Gene copy-number alterations: A cost-benefit analysis

Cell

Volumn 152, Issue 3, 2013, Pages 394-405

  Tang, Yun Chi ^a   Amon, Angelika ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ANEUPLOIDY; CELL PROLIFERATION; CELL STRESS; COPY NUMBER VARIATION; COST BENEFIT ANALYSIS; GENE AMPLIFICATION; GENE DELETION; GENE DOSAGE; GENE MUTATION; GENE OVEREXPRESSION; GENOMIC INSTABILITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SURVIVAL;

EID: 84873314664     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.11.043     Document Type: Review

References (116)

1. C. Alkan, B.P. Coe, and E.E. Eichler Genome structural variation discovery and genotyping Nat. Rev. Genet. 12 2011 363 376
2. D.J. Baker, K.B. Jeganathan, J.D. Cameron, M. Thompson, S. Juneja, A. Kopecka, R. Kumar, R.B. Jenkins, P.C. de Groen, P. Roche, and J.M. van Deursen BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice Nat. Genet. 36 2004 744 749
3. J. Baselga, L. Norton, J. Albanell, Y.M. Kim, and J. Mendelsohn Recombinant humanized anti-HER2 antibody (Herceptin) enhances the antitumor activity of paclitaxel and doxorubicin against HER2/neu overexpressing human breast cancer xenografts Cancer Res. 58 1998 2825 2831
4. J.B. Berletch, F. Yang, J. Xu, L. Carrel, and C.M. Disteche Genes that escape from X inactivation Hum. Genet. 130 2011 237 245
5. M.J. Brauer, C. Huttenhower, E.M. Airoldi, R. Rosenstein, J.C. Matese, D. Gresham, V.M. Boer, O.G. Troyanskaya, and D. Botstein Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast Mol. Biol. Cell 19 2008 352 367
6. C.J. Brown, K.M. Todd, and R.F. Rosenzweig Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment Mol. Biol. Evol. 15 1998 931 942
7. D.D. Brown, and I.B. Dawid Specific gene amplification in oocytes. Oocyte nuclei contain extrachromosomal replicas of the genes for ribosomal RNA Science 160 1968 272 280
8. A.A. Burds, A.S. Lutum, and P.K. Sorger Generating chromosome instability through the simultaneous deletion of Mad2 and p53 Proc. Natl. Acad. Sci. USA 102 2005 11296 11301
9. D. Carling The AMP-activated protein kinase cascade - a unifying system for energy control Trends Biochem. Sci. 29 2004 18 24
10. Y. Chikashige, T. Haraguchi, and Y. Hiraoka Another way to move chromosomes Chromosoma 116 2007 497 505
11. J.M. Claycomb, and T.L. Orr-Weaver Developmental gene amplification: insights into DNA replication and gene expression Trends Genet. 21 2005 149 162
12. K. Crasta, N.J. Ganem, R. Dagher, A.B. Lantermann, E.V. Ivanova, Y. Pan, L. Nezi, A. Protopopov, D. Chowdhury, and D. Pellman DNA breaks and chromosome pulverization from errors in mitosis Nature 482 2012 53 58
13. C. Dai, and W. Gu p53 post-translational modification: deregulated in tumorigenesis Trends Mol. Med. 16 2010 528 536
14. E. de Stanchina, M.E. McCurrach, F. Zindy, S.Y. Shieh, G. Ferbeyre, A.V. Samuelson, C. Prives, M.F. Roussel, C.J. Sherr, and S.W. Lowe E1A signaling to p53 involves the p19(ARF) tumor suppressor Genes Dev. 12 1998 2434 2442
15. M. Dobles, V. Liberal, M.L. Scott, R. Benezra, and P.K. Sorger Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2 Cell 101 2000 635 645
16. A.W. Duncan, M.H. Taylor, R.D. Hickey, A.E. Hanlon Newell, M.L. Lenzi, S.B. Olson, M.J. Finegold, and M. Grompe The ploidy conveyor of mature hepatocytes as a source of genetic variation Nature 467 2010 707 710
17. A.W. Duncan, A.E. Hanlon Newell, W. Bi, M.J. Finegold, S.B. Olson, A.L. Beaudet, and M. Grompe Aneuploidy as a mechanism for stress-induced liver adaptation J. Clin. Invest. 122 2012 3307 3315
18. M.J. Dunham, H. Badrane, T. Ferea, J. Adams, P.O. Brown, F. Rosenzweig, and D. Botstein Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae Proc. Natl. Acad. Sci. USA 99 2002 16144 16149
19. T. Edlund, and S. Normark Recombination between short DNA homologies causes tandem duplication Nature 292 1981 269 271
20. L. Feuk, A.R. Carson, and S.W. Scherer Structural variation in the human genome Nat. Rev. Genet. 7 2006 85 97
21. B. Futcher, and J. Carbon Toxic effects of excess cloned centromeres Mol. Cell. Biol. 6 1986 2213 2222
22. J.G. Gall Differential synthesis of the genes for ribosomal RNA during amphibian oögenesis Proc. Natl. Acad. Sci. USA 60 1968 553 560
23. A.P. Gasch Comparative genomics of the environmental stress response in ascomycete fungi Yeast 24 2007 961 976
24. A.P. Gasch, P.T. Spellman, C.M. Kao, O. Carmel-Harel, M.B. Eisen, G. Storz, D. Botstein, and P.O. Brown Genomic expression programs in the response of yeast cells to environmental changes Mol. Biol. Cell 11 2000 4241 4257
25. K.A. Geiler-Samerotte, M.F. Dion, B.A. Budnik, S.M. Wang, D.L. Hartl, and D.A. Drummond Misfolded proteins impose a dosage-dependent fitness cost and trigger a cytosolic unfolded protein response in yeast Proc. Natl. Acad. Sci. USA 108 2011 680 685
26. S. Girirajan, C.D. Campbell, and E.E. Eichler Human copy number variation and complex genetic disease Annu. Rev. Genet. 45 2011 203 226
27. D.J. Gordon, B. Resio, and D. Pellman Causes and consequences of aneuploidy in cancer Nat. Rev. Genet. 13 2012 189 203
28. D. Gresham, M.M. Desai, C.M. Tucker, H.T. Jenq, D.A. Pai, A. Ward, C.G. DeSevo, D. Botstein, and M.J. Dunham The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast PLoS Genet. 4 2008 e1000303
29. D. Gresham, R. Usaite, S.M. Germann, M. Lisby, D. Botstein, and B. Regenberg Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus Proc. Natl. Acad. Sci. USA 107 2010 18551 18556
30. A. Gropp, U. Kolbus, and D. Giers Systematic approach to the study of trisomy in the mouse. II Cytogenet. Cell Genet. 14 1975 42 62
31. M. Guo, and J.A. Birchler Trans-acting dosage effects on the expression of model gene systems in maize aneuploids Science 266 1994 1999 2002
32. C.O. Hanemann, and H.W. Müller Pathogenesis of Charcot-Marie-Tooth 1A (CMT1A) neuropathy Trends Neurosci. 21 1998 282 286
33. S. Hanks, K. Coleman, S. Reid, A. Plaja, H. Firth, D. Fitzpatrick, A. Kidd, K. Méhes, R. Nash, and N. Robin Constitutional aneuploidy and cancer predisposition caused by biallelic mutations in BUB1B Nat. Genet. 36 2004 1159 1161
34. T.J. Hassold, and P.A. Jacobs Trisomy in man Annu. Rev. Genet. 18 1984 69 97
35. C.N. Henrichsen, N. Vinckenbosch, S. Zöllner, E. Chaignat, S. Pradervand, F. Schütz, M. Ruedi, H. Kaessmann, and A. Reymond Segmental copy number variation shapes tissue transcriptomes Nat. Genet. 41 2009 424 429
36. A.J. Holland, and D.W. Cleveland Losing balance: the origin and impact of aneuploidy in cancer EMBO Rep. 13 2012 501 514
37. B. Huettel, D.P. Kreil, M. Matzke, and A.J. Matzke Effects of aneuploidy on genome structure, expression, and interphase organization in Arabidopsis thaliana PLoS Genet. 4 2008 e1000226
38. A.J. Iafrate, L. Feuk, M.N. Rivera, M.L. Listewnik, P.K. Donahoe, Y. Qi, S.W. Scherer, and C. Lee Detection of large-scale variation in the human genome Nat. Genet. 36 2004 949 951
39. A. Itsara, G.M. Cooper, C. Baker, S. Girirajan, J. Li, D. Absher, R.M. Krauss, R.M. Myers, P.M. Ridker, and D.I. Chasman Population analysis of large copy number variants and hotspots of human genetic disease Am. J. Hum. Genet. 84 2009 148 161
40. A. Itsara, H. Wu, J.D. Smith, D.A. Nickerson, I. Romieu, S.J. London, and E.E. Eichler De novo rates and selection of large copy number variation Genome Res. 20 2010 1469 1481
41. A. Janssen, M. van der Burg, K. Szuhai, G.J. Kops, and R.H. Medema Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations Science 333 2011 1895 1898
42. L. Jones, G. Wei, S. Sevcikova, V. Phan, S. Jain, A. Shieh, J.C. Wong, M. Li, J. Dubansky, and M.L. Maunakea Gain of MYC underlies recurrent trisomy of the MYC chromosome in acute promyelocytic leukemia J. Exp. Med. 207 2010 2581 2594
43. H. Kacser, and J.A. Burns The molecular basis of dominance Genetics 97 1981 639 666
44. P. Kahlem, M. Sultan, R. Herwig, M. Steinfath, D. Balzereit, B. Eppens, N.G. Saran, M.T. Pletcher, S.T. South, and G. Stetten Transcript level alterations reflect gene dosage effects across multiple tissues in a mouse model of down syndrome Genome Res. 14 2004 1258 1267
45. K. Kaizu, H. Moriya, and H. Kitano Fragilities caused by dosage imbalance in regulation of the budding yeast cell cycle PLoS Genet. 6 2010 e1000919
46. K.C. Kao, and G. Sherlock Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae Nat. Genet. 40 2008 1499 1504
47. W. Katz, B. Weinstein, and F. Solomon Regulation of tubulin levels and microtubule assembly in Saccharomyces cerevisiae: consequences of altered tubulin gene copy number Mol. Cell. Biol. 10 1990 5286 5294
48. J.C. Kim, J. Nordman, F. Xie, H. Kashevsky, T. Eng, S. Li, D.M. MacAlpine, and T.L. Orr-Weaver Integrative analysis of gene amplification in Drosophila follicle cells: parameters of origin activation and repression Genes Dev. 25 2011 1384 1398
49. M.A. Kingsbury, Y.C. Yung, S.E. Peterson, J.W. Westra, and J. Chun Aneuploidy in the normal and diseased brain Cell. Mol. Life Sci. 63 2006 2626 2641
50. T. Kobayashi, D.J. Heck, M. Nomura, and T. Horiuchi Expansion and contraction of ribosomal DNA repeats in Saccharomyces cerevisiae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I Genes Dev. 12 1998 3821 3830
51. J.P. Kruse, and W. Gu Modes of p53 regulation Cell 137 2009 609 622
52. L.V. Krushinski, A.P. Dyban, V.S. Baranov, I.I. Poletaeva, and L.G. Romanova [Behavior of mice with robertsonian translocations of chromosomes] Genetika 22 1986 434 441
53. H.M. Lachman, E. Pedrosa, O.A. Petruolo, M. Cockerham, A. Papolos, T. Novak, D.F. Papolos, and P. Stopkova Increase in GSK3beta gene copy number variation in bipolar disorder Am. J. Med. Genet. B. Neuropsychiatr. Genet. 144B 2007 259 265
54. J. Larsson, J.D. Chen, V. Rasheva, A. Rasmuson-Lestander, and V. Pirrotta Painting of fourth, a chromosome-specific protein in Drosophila Proc. Natl. Acad. Sci. USA 98 2001 6273 6278
55. B.H. Lee, M.J. Lee, S. Park, D.C. Oh, S. Elsasser, P.C. Chen, C. Gartner, N. Dimova, J. Hanna, and S.P. Gygi Enhancement of proteasome activity by a small-molecule inhibitor of USP14 Nature 467 2010 179 184
56. M. Li, X. Fang, Z. Wei, J.P. York, and P. Zhang Loss of spindle assembly checkpoint-mediated inhibition of Cdc20 promotes tumorigenesis in mice J. Cell Biol. 185 2009 983 994
57. M. Li, X. Fang, D.J. Baker, L. Guo, X. Gao, Z. Wei, S. Han, J.M. van Deursen, and P. Zhang The ATM-p53 pathway suppresses aneuploidy-induced tumorigenesis Proc. Natl. Acad. Sci. USA 107 2010 14188 14193
58. J.R. Lupski Genomic rearrangements and sporadic disease Nat. Genet. 39 7, Suppl 2007 S43 S47
59. R. Lyle, C. Gehrig, C. Neergaard-Henrichsen, S. Deutsch, and S.E. Antonarakis Gene expression from the aneuploid chromosome in a trisomy mouse model of down syndrome Genome Res. 14 2004 1268 1274
60. D. Malhotra, and J. Sebat CNVs: harbingers of a rare variant revolution in psychiatric genetics Cell 148 2012 1223 1241
61. M. Miclaus, J.H. Xu, and J. Messing Differential gene expression and epiregulation of alpha zein gene copies in maize haplotypes PLoS Genet. 7 2011 e1002131
62. D.K. Nguyen, and C.M. Disteche Dosage compensation of the active X chromosome in mammals Nat. Genet. 38 2006 47 53
63. D. Nijhawan, T.I. Zack, Y. Ren, M.R. Strickland, R. Lamothe, S.E. Schumacher, A. Tsherniak, H.C. Besche, J. Rosenbluh, and S. Shehata Cancer vulnerabilities unveiled by genomic loss Cell 150 2012 842 854
64. O. Niwa, Y. Tange, and A. Kurabayashi Growth arrest and chromosome instability in aneuploid yeast Yeast 23 2006 937 950
65. J. Nordman, and T.L. Orr-Weaver Regulation of DNA replication during development Development 139 2012 455 464
66. M.L. Oakes, K. Johzuka, L. Vu, K. Eliason, and M. Nomura Expression of rRNA genes and nucleolus formation at ectopic chromosomal sites in the yeast Saccharomyces cerevisiae Mol. Cell. Biol. 26 2006 6223 6238
67. H. Olzscha, S.M. Schermann, A.C. Woerner, S. Pinkert, M.H. Hecht, G.G. Tartaglia, M. Vendruscolo, M. Hayer-Hartl, F.U. Hartl, and R.M. Vabulas Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions Cell 144 2011 67 78
68. A.B. Oromendia, S.E. Dodgson, and A. Amon Aneuploidy causes proteotoxic stress in yeast Genes Dev. 26 2012 2696 2708
69. J.G. Paez, P.A. Jänne, J.C. Lee, S. Tracy, H. Greulich, S. Gabriel, P. Herman, F.J. Kaye, N. Lindeman, and T.J. Boggon EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy Science 304 2004 1497 1500
70. N. Pavelka, G. Rancati, J. Zhu, W.D. Bradford, A. Saraf, L. Florens, B.W. Sanderson, G.L. Hattem, and R. Li Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast Nature 468 2010 321 325
71. J.A. Pesin, and T.L. Orr-Weaver Regulation of APC/C activators in mitosis and meiosis Annu. Rev. Cell Dev. Biol. 24 2008 475 499
72. S.J. Pfau, and A. Amon Chromosomal instability and aneuploidy in cancer: from yeast to man EMBO Rep. 13 2012 515 527
73. M. Prestel, C. Feller, and P.B. Becker Dosage compensation and the global re-balancing of aneuploid genomes Genome Biol. 11 2010 216
74. F.R. Putkey, T. Cramer, M.K. Morphew, A.D. Silk, R.S. Johnson, J.R. McIntosh, and D.W. Cleveland Unstable kinetochore-microtubule capture and chromosomal instability following deletion of CENP-E Dev. Cell 3 2002 351 365
75. G. Rancati, N. Pavelka, B. Fleharty, A. Noll, R. Trimble, K. Walton, A. Perera, K. Staehling-Hampton, C.W. Seidel, and R. Li Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor Cell 135 2008 879 893
76. B. Regenberg, T. Grotkjaer, O. Winther, A. Fausbøll, M. Akesson, C. Bro, L.K. Hansen, S. Brunak, and J. Nielsen Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiae Genome Biol. 7 2006 R107
77. S.K. Rehen, M.J. McConnell, D. Kaushal, M.A. Kingsbury, A.H. Yang, and J. Chun Chromosomal variation in neurons of the developing and adult mammalian nervous system Proc. Natl. Acad. Sci. USA 98 2001 13361 13366
78. S.K. Rehen, Y.C. Yung, M.P. McCreight, D. Kaushal, A.H. Yang, B.S. Almeida, M.A. Kingsbury, K.M. Cabral, M.J. McConnell, and B. Anliker Constitutional aneuploidy in the normal human brain J. Neurosci. 25 2005 2176 2180
79. P.G. Richardson, P. Sonneveld, M.W. Schuster, D. Irwin, E.A. Stadtmauer, T. Facon, J.L. Harousseau, D. Ben-Yehuda, S. Lonial, H. Goldschmidt Assessment of Proteasome Inhibition for Extending Remissions (APEX) Investigators Bortezomib or high-dose dexamethasone for relapsed multiple myeloma N. Engl. J. Med. 352 2005 2487 2498
80. K.W. Runge, and V.A. Zakian Introduction of extra telomeric DNA sequences into Saccharomyces cerevisiae results in telomere elongation Mol. Cell. Biol. 9 1989 1488 1497
81. J. Sebat, B. Lakshmi, J. Troge, J. Alexander, J. Young, P. Lundin, S. Månér, H. Massa, M. Walker, and M. Chi Large-scale copy number polymorphism in the human genome Science 305 2004 525 528
82. A. Selmecki, A. Forche, and J. Berman Aneuploidy and isochromosome formation in drug-resistant Candida albicans Science 313 2006 367 370
83. M. Serrano, A.W. Lin, M.E. McCurrach, D. Beach, and S.W. Lowe Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a Cell 88 1997 593 602
84. J.M. Sheltzer, H.M. Blank, S.J. Pfau, Y. Tange, B.M. George, T.J. Humpton, I.L. Brito, Y. Hiraoka, O. Niwa, and A. Amon Aneuploidy drives genomic instability in yeast Science 333 2011 1026 1030
85. J.M. Sheltzer, E.M. Torres, M.J. Dunham, and A. Amon Transcriptional consequences of aneuploidy Proc. Natl. Acad. Sci. USA 109 2012 12644 12649
86. A.B. Singleton, M. Farrer, J. Johnson, A. Singleton, S. Hague, J. Kachergus, M. Hulihan, T. Peuralinna, A. Dutra, and R. Nussbaum alpha-Synuclein locus triplication causes Parkinson's disease Science 302 2003 841
87. D.J. Slamon, G.M. Clark, S.G. Wong, W.J. Levin, A. Ullrich, and W.L. McGuire Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene Science 235 1987 177 182
88. A.C. Spradling The organization and amplification of two chromosomal domains containing Drosophila chorion genes Cell 27 1981 193 201
89. P. Stenberg, and J. Larsson Buffering and the evolution of chromosome-wide gene regulation Chromosoma 120 2011 213 225
90. P.J. Stephens, C.D. Greenman, B. Fu, F. Yang, G.R. Bignell, L.J. Mudie, E.D. Pleasance, K.W. Lau, D. Beare, and L.A. Stebbings Massive genomic rearrangement acquired in a single catastrophic event during cancer development Cell 144 2011 27 40
91. S. Stingele, G. Stoehr, K. Peplowska, J. Cox, M. Mann, and Z. Storchova Global analysis of genome, transcriptome and proteome reveals the response to aneuploidy in human cells Mol. Syst. Biol. 8 2012 608
92. Z. Storchová, A. Breneman, J. Cande, J. Dunn, K. Burbank, E. O'Toole, and D. Pellman Genome-wide genetic analysis of polyploidy in yeast Nature 443 2006 541 547
93. B.E. Stranger, M.S. Forrest, M. Dunning, C.E. Ingle, C. Beazley, N. Thorne, R. Redon, C.P. Bird, A. de Grassi, and C. Lee Relative impact of nucleotide and copy number variation on gene expression phenotypes Science 315 2007 848 853
94. X. Su, W. Qiu, M.L. Gupta Jr., J.B. Pereira-Leal, S.L. Reck-Peterson, and D. Pellman Mechanisms underlying the dual-mode regulation of microtubule dynamics by Kip3/kinesin-8 Mol. Cell 43 2011 751 763
95. Y.C. Tang, B.R. Williams, J.J. Siegel, and A. Amon Identification of aneuploidy-selective antiproliferation compounds Cell 144 2011 499 512
96. S.L. Thompson, and D.A. Compton Examining the link between chromosomal instability and aneuploidy in human cells J. Cell Biol. 180 2008 665 672
97. S.L. Thompson, and D.A. Compton Proliferation of aneuploid human cells is limited by a p53-dependent mechanism J. Cell Biol. 188 2010 369 381
98. F. Toledo, and G.M. Wahl Regulating the p53 pathway: in vitro hypotheses, in vivo veritas Nat. Rev. Cancer 6 2006 909 923
99. E.M. Torres, T. Sokolsky, C.M. Tucker, L.Y. Chan, M. Boselli, M.J. Dunham, and A. Amon Effects of aneuploidy on cellular physiology and cell division in haploid yeast Science 317 2007 916 924
100. E.M. Torres, B.R. Williams, and A. Amon Aneuploidy: cells losing their balance Genetics 179 2008 737 746
101. E.M. Torres, N. Dephoure, A. Panneerselvam, C.M. Tucker, C.A. Whittaker, S.P. Gygi, M.J. Dunham, and A. Amon Identification of aneuploidy-tolerating mutations Cell 143 2010 71 83
102. M.B. Upender, J.K. Habermann, L.M. McShane, E.L. Korn, J.C. Barrett, M.J. Difilippantonio, and T. Ried Chromosome transfer induced aneuploidy results in complex dysregulation of the cellular transcriptome in immortalized and cancer cells Cancer Res. 64 2004 6941 6949
103. T. Vacík, M. Ort, S. Gregorová, P. Strnad, R. Blatny, N. Conte, A. Bradley, J. Bures, and J. Forejt Segmental trisomy of chromosome 17: a mouse model of human aneuploidy syndromes Proc. Natl. Acad. Sci. USA 102 2005 4500 4505
104. T. Vavouri, J.I. Semple, R. Garcia-Verdugo, and B. Lehner Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity Cell 138 2009 198 208
105. R.A. Veitia Exploring the etiology of haploinsufficiency Bioessays 24 2002 175 184
106. B.A. Weaver, A.D. Silk, C. Montagna, P. Verdier-Pinard, and D.W. Cleveland Aneuploidy acts both oncogenically and as a tumor suppressor Cancer Cell 11 2007 25 36
107. J.W. Westra, S.E. Peterson, Y.C. Yung, T. Mutoh, S. Barral, and J. Chun Aneuploid mosaicism in the developing and adult cerebellar cortex J. Comp. Neurol. 507 2008 1944 1951
108. B.R. Williams, V.R. Prabhu, K.E. Hunter, C.M. Glazier, C.A. Whittaker, D.E. Housman, and A. Amon Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells Science 322 2008 703 709
109. S.R. Wolman, H. Gundacker, F.R. Appelbaum, M.L. Slovak Southwest Oncology Group Impact of trisomy 8 (+8) on clinical presentation, treatment response, and survival in acute myeloid leukemia: a Southwest Oncology Group study Blood 100 2002 29 35
110. Q. Yang, S.A. Rasmussen, and J.M. Friedman Mortality associated with Down's syndrome in the USA from 1983 to 1997: a population-based study Lancet 359 2002 1019 1025
111. Y. Yang, E.K. Chung, Y.L. Wu, S.L. Savelli, H.N. Nagaraja, B. Zhou, M. Hebert, K.N. Jones, Y. Shu, and K. Kitzmiller Gene copy-number variation and associated polymorphisms of complement component C4 in human systemic lupus erythematosus (SLE): low copy number is a risk factor for and high copy number is a protective factor against SLE susceptibility in European Americans Am. J. Hum. Genet. 80 2007 1037 1054
112. M.C. Yao, A.R. Kimmel, and M.A. Gorovsky A small number of cistrons for ribosomal RNA in the germinal nucleus of a eukaryote, Tetrahymena pyriformis Proc. Natl. Acad. Sci. USA 71 1974 3082 3086
113. A.H. Yona, Y.S. Manor, R.H. Herbst, G.H. Romano, A. Mitchell, M. Kupiec, Y. Pilpel, and O. Dahan Chromosomal duplication is a transient evolutionary solution to stress Proc. Natl. Acad. Sci. USA 2012 10.1073/pnas.1211150109 Published online November 29, 2012
114. F. Zhang, W. Gu, M.E. Hurles, and J.R. Lupski Copy number variation in human health, disease, and evolution Annu. Rev. Genomics Hum. Genet. 10 2009 451 481
115. Y. Zhong, Q.J. Wang, X. Li, Y. Yan, J.M. Backer, B.T. Chait, N. Heintz, and Z. Yue Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex Nat. Cell Biol. 11 2009 468 476
116. J. Zhu, N. Pavelka, W.D. Bradford, G. Rancati, and R. Li Karyotypic determinants of chromosome instability in aneuploid budding yeast PLoS Genet. 8 2012 e1002719