovic, S. Cekic et al., 2013 Ocular melanoma: an overview of the current status. Int. J. Clin. Exp. Pathol. 6: 1230–1244.
33. Jungmann, J., J. C. Rayner, and S. Munro, 1999 The Saccharomyces cerevisiae protein Mnn10p/Bed1p is a subunit of a Golgi mannosyltransferase complex. J. Biol. Chem. 274: 6579–6585.
34. Koh, J. L. Y., H. Ding, M. Costanzo, A. Baryshnikova, K. Toufighi et al., 2009 DRYGIN: a database of quantitative genetic interaction networks in yeast. Nucleic Acids Res. 38: D502–D507.
35. Kontoyiannis, D. P., 2000 Modulation of fluconazole sensitivity by the interaction of mitochondria and erg3p in Saccharomyces cerevisiae. J. Antimicrob. Chemother. 46: 191–197.
36. Kornberg, A., N. N. Rao, and D. Ault-Riché, 1999 Inorganic polyphosphate: a molecule of many functions. Annu. Rev. Biochem. 68: 89–125.
37. Longtine, M. S., A. McKenzie, D. J. Demarini, N. G. Shah, A. Wach et al., 1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953–961.
38. Lopez-Gines, C., M. Cerda-Nicolas, R. Gil-Benso, A. Pellin, J. A. Lopez-Guerrero et al., 2005 Association of chromosome 7, chromosome 10 and EGFR gene amplification in glioblastoma multiforme. Clin. Neuropathol. 24: 209–218.
39. Makanae, K., R. Kintaka, T. Makino, H. Kitano, and H. Moriya, 2012 Identification of dosage-sensitive genes in Saccharomyces cerevisiae using the genetic tug-of-war method. Genome Res. 23: 300–311.
40. Maurici, D., A. Perez-Atayde, H. E. Grier, N. Baldini, M. Serra et al., 1998 Frequency and implications of chromosome 8 and 12 gains in Ewing sarcoma. Cancer Genet. Cytogenet. 100: 106–110.
41. Moukadiri, I., J. Armero, A. Abad, R. Sentandreu, and J. Zueco, 1997 Identification of a mannoprotein present in the inner layer of the cell wall of Saccharomyces cerevisiae. J. Bacteriol. 179: 2154–2162.
42. Mrsa, V., M. Ecker, S. Strahl-Bolsinger, M. Nimtz, L. Lehle et al., 1999 Deletion of new covalently linked cell wall glycoproteins alters the electrophoretic mobility of phosphorylated wall components of Saccharomyces cerevisiae. J. Bacteriol. 181: 3076–3086.
43. Nagaoka, S. I., T. J. Hassold, and P. A. Hunt, 2012 Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Rev. Genet. 13: 493–504.
44. Oromendia, A. B., S. E. Dodgson, and A. Amon, 2012 Aneuploidy causes proteotoxic stress in yeast. Genes Dev. 26: 2696–2708.
45. Ossareh-Nazari, B., M. Cohen, and C. Dargemont, 2010 The Rsp5 ubiquitin ligase and the AAA-ATPase Cdc48 control the ubiquitin-mediated degradation of the COPII component Sec23. Exp. Cell Res. 316: 3351–3357.
46. Pavelka, N., G. Rancati, J. Zhu, W. D. Bradford, A. Saraf et al., 2010 Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468: 321–325.
47. Pestov, N. A., T. V. Kulakovskaya, and I. S. Kulaev, 2005 Effects of inactivation of the PPN1 gene on exopolyphosphatases, inorganic polyphosphates and function of mitochondria in the yeast Saccharomyces cerevisiae. FEMS Yeast Res. 5: 823–828.
48. Ram, A. F. J., and F. M. Klis, 2006 Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat. Protoc. 1: 2253–2256.
49. Ram, R. J., B. Li, and C. A. Kaiser, 2002 Identification of Sec36p, Sec37p, and Sec38p: components of yeast complex that contains Sec34p and Sec35p. Mol. Biol. Cell 13: 1484–1500.
50. Santaguida, S., E. Vasile, E. White, and A. Amon, 2015 Aneuploidy-induced cellular stresses limit autophagic degradation. Genes Dev. 29: 2010–2021.
51. Sethuraman, A., N. N. Rao, and A. Kornberg, 2001 The endopolyphosphatase gene: essential in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98: 8542–8547.
52. Shah, N., and R. D. Klausner, 1993 Brefeldin A reversibly inhibits secretion in Saccharomyces cerevisiae. J. Biol. Chem. 268: 5345–5348.
53. Sheltzer, J. M., H. M. Blank, S. J. Pfau, Y. Tange, B. M. George et al., 2011 Aneuploidy drives genomic instability in yeast. Science 333: 1026–1030.
54. Singer, M. A., and S. Lindquist, 1998 Multiple effects of trehalose on protein folding in vitro and in vivo. Mol. Cell 1: 639–648.
55. Smaczynska-de Rooij, I. I., E. G. Allwood, R. Mishra, W. I. Booth, S. Aghamohammadzadeh et al., 2011 Yeast dynamin Vps1 and amphiphysin Rvs167 function together during endocytosis. Traffic 13: 317–328.
56. Smith, R. D., and V. V. Lupashin, 2008 Role of the conserved oligomeric Golgi (COG) complex in protein glycosylation. Carbohydr. Res. 343: 2024–2031.
57. Sopko, R., D. Huang, N. Preston, G. Chua, B. Papp et al., 2006 Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell 21: 319–330.
58. Stingele, S., G. Stoehr, K. Peplowska, J. U. R. Cox, M. Mann et al., 2012 Global analysis of genome, transcriptome and proteome reveals the response to aneuploidy in human cells. Mol. Syst. Biol. 8: 1–12.
59. Suvorova, E. S., 2002 The Sec34/Sec35p complex, a Ypt1p effec-tor required for retrograde intra-Golgi trafficking, interacts with Golgi SNAREs and COPI vesicle coat proteins. J. Cell Biol. 157: 631–643.
60. Tang, Y.-C., B. R. Williams, J. J. Siegel, and A. Amon, 2011 Identification of aneuploidy-selective antiproliferation compounds. Cell 144: 499–512.
61. Thorburn, R. R., C. Gonzalez, G. A. Brar, S. Christen, T. M. Carlile et al., 2013 Aneuploid yeast strains exhibit defects in cell growth and passage through START. Mol. Biol. Cell 24: 1274–1289.
62. Tong, A. H. Y., 2001 Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364–2368.
63. Tong, A. H. Y., and C. Boone, 2012 Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 313: 171–192.
64. Torres, E. M., T. Sokolsky, C. M. Tucker, L. Y. Chan, M. Boselli et al., 2007 Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916–924.
65. Torres, E. M., N. Dephoure, A. Panneerselvam, C. M. Tucker, C. A. Whittaker et al., 2010 Identification of aneuploidy-tolerating mutations. Cell 143: 71–83.
66. Ungar, D., T. Oka, M. Krieger, and F. M. Hughson, 2006 Retrograde transport on the COG railway. Trends Cell Biol. 16: 113–120.
67. Wagih, O., M. Usaj, A. Baryshnikova, B. VanderSluis, E. Kuzmin et al., 2013 SGAtools: one-stop analysis and visualization of array-based genetic interaction screens. Nucleic Acids Res. 41: W591–W596.
68. Weaver, B. A., and D. W. Cleveland, 2006 Does aneuploidy cause cancer? Curr. Opin. Cell Biol. 18: 658–667.
69. Whyte, J. R., and S. Munro, 2001 The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic. Dev. Cell 1: 527–537.
70. Willett, R., D. Ungar, and V. Lupashin, 2013 The Golgi puppet master: COG complex at center stage of membrane trafficking interactions. Histochem. Cell Biol. 140: 271–283.
71. Williams, B. R., V. R. Prabhu, K. E. Hunter, C. M. Glazier, C. A. Whittaker et al., 2008 Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 322: 703–709.
72. Youn, J.-Y., H. Friesen, T. Kishimoto, W. M. Henne, C. F. Kurat et al., 2010 Dissecting BAR domain function in the yeast Amphiphysins Rvs161 and Rvs167 during endocytosis. Mol. Biol. Cell 21: 3054–3069.
73. Zeng, G., and M. Cai, 1999 Regulation of the actin cytoskeleton organization in yeast by a novel serine/threonine kinase Prk1p. J. Cell Biol. 144: 71–82.
74. Zeng, G., and M. Cai, 2005 Prk1p. Int. J. Biochem. Cell Biol. 37: 48–53.