One-hit wonders of genomic instability

Springer Science and Business Media LLC - Tập 5 - Trang 1-12 - 2010
Alexander V Strunnikov1
1Laboratory of Immunopathology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, USA

Tóm tắt

Recent data show that cells from many cancers exhibit massive chromosome instability. The traditional view is that the gradual accumulation of mutations in genes involved in transcriptional regulation and cell cycle controls results in tumor development. This, however, does not exclude the possibility that some mutations could be more potent than others in destabilizing the genome by targeting both chromosomal integrity and corresponding checkpoint mechanisms simultaneously. Three such examples of "single-hit" lesions potentially leading to heritable genome destabilization are discussed. They include: failure to release sister chromatid cohesion due to the incomplete proteolytic cleavage of cohesin; massive merotelic kinetochore misattachments upon condensin depletion; and chromosome under-replication. In all three cases, cells fail to detect potential chromosomal bridges before anaphase entry, indicating that there is a basic cell cycle requirement to maintain a degree of sister chromatid bridging that is not recognizable as chromosomal damage.

Tài liệu tham khảo

Santarius T, Shipley J, Brewer D, Stratton MR, Cooper CS: A census of amplified and overexpressed human cancer genes. Nat Rev Cancer 2010,10(1):59–64. 10.1038/nrc2771

Pleasance ED, Cheetham RK, Stephens PJ, McBride DJ, Humphray SJ, Greenman CD, Varela I, Lin ML, Ordonez GR, Bignell GR, et al.: A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 2010,463(7278):191–196. 10.1038/nature08658

Stephens PJ, McBride DJ, Lin ML, Varela I, Pleasance ED, Simpson JT, Stebbings LA, Leroy C, Edkins S, Mudie LJ, et al.: Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 2009,462(7276):1005–1010. 10.1038/nature08645

Campbell PJ, Stephens PJ, Pleasance ED, O'Meara S, Li H, Santarius T, Stebbings LA, Leroy C, Edkins S, Hardy C, et al.: Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat Genet 2008,40(6):722–729. 10.1038/ng.128

Lengauer C, Kinzler KW, Vogelstein B: Genetic instability in colorectal cancers. Nature 1997,386(6625):623–627. 10.1038/386623a0

Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, et al.: Finding the missing heritability of complex diseases. Nature 2009,461(7265):747–753. 10.1038/nature08494

Hannan AJ: Tandem repeat polymorphisms: modulators of disease susceptibility and candidates for 'missing heritability'. Trends Genet 2010,26(2):59–65. 10.1016/j.tig.2009.11.008

Segditsas S, Rowan AJ, Howarth K, Jones A, Leedham S, Wright NA, Gorman P, Chambers W, Domingo E, Roylance RR, et al.: APC and the three-hit hypothesis. Oncogene 2009,28(1):146–155. 10.1038/onc.2008.361

Soutoglou E, Dorn JF, Sengupta K, Jasin M, Nussenzweig A, Ried T, Danuser G, Misteli T: Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 2007,9(6):675–682. 10.1038/ncb1591

Michaelis C, Ciosk R, Nasmyth K: Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 1997,91(1):35–45. 10.1016/S0092-8674(01)80007-6

Nasmyth K, Haering CH: Cohesin: its roles and mechanisms. Annu Rev Genet 2009, 43: 525–558. 10.1146/annurev-genet-102108-134233

Canudas S, Smith S: Differential regulation of telomere and centromere cohesion by the Scc3 homologues SA1 and SA2, respectively, in human cells. J Cell Biol 2009,187(2):165–173. 10.1083/jcb.200903096

Pauli A, Althoff F, Oliveira RA, Heidmann S, Schuldiner O, Lehner CF, Dickson BJ, Nasmyth K: Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons. Dev Cell 2008,14(2):239–251. 10.1016/j.devcel.2007.12.009

Schuldiner O, Berdnik D, Levy JM, Wu JS, Luginbuhl D, Gontang AC, Luo L: piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev Cell 2008,14(2):227–238. 10.1016/j.devcel.2007.11.001

Oliveira RA, Hamilton RS, Pauli A, Davis I, Nasmyth K: Cohesin cleavage and Cdk inhibition trigger formation of daughter nuclei. Nat Cell Biol 2010,12(2):185–192. 10.1038/ncb2018

Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K: Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 2000,103(3):375–386. 10.1016/S0092-8674(00)00130-6

Uzawa S, Samejima I, Hirano T, Tanaka K, Yanagida M: The fission teast cut1+ gene regulates spindle pole doby duplication and has homology to the budding yeast ESP1 gene. Cell 1990, 62: 913–925. 10.1016/0092-8674(90)90266-H

Kumada K, Yao R, Kawaguchi T, Karasawa M, Hoshikawa Y, Ichikawa K, Sugitani Y, Imoto I, Inazawa J, Sugawara M, et al.: The selective continued linkage of centromeres from mitosis to interphase in the absence of mammalian separase. J Cell Biol 2006,172(6):835–846. 10.1083/jcb.200511126

Lu Y, Cross F: Mitotic exit in the absence of separase activity. Mol Biol Cell 2009,20(5):1576–1591. 10.1091/mbc.E08-10-1042

Jager H, Herzig A, Lehner CF, Heidmann S: Drosophila separase is required for sister chromatid separation and binds to PIM and THR. Genes Dev 2001,15(19):2572–2584. 10.1101/gad.207301

Wirth KG, Wutz G, Kudo NR, Desdouets C, Zetterberg A, Taghybeeglu S, Seznec J, Ducos GM, Ricci R, Firnberg N, et al.: Separase: a universal trigger for sister chromatid disjunction but not chromosome cycle progression. J Cell Biol 2006,172(6):847–860. 10.1083/jcb.200506119

Hauf S, Waizenegger IC, Peters JM: Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 2001,293(5533):1320–1323. 10.1126/science.1061376

Shaw CJ, Lupski JR: Implications of human genome architecture for rearrangement-based disorders: the genomic basis of disease. Hum Mol Genet 2004,13(Spec No 1):R57–64. 10.1093/hmg/ddh073

Hirota T, Gerlich D, Koch B, Ellenberg J, Peters JM: Distinct functions of condensin I and II in mitotic chromosome assembly. J Cell Sci 2004,117(Pt 26):6435–6445. 10.1242/jcs.01604

Palframan WJ, Meehl JB, Jaspersen SL, Winey M, Murray AW: Anaphase inactivation of the spindle checkpoint. Science 2006,313(5787):680–684. 10.1126/science.1127205

Mannini L, Liu J, Krantz ID, Musio A: Spectrum and consequences of SMC1A mutations: the unexpected involvement of a core component of cohesin in human disease. Hum Mutat 2010,31(1):5–10. 10.1002/humu.21129

Revenkova E, Focarelli ML, Susani L, Paulis M, Bassi MT, Mannini L, Frattini A, Delia D, Krantz I, Vezzoni P, et al.: Cornelia de Lange syndrome mutations in SMC1A or SMC3 affect binding to DNA. Hum Mol Genet 2009,18(3):418–427. 10.1093/hmg/ddn369

Barber TD, McManus K, Yuen KW, Reis M, Parmigiani G, Shen D, Barrett I, Nouhi Y, Spencer F, Markowitz S, et al.: Chromatid cohesion defects may underlie chromosome instability in human colorectal cancers. Proc Natl Acad Sci USA 2008,105(9):3443–3448. 10.1073/pnas.0712384105

Zhang N, Ge G, Meyer R, Sethi S, Basu D, Pradhan S, Zhao YJ, Li XN, Cai WW, El-Naggar AK, et al.: Overexpression of Separase induces aneuploidy and mammary tumorigenesis. Proc Natl Acad Sci USA 2008,105(35):13033–13038. 10.1073/pnas.0801610105

Shepard JL, Amatruda JF, Finkelstein D, Ziai J, Finley KR, Stern HM, Chiang K, Hersey C, Barut B, Freeman JL, et al.: A mutation in separase causes genome instability and increased susceptibility to epithelial cancer. Genes Dev 2007,21(1):55–59. 10.1101/gad.1470407

Kimura K, Hirano T: ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell 1997,90(4):625–634. 10.1016/S0092-8674(00)80524-3

Freeman L, Aragon-Alcaide L, Strunnikov A: The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J Cell Biol 2000,149(4):811–824. 10.1083/jcb.149.4.811

Yu HG, Koshland D: Chromosome morphogenesis: condensin-dependent cohesin removal during meiosis. Cell 2005,123(3):397–407. 10.1016/j.cell.2005.09.014

Onn I, Aono N, Hirano M, Hirano T: Reconstitution and subunit geometry of human condensin complexes. Embo J 2007,26(4):1024–1034. 10.1038/sj.emboj.7601562

Takemoto A, Maeshima K, Ikehara T, Yamaguchi K, Murayama A, Imamura S, Imamoto N, Yokoyama S, Hirano T, Watanabe Y, et al.: The chromosomal association of condensin II is regulated by a noncatalytic function of PP2A. Nat Struct Mol Biol 2009,16(12):1302–1308. 10.1038/nsmb.1708

Ono T, Fang Y, Spector DL, Hirano T: Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 2004,15(7):3296–3308. 10.1091/mbc.E04-03-0242

Takemoto A, Kimura K, Yanagisawa J, Yokoyama S, Hanaoka F: Negative regulation of condensin I by CK2-mediated phosphorylation. Embo J 2006,25(22):5339–5348. 10.1038/sj.emboj.7601394

Kimura K, Rybenkov VV, Crisona NJ, Hirano T, Cozzarelli NR: 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 1999,98(2):239–248. 10.1016/S0092-8674(00)81018-1

Mora-Bermudez F, Gerlich D, Ellenberg J: Maximal chromosome compaction occurs by axial shortening in anaphase and depends on Aurora kinase. Nat Cell Biol 2007,9(7):822–831. 10.1038/ncb1606

Hagstrom KA, Holmes VF, Cozzarelli NR, Meyer BJ: C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev 2002,16(6):729–742. 10.1101/gad.968302

Oliveira RA, Coelho PA, Sunkel CE: The condensin I subunit Barren/CAP-H is essential for the structural integrity of centromeric heterochromatin during mitosis. Mol Cell Biol 2005,25(20):8971–8984. 10.1128/MCB.25.20.8971-8984.2005

Yong-Gonzalez V, Wang BD, Butylin P, Ouspenski I, Strunnikov A: Condensin function at centromere chromatin facilitates proper kinetochore tension and ensures correct mitotic segregation of sister chromatids. Genes Cells 2007,12(9):1075–1090. 10.1111/j.1365-2443.2007.01109.x

Ribeiro SA, Gatlin JC, Dong Y, Joglekar A, Cameron L, Hudson DF, Farr CJ, McEwen BF, Salmon ED, Earnshaw WC, et al.: Condensin Regulates the Stiffness of Vertebrate Centromeres. Mol Biol Cell 2009,20(9):2371–2380. 10.1091/mbc.E08-11-1127

Uchida KS, Takagaki K, Kumada K, Hirayama Y, Noda T, Hirota T: Kinetochore stretching inactivates the spindle assembly checkpoint. J Cell Biol 2009,184(3):383–390. 10.1083/jcb.200811028

Bazett-Jones DP, Kimura K, Hirano T: Efficient supercoiling of DNA by a single condensin complex as revealed by electron spectroscopic imaging. Mol Cell 2002,9(6):1183–1190. 10.1016/S1097-2765(02)00546-4

Furuyama T, Henikoff S: Centromeric nucleosomes induce positive DNA supercoils. Cell 2009,138(1):104–113. 10.1016/j.cell.2009.04.049

Vagnarelli P, Hudson DF, Ribeiro SA, Trinkle-Mulcahy L, Spence JM, Lai F, Farr CJ, Lamond AI, Earnshaw WC: Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat Cell Biol 2006,8(10):1133–1142. 10.1038/ncb1475

Moore LL, Stanvitch G, Roth MB, Rosen D: HCP-4/CENP-C promotes the prophase timing of centromere resolution by enabling the centromere association of HCP-6 in Caenorhabditis elegans. Mol Cell Biol 2005,25(7):2583–2592. 10.1128/MCB.25.7.2583-2592.2005

Salmon ED, Cimini D, Cameron LA, DeLuca JG: Merotelic kinetochores in mammalian tissue cells. Philos Trans R Soc Lond B Biol Sci 2005,360(1455):553–568. 10.1098/rstb.2004.1610

Liu D, Vader G, Vromans MJ, Lampson MA, Lens SM: Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 2009,323(5919):1350–1353. 10.1126/science.1167000

Lilly MA, Duronio RJ: New insights into cell cycle control from the Drosophila endocycle. Oncogene 2005,24(17):2765–2775. 10.1038/sj.onc.1208610

Hong A, Narbonne-Reveau K, Riesgo-Escovar J, Fu H, Aladjem MI, Lilly MA: The cyclin-dependent kinase inhibitor Dacapo promotes replication licensing during Drosophila endocycles. Embo J 2007,26(8):2071–2082. 10.1038/sj.emboj.7601648

Mehrotra S, Maqbool SB, Kolpakas A, Murnen K, Calvi BR: Endocycling cells do not apoptose in response to DNA rereplication genotoxic stress. Genes Dev 2008,22(22):3158–3171. 10.1101/gad.1710208

McCleland ML, Shermoen AW, O'Farrell PH: DNA replication times the cell cycle and contributes to the mid-blastula transition in Drosophila embryos. J Cell Biol 2009,187(1):7–14. 10.1083/jcb.200906191

Zhang J, Song YH, Brannigan BW, Wahrer DC, Schiripo TA, Harris PL, Haserlat SM, Ulkus LE, Shannon KM, Garber JE, et al.: Prevalence and functional analysis of sequence variants in the ATR checkpoint mediator Claspin. Mol Cancer Res 2009,7(9):1510–1516. 10.1158/1541-7786.MCR-09-0033

Navas TA, Zhou Z, Elledge SJ: DNA polymerase epsilon links the DNA replication machinery to the S phase checkpoint. Cell 1995,80(1):29–39. 10.1016/0092-8674(95)90448-4

D'Urso G, Nurse P: Schizosaccharomyces pombe cdc20+ encodes DNA polymerase epsilon and is required for chromosomal replication but not for the S phase checkpoint. Proc Natl Acad Sci USA 1997,94(23):12491–12496. 10.1073/pnas.94.23.12491

Early A, Drury LS, Diffley JF: Mechanisms involved in regulating DNA replication origins during the cell cycle and in response to DNA damage. Philos Trans R Soc Lond B Biol Sci 2004,359(1441):31–38. 10.1098/rstb.2003.1362

Lengronne A, Schwob E: The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G(1). Mol Cell 2002,9(5):1067–1078. 10.1016/S1097-2765(02)00513-0

Clifford DM, Chen CT, Roberts RH, Feoktistova A, Wolfe BA, Chen JS, McCollum D, Gould KL: The role of Cdc14 phosphatases in the control of cell division. Biochem Soc Trans 2008,36(Pt 3):436–438. 10.1042/BST0360436

Rock JM, Amon A: The FEAR network. Curr Biol 2009,19(23):R1063–1068. 10.1016/j.cub.2009.10.002

Khmelinskii A, Roostalu J, Roque H, Antony C, Schiebel E: Phosphorylation-dependent protein interactions at the spindle midzone mediate cell cycle regulation of spindle elongation. Dev Cell 2009,17(2):244–256. 10.1016/j.devcel.2009.06.011

Bassermann F, Frescas D, Guardavaccaro D, Busino L, Peschiaroli A, Pagano M: The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 2008,134(2):256–267. 10.1016/j.cell.2008.05.043

Dulev S, de Renty C, Mehta R, Minkov I, Schwob E, Strunnikov A: Essential global role of CDC14 in DNA synthesis revealed by chromosome underreplication unrecognized by checkpoints in cdc14 mutants. Proc Natl Acad Sci USA 2009,106(34):14466–14471. 10.1073/pnas.0900190106

Geymonat M, Spanos A, Wells GP, Smerdon SJ, Sedgwick SG: Clb6/Cdc28 and Cdc14 regulate phosphorylation status and cellular localization of Swi6. Mol Cell Biol 2004,24(6):2277–2285. 10.1128/MCB.24.6.2277-2285.2004

Bloom J, Cross FR: Novel role for Cdc14 sequestration: Cdc14 dephosphorylates factors that promote DNA replication. Mol Cell Biol 2007,27(3):842–853. 10.1128/MCB.01069-06

Tomson BN, D'Amours D, Adamson BS, Aragon L, Amon A: Ribosomal DNA transcription-dependent processes interfere with chromosome segregation. Mol Cell Biol 2006,26(16):6239–6247. 10.1128/MCB.00693-06

Clemente-Blanco A, Mayan-Santos M, Schneider DA, Machin F, Jarmuz A, Tschochner H, Aragon L: Cdc14 inhibits transcription by RNA polymerase I during anaphase. Nature 2009,458(7235):219–222. 10.1038/nature07652

Wang BD, Eyre D, Basrai M, Lichten M, Strunnikov A: Condensin binding at distinct and specific chromosomal sites in the Saccharomyces cerevisiae genome. Mol Cell Biol 2005,25(16):7216–7225. 10.1128/MCB.25.16.7216-7225.2005

Ganier O, Mechali M: New cell or new cycle? Genes Dev 2008,22(21):2908–2913. 10.1101/gad.1740808

Ishida T, Fujiwara S, Miura K, Stacey N, Yoshimura M, Schneider K, Adachi S, Minamisawa K, Umeda M, Sugimoto K: SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 2009,21(8):2284–2297. 10.1105/tpc.109.068072

Zielke N, Querings S, Rottig C, Lehner C, Sprenger F: The anaphase-promoting complex/cyclosome (APC/C) is required for rereplication control in endoreplication cycles. Genes Dev 2008,22(12):1690–1703. 10.1101/gad.469108

McCarroll RM, Fangman WL: Time of replication of yeast centromeres and telomeres. Cell 1988,54(4):505–513. 10.1016/0092-8674(88)90072-4

Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, Conway A, Lockhart DJ, Davis RW, Brewer BJ, Fangman WL: Replication dynamics of the yeast genome. Science 2001,294(5540):115–121. 10.1126/science.294.5540.115

Feng W, Bachant J, Collingwood D, Raghuraman MK, Brewer BJ: Centromere replication timing determines different forms of genomic instability in Saccharomyces cerevisiae checkpoint mutants during replication stress. Genetics 2009,183(4):1249–1260. 10.1534/genetics.109.107508

Mendoza M, Norden C, Durrer K, Rauter H, Uhlmann F, Barral Y: A mechanism for chromosome segregation sensing by the NoCut checkpoint. Nat Cell Biol 2009,11(4):477–483. 10.1038/ncb1855