Alterations in DNA replication and histone levels promote histone gene amplification in Saccharomyces cerevisiae

Genetics

Volumn 184, Issue 4, 2010, Pages 985-997

  Libuda, Diana E ^a,b   Winston, Fred ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; HYDROXYUREA;

ARTICLE; CHROMATIN STRUCTURE; DNA REPLICATION; GENE AMPLIFICATION; GENE CONTROL; GENE DELETION; GENE MUTATION; GENETIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; CHROMATIN; CYTOLOGY; DRUG EFFECT; GENETICS; METABOLISM;

SACCHAROMYCES CEREVISIAE;

CHROMATIN; DNA REPLICATION; GENE AMPLIFICATION; GENE DELETION; HISTONES; HYDROXYUREA; SACCHAROMYCES CEREVISIAE;

EID: 77955880291     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.109.113662     Document Type: Article

References (87)

1. ALBERTSON, D. G., 2006 Gene amplification in cancer. Trends Genet. 22: 447-455.
2. ALVINO, G. M., D. COLLINGWOOD, J. M. MURPHY, J. DELROW, B. J. BREWER et al., 2007 Replication in hydroxyurea: it's a matter of time. Mol. Cell. Biol. 27: 6396-6406.
3. ARAKI, H., R. K. HAMATAKE, A. MORRISON, A. L. JOHNSON, L. H. JOHNSTON et al., 1991 Cloning DPB3, the gene encoding the third subunit of DNA polymerase II of Saccharomyces cerevisiae. Nucleic Acids Res. 19: 4867-4872. (Pubitemid 21912868)
4. ARGUESO, J. L., J. WESTMORELAND, P. A. MIECZKOWSKI, M. GAWEL, T. D. PETES et al., 2008 Double-strand breaks associated with repetitive DNA can reshape the genome. Proc. Natl. Acad. Sci. USA 105: 11845-11850.
5. ASHBY, M. N., S. Y. KUTSUNAI, S. ACKERMAN, A. TZAGOLOFF and P. A. EDWARDS, 1992 COQ2 is a candidate for the structural gene encoding para-hydroxybenzoate:polyprenyltransferase. J. Biol. Chem. 267: 4128-4136.
6. AUSUBEL, F. M., R. BRENT, R. E. KINGSTON, D. D. MOORE, J. G. SEIDMAN et al., 1991 Current Protocols in Molecular Biology. Greene Publishing Associates and Wiley-Interscience, New York.
7. AZVOLINSKY, A., S. DUNAWAY, J. Z. TORRES, J. B. BESSLER and V. A. ZAKIAN, 2006 The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes. Genes Dev. 20: 3104-3116.
8. AZVOLINSKY, A., P. G. GIRESI, J. D. LIEB and V. A. ZAKIAN, 2009 Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol. Cell 34: 722-734.
9. BAILIS, J. M., D. D. LUCHE, T. HUNTER and S. L. FORSBURG, 2008 MCM proteins interact with checkpoint and recombination proteins to promote S phase genome stability. Mol. Cell. Biol. 28: 1724-1738.
10. BRACHMANN, C. B., A. DAVIES, G. J. COST, E. CAPUTO, J. LI et al., 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.
11. BROWN, C. J., K. M. TODD and R. F. ROSENZWEIG, 1998 Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol. Biol. Evol. 15: 931-942.
12. CHA, R. S., and N. KLECKNER, 2002 ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297: 602-606.
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. (Pubitemid 23324813)
14. CLARK-ADAMS, C. D., D. NORRIS, M. A. OSLEY, J. S. FASSLER and F. WINSTON, 1988 Changes in histone gene dosage alter transcription in yeast. Genes Dev. 2: 150-159.
15. CLAYCOMB, J. M., M. BENASUTTI, G. BOSCO, D. D. FENGER and T. L. ORR-WEAVER, 2004 Gene amplification as a developmental strategy: isolation of two developmental amplicons in Drosophila. Dev. Cell 6: 145-155.
16. CROSS, S. L., and M. M. SMITH, 1988 Comparison of the structure and cell cycle expression of mRNAs encoded by two histone H3-H4 loci in Saccharomyces cerevisiae. Mol. Cell. Biol. 8: 945-954.
17. DONALDSON, A. D., M. K. RAGHURAMAN, K. L. FRIEDMAN, F. R. CROSS, B. J. BREWER et al., 1998 CLB5-dependent activation of late replication origins in S. cerevisiae. Mol. Cell 2: 173-182.
18. DUA, R., D. L. LEVY and J. L. CAMPBELL, 1998 Role of the putative zinc finger domain of Saccharomyces cerevisiae DNA polymerase epsilon in DNA replication and the S/M checkpoint pathway. J. Biol. Chem. 273: 30046-30055.
19. DUNHAM, M. J., H. BADRANE, T. FEREA, J. ADAMS, P. O. BROWN et al., 2002 Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99: 16144-16149.
20. ELLEDGE, S. J., and R. W. DAVIS, 1990 Two genes differentially regulated in the cell cycle and by DNA-damaging agents encode alternative regulatory subunits of ribonucleotide reductase. Genes Dev. 4: 740-751.
21. EPSTEIN, C. B., and F. R. CROSS, 1992 CLB5: a novel B cyclin from budding yeast with a role in S phase. Genes Dev. 6: 1695-1706.
22. FENG, W., D. COLLINGWOOD, M. E. BOECK, L. A. FOX, G. M. ALVINO et al., 2006 Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nat. Cell Biol. 8: 148-155.
23. FRIDLYAND, J., A. M. SNIJDERS, B. YLSTRA, H. LI, A. OLSHEN et al., 2006 Breast tumor copy number aberration phenotypes and genomic instability. BMC Cancer 6: 96.
24. GASCH, A. P., M. HUANG, S. METZNER, D. BOTSTEIN, S. J. ELLEDGE et al., 2001 Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol. Biol. Cell 12: 2987-3003.
25. 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.
26. GRAUX, C., J. COOLS, C. MELOTTE, H. QUENTMEIER, A. FERRANDO et al., 2004 Fusion of NUP214 to ABL1 on amplified episomes in T-cell acute lymphoblastic leukemia. Nat. Genet. 36: 1084-1089.
27. GRESHAM, D., M. M. DESAI, C. M. TUCKER, H. T. JENQ, D. A. PAI et al., 2008 The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet. 4: e1000303.
28. GUNJAN, A., and A. VERREAULT, 2003 A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 115: 537-549.
29. GUNJAN, A., J. PAIK and A. VERREAULT, 2005 Regulation of histone synthesis and nucleosome assembly. Biochimie 87: 625-635.
30. HAHN, P. J., 1993 Molecular biology of double-minute chromosomes. Bioessays 15: 477-484.
31. HASTINGS, P. J., A. SLACK, J. F. PETROSINO and S. M. ROSENBERG, 2004 Adaptive amplification and point mutation are independent mechanisms: evidence for various stress-inducible mutation mechanisms. PLoS Biol. 2: e399.
32. HEREFORD, L. M., M. A. OSLEY, T. R. LUDWIG, II and C. S. MCLAUGHLIN, 1981 Cell-cycle regulation of yeast histone mRNA. Cell 24: 367-375.
33. HIRSCHHORN, J. N., S. A. BROWN, C. D. CLARK and F. WINSTON, 1992 Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 6: 2288-2298.
34. HIRSCHHORN, J. N., A. L. BORTVIN, S. L. RICUPERO-HOVASSE and F. WINSTON, 1995 A new class of histone H2A mutations in Saccharomyces cerevisiae causes specific transcriptional defects in vivo. Mol. Cell. Biol. 15: 1999-2009.
35. 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.
36. IIDA, T., and H. ARAKI, 2004 Noncompetitive counteractions of DNA polymerase epsilon and ISW2/yCHRAC for epigenetic inheritance of telomere position effect in Saccharomyces cerevisiae. Mol. Cell. Biol. 24: 217-227.
37. INFANTE, J. J., K. M. DOMBEK, L. REBORDINOS, J. M. CANTORAL and E. T. YOUNG, 2003 Genome-wide amplifications caused by chromosomal rearrangements play a major role in the adaptive evolution of natural yeast. Genetics 165: 1745-1759.
38. IVESSA, A. S., J. Q. ZHOU and V. A. ZAKIAN, 2000 The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell 100: 479-489.
39. IVESSA, A. S., J. Q. ZHOU, V. P. SCHULZ, E. K. MONSON and V. A. ZAKIAN, 2002 Saccharomyces Rrm3p, a 5′ to 3′ DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 16: 1383-1396.
40. KOLODRUBETZ, D., M. C. RYKOWSKI and M. GRUNSTEIN, 1982 Histone H2A subtypes associate interchangeably in vivo with histone H2B subtypes. Proc. Natl. Acad. Sci. USA 79: 7814-7818.
41. KOSZUL, R., S. CABURET, B. DUJON and G. FISCHER, 2004 Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments. EMBO J. 23: 234-243.
42. KUGELBERG, E., E. KOFOID, A. B. REAMS, D. I. ANDERSSON and J. R. ROTH, 2006 Multiple pathways of selected gene amplification during adaptive mutation. Proc. Natl. Acad. Sci. USA 103: 17319-17324.
43. KUHNE, C., and P. LINDER, 1993 A new pair of B-type cyclins from Saccharomyces cerevisiae that function early in the cell cycle. EMBO J. 12: 3437-3447.
44. LAMBERT, S., and A. M. CARR, 2005 Checkpoint responses to replication fork barriers. Biochimie 87: 591-602.
45. LAMBERT, S., A. WATSON, D. M. SHEEDY, B. MARTIN and A. M. CARR, 2005 Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell 121: 689-702.
46. LEMOINE, F. J., N. P. DEGTYAREVA, K. LOBACHEV and T. D. PETES, 2005 Chromosomal translocations in yeast induced by low levels of DNA polymerase: a model for chromosome fragile sites. Cell 120: 587-598.
47. LIBUDA, D. E., and F. WINSTON, 2006 Amplification of histone genes by circular chromosome formation in Saccharomyces cerevisiae. Nature 443: 1003-1007.
48. LIEBMAN, S., P. SHALIT and S. PICOLOGLOU, 1981 Ty elements are involved in the formation of deletions in DEL1 strains of Saccharomyces cerevisiae. Cell 26: 401-409.
49. LYCAN, D. E., M. A. OSLEY and L. M. HEREFORD, 1987 Role of transcriptional and posttranscriptional regulation in expression of histone genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 7: 614-621.
50. MANN, R. K., and M. GRUNSTEIN, 1992 Histone H3 N-terminal mutations allow hyperactivation of the yeast GAL1 gene in vivo. EMBO J. 11: 3297-3306.
51. MCCARROLL, S. A., and D. M. ALTSHULER, 2007 Copy-number variation and association studies of human disease. Nat. Genet. 39: S37-S42.
52. MCCONNELL, A. D., M. E. GELBART and T. TSUKIYAMA, 2004 Histone fold protein Dls1p is required for Isw2-dependent chromatin remodeling in vivo. Mol. Cell. Biol. 24: 2605-2613.
53. MCCUNE, H. J., L. S. DANIELSON, G. M. ALVINO, D. COLLINGWOOD, J. J. DELROW et al., 2008 The temporal program of chromosome replication: genomewide replication in clb5Δ Saccharomyces cerevisiae. Genetics 180: 1833-1847.
54. MEEKS-WAGNER, D., and L. H. HARTWELL, 1986 Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell 44: 43-52.
55. MIECZKOWSKI, P. A., F. J. LEMOINE and T. D. PETES, 2006 Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair (Amst.) 5: 1010-1020.
56. NORRIS, D., and M. A. OSLEY, 1987 The two gene pairs encoding H2A and H2B play different roles in the Saccharomyces cerevisiae life cycle. Mol. Cell. Biol. 7: 3473-3481.
57. NORRIS, D., B. DUNN and M. A. OSLEY, 1988 The effect of histone gene deletions on chromatin structure in Saccharomyces cerevisiae. Science 242: 759-761.
58. OHYA, T., S. MAKI, Y. KAWASAKI and A. SUGINO, 2000 Structure and function of the fourth subunit (Dpb4p) of DNA polymerase epsilon in Saccharomyces cerevisiae. Nucleic Acids Res. 28: 3846-3852.
59. ORR, W., K. KOMITOPOULOU and F. C. KAFATOS, 1984 Mutants suppressing in trans chorion gene amplification in Drosophila. Proc. Natl. Acad. Sci. USA 81: 3773-3777.
60. OSLEY, M. A., 1991 The regulation of histone synthesis in the cell cycle. Annu. Rev. Biochem. 60: 827-861.
61. OSLEY, M. A., and L. HEREFORD, 1982 Identification of a sequence responsible for periodic synthesis of yeast histone 2A mRNA. Proc. Natl. Acad. Sci. USA 79: 7689-7693.
62. PARKET, A., and M. KUPIEC, 1992 Ectopic recombination between Ty elements in Saccharomyces cerevisiae is not induced by DNA damage. Mol. Cell. Biol. 12: 4441-4448.
63. PAYEN, C., R. KOSZUL, B. DUJON and G. FISCHER, 2008 Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms. PLoS Genet. 4: e1000175.
64. PRADO, F., and A. AGUILERA, 2005 Partial depletion of histone H4 increases homologous recombination-mediated genetic instability. Mol. Cell. Biol. 25: 1526-1536.
65. RACHIDI, N., P. BARRE and B. BLONDIN, 1999 Multiple Ty-mediated chromosomal translocations lead to karyotype changes in a wine strain of Saccharomyces cerevisiae. Mol. Gen. Genet. 261: 841-850.
66. ROSE, M. D., F. WINSTON and P. HIETER, 1990 Methods in Yeast Genetics: A Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
67. ROSENBERG, S. M., 2001 Evolving responsively: adaptive mutation. Nat. Rev. Genet. 2: 504-515.
68. ROTH, J. R., E. KUGELBERG, A. B. REAMS, E. KOFOID and D. I. ANDERSSON, 2006 Origin of mutations under selection: the adaptive mutation controversy. Annu. Rev. Microbiol. 60: 477-501.
69. RYKOWSKI, M. C., J. W. WALLIS, J. CHOE and M. GRUNSTEIN, 1981 Histone H2B subtypes are dispensable during the yeast cell cycle. Cell 25: 477-487.
70. SCHACHERER, J., Y. TOURRETTE, J. L. SOUCIET, S. POTIER and J. DE MONTIGNY, 2004 Recovery of a function involving gene duplication by retroposition in Saccharomyces cerevisiae. Genome Res. 14: 1291-1297.
71. SCHWOB, E., and K. NASMYTH, 1993 CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev. 7: 1160-1175.
72. SELMECKI, A., A. FORCHE and J. BERMAN, 2006 Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313: 367-370.
73. SINGH, R. K., M. H. KABBAJ, J. PAIK and A. GUNJAN, 2009 Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat. Cell Biol. 11: 925-933.
74. SMITH, M. M., and V. B. STIRLING, 1988 Histone H3 and H4 gene deletions in Saccharomyces cerevisiae. J. Cell Biol. 106: 557-566.
75. SPRADLING, A. C., 1981 The organization and amplification of two chromosomal domains containing Drosophila chorion genes. Cell 27: 193-201.
76. STARK, G. R., and G. M. WAHL, 1984 Gene amplification. Annu. Rev. Biochem. 53: 447-491.
77. SU, C., G. GAO, S. SCHNEIDER, C. HELT, C. WEISS et al., 2004 DNA damage induces downregulation of histone gene expression through the G1 checkpoint pathway. EMBO J. 23: 1133-1143.
78. SWANSON, M. S., E. A. MALONE and F. WINSTON, 1991 SPT5, an essential gene important for normal transcription in Saccharomyces cerevisiae, encodes an acidic nuclear protein with a carboxyterminal repeat. Mol. Cell. Biol. 11: 4286.
79. TOWER, J., 2004 Developmental gene amplification and origin regulation. Annu. Rev. Genet. 38: 273-304.
80. TSUBOTA, T., R. TAJIMA, K. ODE, H. KUBOTA, N. FUKUHARA et al., 2006 Double-stranded DNA binding, an unusual property of DNA polymerase epsilon, promotes epigenetic silencing in Saccharomyces cerevisiae. J. Biol. Chem. 281: 32898-32908.
81. VERNON, M., K. LOBACHEV and T. D. PETES, 2008 High rates of "unselected" aneuploidy and chromosome rearrangements in tel1 mec1 haploid yeast strains. Genetics 179: 237-247.
82. VOGT, N., S. H. LEFEVRE, F. APIOU, A. M. DUTRILLAUX, A. COR et al., 2004 Molecular structure of double-minute chromosomes bearing amplified copies of the epidermal growth factor receptor gene in gliomas. Proc. Natl. Acad. Sci. USA 101: 11368-11373.
83. WINSTON, F., C. DOLLARD and S. L. RICUPERO-HOVASSE, 1995 Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11: 53-55.
84. WYRICK, J. J., F. C. HOLSTEGE, E. G. JENNINGS, H. C. CAUSTON, D. SHORE et al., 1999 Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature 402: 418-421.
85. ZEYL, C., 2004 Capturing the adaptive mutation in yeast. Res. Microbiol. 155: 217-223.
86. ZHAO, J., 2004 Coordination of DNA synthesis and histone gene expression during normal cell cycle progression and after DNA damage. Cell Cycle 3: 695-697.
87. ZHAO, X., E. G. MULLER and R. ROTHSTEIN, 1998 A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 2: 329-340.