Histone deacetylase inhibitors and genomic instability

Cancer Letters

Volumn 274, Issue 2, 2009, Pages 169-176

  Eot Houllier, Grégory ^a   Fulcrand, Géraldine ^b   Magnaghi Jaulin, Laura ^b   Jaulin, Christian ^b  

^a CNRS   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Chromosome segregation; DNA damage and repair; Genomic instability; Histone deacetylase inhibitors

Indexed keywords

DNA; HISTONE DEACETYLASE INHIBITOR; REACTIVE OXYGEN METABOLITE;

CHROMOSOME; DNA DAMAGE; DNA REPAIR; GENOMIC INSTABILITY; GENOTOXICITY; MITOSIS; OXIDATIVE STRESS; PRIORITY JOURNAL; SHORT SURVEY;

EID: 58149310725     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2008.06.005     Document Type: Review

References (110)

1. Phillips D.M. The presence of acetyl groups of histones. Biochem. J. 87 (1963) 258-263
2. Allfrey V.G., Faulkner R., and Mirsky A.E. Acetylation and methylation of histones and their possible role in regulation of RNA synthesis. Proc. Natl. Acad. Sci. USA 51 (1964) 786-794
3. Brownell J.E., Zhou J., Ranalli T., Kobayashi R., Edmondson D.G., Roth S.Y., and Allis C.D. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84 (1996) 843-851
4. Brownell J.E., and Allis C.D. An activity gel assay detects a single, catalytically active histone acetyltransferase subunit in Tetrahymena macronuclei. Proc. Natl. Acad. Sci. USA 92 (1995) 6364-6368
5. Bannister A.J., and Kouzarides T. The CBP co-activator is a histone acetyltransferase. Nature 384 (1996) 641-643
6. Ogryzko V.V., Schiltz R.L., Russanova V., Howard B.H., and Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 87 (1996) 953-959
7. Rundlett S.E., Carmen A.A., Kobayashi R., Bavykin S., Turner B.M., and Grunstein M. HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc. Natl. Acad. Sci. USA 93 (1996) 14503-14508
8. Taunton J., Hassig C.A., and Schreiber S.L. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272 (1996) 408-411
9. Yang W.M., Inouye C., Zeng Y., Bearss D., and Seto E. Transcriptional repression by YY1 is mediated by interaction with a mammalian homolog of the yeast global regulator RPD3. Proc. Natl. Acad. Sci. USA 93 (1996) 12845-12850
10. Ehrenhofer-Murray A.E. Chromatin dynamics at DNA replication, transcription and repair. Eur. J. Biochem. 271 (2004) 2335-2349
11. Bhaumik S.R., Smith E., and Shilatifard A. Covalent modifications of histones during development and disease pathogenesis. Nat. Struct. Mol. Biol. 14 (2007) 1008-1016
12. Kouzarides T. Chromatin modifications and their function. Cell 128 (2007) 693-705
13. Li B., Carey M., and Workman J.L. The role of chromatin during transcription. Cell 128 (2007) 707-719
14. Yang X.J. Lysine acetylation and the bromodomain: a new partnership for signaling. Bioessays 26 (2004) 1076-1087
15. Frye R.A. Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem. Biophys. Res. Commun. 273 (2000) 793-798
16. Yang X.J. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 32 (2004) 959-976
17. Glozak M.A., Sengupta N., Zhang X., and Seto E. Acetylation and deacetylation of non-histone proteins. Gene 363 (2005) 15-23
18. Batta K., Das C., Gadad S., Shandilya J., and Kundu T.K. Reversible acetylation of non histone proteins: role in cellular function and disease. Subcell. Biochem. 41 (2007) 193-212
19. Thiagalingam S., Cheng K.H., Lee H.J., Mineva N., Thiagalingam A., and Ponte J.F. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann. N. Y. Acad. Sci. 983 (2003) 84-100
20. Denu J.M. The Sir 2 family of protein deacetylases. Curr. Opin. Chem. Biol. 9 (2005) 431-440
21. Gregoretti I.V., Lee Y.M., and Goodson H.V. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 338 (2004) 17-31
22. Dokmanovic M., Clarke C., and Marks P.A. Histone deacetylase inhibitors: overview and perspectives. Mol. Cancer Res. 5 (2007) 981-989
23. Neugebauer R.C., Sippl W., and Jung M. Inhibitors of NAD+ dependent histone deacetylases (sirtuins). Curr. Pharm. Des. 14 (2008) 562-573
24. Bolden J.E., Peart M.J., and Johnstone R.W. Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov. 5 (2006) 769-784
25. Glozak M.A., and Seto E. Histone deacetylases and cancer. Oncogene 26 (2007) 5420-5432
26. Rasheed W., Bishton M., Johnstone R.W., and Prince H.M. Histone deacetylase inhibitors in lymphoma and solid malignancies. Expert Rev. Anticancer Ther. 8 (2008) 413-432
27. Rasheed W.K., Johnstone R.W., and Prince H.M. Histone deacetylase inhibitors in cancer therapy. Expert Opin. Investig. Drugs 16 (2007) 659-678
28. Mann B.S., Johnson J.R., Cohen M.H., Justice R., and Pazdur R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 12 (2007) 1247-1252
29. Rocchi P., Tonelli R., Camerin C., Purgato S., Fronza R., Bianucci F., Guerra F., Pession A., and Ferreri A.M. p21Waf1/Cip1 is a common target induced by short-chain fatty acid HDAC inhibitors (valproic acid, tributyrin and sodium butyrate) in neuroblastoma cells. Oncol. Rep. 13 (2005) 1139-1144
30. Richon V.M., Sandhoff T.W., Rifkind R.A., and Marks P.A. Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc. Natl. Acad. Sci. USA 97 (2000) 10014-10019
31. Kramer O.H., Zhu P., Ostendorff H.P., Golebiewski M., Tiefenbach J., Peters M.A., Brill B., Groner B., Bach I., Heinzel T., and Gottlicher M. The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J. 22 (2003) 3411-3420
32. Xu W.S., Parmigiani R.B., and Marks P.A. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 26 (2007) 5541-5552
33. Mariadason J.M., Corner G.A., and Augenlicht L.H. Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, and curcumin and implications for chemoprevention of colon cancer. Cancer Res. 60 (2000) 4561-4572
34. Glaser K.B., Staver M.J., Waring J.F., Stender J., Ulrich R.G., and Davidsen S.K. Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. Mol. Cancer. Ther. 2 (2003) 151-163
35. Chiba T., Yokosuka O., Fukai K., Kojima H., Tada M., Arai M., Imazeki F., and Saisho H. Cell growth inhibition and gene expression induced by the histone deacetylase inhibitor, trichostatin A, on human hepatoma cells. Oncology 66 (2004) 481-491
36. Johnstone R.W., and Licht J.D. Histone deacetylase inhibitors in cancer therapy: is transcription the primary target?. Cancer Cell 4 (2003) 13-18
37. Taddei A., Roche D., Bickmore W.A., and Almouzni G. The effects of histone deacetylase inhibitors on heterochromatin: implications for anticancer therapy?. EMBO Rep. 6 (2005) 520-524
38. Prasad K.N., Sinha P.K., Ramanujam M., and Sakamoto A. Sodium ascorbate potentiates the growth inhibitory effect of certain agents on neuroblastoma cells in culture. Proc. Natl. Acad. Sci. USA 76 (1979) 829-832
39. Arundel C.M., Glicksman A.S., and Leith J.T. Enhancement of radiation injury in human colon tumor cells by the maturational agent sodium butyrate (NaB). Radiat. Res. 104 (1985) 443-448
40. Nackerdien Z., Michie J., and Bohm L. Chromatin decondensed by acetylation shows an elevated radiation response. Radiat. Res. 117 (1989) 234-244
41. Karagiannis T.C., and El-Osta A. The paradox of histone deacetylase inhibitor-mediated modulation of cellular responses to radiation. Cell Cycle 5 (2006) 288-295
42. Camphausen K., Scott T., Sproull M., and Tofilon P.J. Enhancement of xenograft tumor radiosensitivity by the histone deacetylase inhibitor MS-275 and correlation with histone hyperacetylation. Clin. Cancer Res. 10 (2004) 6066-6071
43. Camphausen K., Cerna D., Scott T., Sproull M., Burgan W.E., Cerra M.A., Fine H., and Tofilon P.J. Enhancement of in vitro and in vivo tumor cell radiosensitivity by valproic acid. Int. J. Cancer 114 (2005) 380-386
44. Geng L., Cuneo K.C., Fu A., Tu T., Atadja P.W., and Hallahan D.E. Histone deacetylase (HDAC) inhibitor LBH589 increases duration of gamma-H2AX foci and confines HDAC4 to the cytoplasm in irradiated non-small cell lung cancer. Cancer Res. 66 (2006) 11298-11304
45. Cuneo K.C., Fu A., Osusky K., Huamani J., Hallahan D.E., and Geng L. Histone deacetylase inhibitor NVP-LAQ824 sensitizes human nonsmall cell lung cancer to the cytotoxic effects of ionizing radiation. Anticancer Drugs 18 (2007) 793-800
46. Entin-Meer M., Yang X., VandenBerg S.R., Lamborn K.R., Nudelman A., Rephaeli A., and Haas-Kogan D.A. In vivo efficacy of a novel histone deacetylase inhibitor in combination with radiation for the treatment of gliomas. Neuro Oncol. 9 (2007) 82-88
47. Karagiannis T.C., Harikrishnan K.N., and El-Osta A. The histone deacetylase inhibitor, trichostatin A, enhances radiation sensitivity and accumulation of gammaH2A.X. Cancer Biol. Ther. 4 (2005) 787-793
48. Zhang Y., Adachi M., Zou H., Hareyama M., Imai K., and Shinomura Y. Histone deacetylase inhibitors enhance phosphorylation of histone H2AX after ionizing radiation. Int. J. Radiat. Oncol. Biol. Phys. 65 (2006) 859-866
49. Munshi A., Tanaka T., Hobbs M.L., Tucker S.L., Richon V.M., and Meyn R.E. Vorinostat, a histone deacetylase inhibitor, enhances the response of human tumor cells to ionizing radiation through prolongation of gamma-H2AX foci. Mol. Cancer Ther. 5 (2006) 1967-1974
50. Chung Y.L., Wang A.J., and Yao L.F. Antitumor histone deacetylase inhibitors suppress cutaneous radiation syndrome: Implications for increasing therapeutic gain in cancer radiotherapy. Mol. Cancer Ther. 3 (2004) 317-325
51. Kim M.S., Blake M., Baek J.H., Kohlhagen G., Pommier Y., and Carrier F. Inhibition of histone deacetylase increases cytotoxicity to anticancer drugs targeting DNA. Cancer Res. 63 (2003) 7291-7300
52. Ozaki K.I., Kishikawa F., Tanaka M., Sakamoto T., Tanimura S., and Kohno M. Histone deacetylase inhibitors enhance the chemosensitivity of tumor cells with cross-resistance to a wide range of DNA-damaging drugs. Cancer Sci. 99 (2008) 376-384
53. Nicolas E., Yamada T., Cam H.P., Fitzgerald P.C., Kobayashi R., and Grewal S.I. Distinct roles of HDAC complexes in promoter silencing, antisense suppression and DNA damage protection. Nat. Struct. Mol. Biol. 14 (2007) 372-380
54. Li X., and Manley J.L. Cotranscriptional processes and their influence on genome stability. Genes Dev. 20 (2006) 1838-1847
55. Vilenchik M.M., and Knudson A.G. Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc. Natl. Acad. Sci. USA 100 (2003) 12871-12876
56. Couedel C., Mills K.D., Barchi M., Shen L., Olshen A., Johnson R.D., Nussenzweig A., Essers J., Kanaar R., Li G.C., Alt F.W., and Jasin M. Collaboration of homologous recombination and nonhomologous end-joining factors for the survival and integrity of mice and cells. Genes Dev. 18 (2004) 1293-1304
57. Bakkenist C.J., and Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421 (2003) 499-506
58. Tamburini B.A., and Tyler J.K. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol. Cell. Biol. 25 (2005) 4903-4913
59. Jazayeri A., McAinsh A.D., and Jackson S.P. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 101 (2004) 1644-1649
60. Utley R.T., Lacoste N., Jobin-Robitaille O., Allard S., and Cote J. Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol. Cell. Biol. 25 (2005) 8179-8190
61. Murga M., Jaco I., Fan Y., Soria R., Martinez-Pastor B., Cuadrado M., Yang S.M., Blasco M.A., Skoultchi A.I., and Fernandez-Capetillo O. Global chromatin compaction limits the strength of the DNA damage response. J. Cell Biol. 178 (2007) 1101-1108
62. Masumoto H., Hawke D., Kobayashi R., and Verreault A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436 (2005) 294-298
63. Driscoll R., Hudson A., and Jackson S.P. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315 (2007) 649-652
64. Maas N.L., Miller K.M., DeFazio L.G., and Toczyski D.P. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol. Cell 23 (2006) 109-119
65. Chen C.S., Wang Y.C., Yang H.C., Huang P.H., Kulp S.K., Yang C.C., Lu Y.S., Matsuyama S., Chen C.Y., and Chen C.S. Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation. Cancer Res. 67 (2007) 5318-5327
66. Zhang Y., Carr T., Dimtchev A., Zaer N., Dritschilo A., and Jung M. Attenuated DNA damage repair by trichostatin A through BRCA1 suppression. Radiat. Res. 168 (2007) 115-124
67. Adimoolam S., Sirisawad M., Chen J., Thiemann P., Ford J.M., and Buggy J.J. HDAC inhibitor PCI-24781 decreases RAD51 expression and inhibits homologous recombination. Proc. Natl. Acad. Sci. USA 104 (2007) 19482-19487
68. Bhaskara S., Chyla B.J., Amann J.M., Knutson S.K., Cortez D., Sun Z.W., and Hiebert S.W. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol. Cell 30 (2008) 61-72
69. Sancar A., Lindsey-Boltz L.A., Unsal-Kacmaz K., and Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73 (2004) 39-85
70. Demple B., and DeMott M.S. Dynamics and diversions in base excision DNA repair of oxidized abasic lesions. Oncogene 21 (2002) 8926-8934
71. Caldecott K.W. Mammalian single-strand break repair: mechanisms and links with chromatin. DNA Repair (Amst) 6 (2007) 443-453
72. Ruefli A.A., Ausserlechner M.J., Bernhard D., Sutton V.R., Tainton K.M., Kofler R., Smyth M.J., and Johnstone R.W. The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proc. Natl. Acad. Sci. USA 98 (2001) 10833-10838
73. Rosato R.R., Almenara J.A., and Grant S. The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21CIP1/WAF1 1. Cancer Res. 63 (2003) 3637-3645
74. Ungerstedt J.S., Sowa Y., Xu W.S., Shao Y., Dokmanovic M., Perez G., Ngo L., Holmgren A., Jiang X., and Marks P.A. Role of thioredoxin in the response of normal and transformed cells to histone deacetylase inhibitors. Proc. Natl. Acad. Sci. USA 102 (2005) 673-678
75. Xu W., Ngo L., Perez G., Dokmanovic M., and Marks P.A. Intrinsic apoptotic and thioredoxin pathways in human prostate cancer cell response to histone deacetylase inhibitor. Proc. Natl. Acad. Sci. USA 103 (2006) 15540-15545
76. Sanda T., Okamoto T., Uchida Y., Nakagawa H., Iida S., Kayukawa S., Suzuki T., Oshizawa T., Suzuki T., Miyata N., and Ueda R. Proteome analyses of the growth inhibitory effects of NCH-51, a novel histone deacetylase inhibitor, on lymphoid malignant cells. Leukemia 21 (2007) 2344-2353
77. Butler L.M., Zhou X., Xu W.S., Scher H.I., Rifkind R.A., Marks P.A., and Richon V.M. The histone deacetylase inhibitor SAHA arrests cancer cell growth, up-regulates thioredoxin-binding protein-2, and down-regulates thioredoxin. Proc. Natl. Acad. Sci. USA 99 (2002) 11700-11705
78. Bhakat K.K., Mokkapati S.K., Boldogh I., Hazra T.K., and Mitra S. Acetylation of human 8-oxoguanine-DNA glycosylase by p300 and its role in 8-oxoguanine repair in vivo. Mol. Cell. Biol. 26 (2006) 1654-1665
79. Kops G.J., Foltz D.R., and Cleveland D.W. Lethality to human cancer cells through massive chromosome loss by inhibition of the mitotic checkpoint. Proc. Natl. Acad. Sci. USA 101 (2004) 8699-8704
80. Taddei A., Maison C., Roche D., and Almouzni G. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat. Cell. Biol. 3 (2001) 114-120
81. Rea S., Eisenhaber F., O'Carroll D., Strahl B.D., Sun Z.W., Schmid M., Opravil S., Mechtler K., Ponting C.P., Allis C.D., and Jenuwein T. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406 (2000) 593-599
82. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., and Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410 (2001) 120-124
83. Bernard P., Maure J.F., Partridge J.F., Genier S., Javerzat J.P., and Allshire R.C. Requirement of heterochromatin for cohesion at centromeres. Science 294 (2001) 2539-2542
84. Nonaka N., Kitajima T., Yokobayashi S., Xiao G., Yamamoto M., Grewal S.I., and Watanabe Y. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat. Cell. Biol. 4 (2002) 89-93
85. Koch B., Kueng S., Ruckenbauer C., Wendt K.S., and Peters J.M. The Suv39h-HP1 histone methylation pathway is dispensable for enrichment and protection of cohesin at centromeres in mammalian cells. Chromosoma (2007)
86. Cimini D., Mattiuzzo M., Torosantucci L., and Degrassi F. Histone hyperacetylation in mitosis prevents sister chromatid separation and produces chromosome segregation defects. Mol. Biol. Cell. 14 (2003) 3821-3833
87. Magnaghi-Jaulin L., and Jaulin C. Histone deacetylase activity is necessary for chromosome condensation during meiotic maturation in Xenopus laevis. Chromosome Res. 14 (2006) 319-332
88. Li Y., Kao G.D., Garcia B.A., Shabanowitz J., Hunt D.F., Qin J., Phelan C., and Lazar M.A. A novel histone deacetylase pathway regulates mitosis by modulating Aurora B kinase activity. Genes Dev. 20 (2006) 2566-2579
89. Ishii S., Kurasawa Y., Wong J., and Yu-Lee L.Y. Histone deacetylase 3 localizes to the mitotic spindle and is required for kinetochore-microtubule attachment. Proc. Natl. Acad. Sci. USA 105 (2008) 4179-4184
90. Park J.H., Jong H.S., Kim S.G., Jung Y., Lee K.W., Lee J.H., Kim D.K., Bang Y.J., and Kim T.Y. Inhibitors of histone deacetylases induce tumor-selective cytotoxicity through modulating Aurora-A kinase. J. Mol. Med. 86 (2008) 117-128
91. Stevens F.E., Beamish H., Warrener R., and Gabrielli B. Histone deacetylase inhibitors induce mitotic slippage. Oncogene 27 (2008) 1345-1354
92. Musacchio A., and Salmon E.D. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell. Biol 8 (2007) 379-393
93. Brito D.A., and Rieder C.L. Mitotic Checkpoint Slippage in Humans Occurs via Cyclin B Destruction in the Presence of an Active Checkpoint. Curr. Biol. 16 (2006) 1194-1200
94. Warrener R., Beamish H., Burgess A., Waterhouse N.J., Giles N., Fairlie D., and Gabrielli B. Tumor cell-selective cytotoxicity by targeting cell cycle checkpoints. FASEB J. 17 (2003) 1550-1552
95. Magnaghi-Jaulin L., Eot-Houllier G., Fulcrand G., and Jaulin C. Histone deacetylase inhibitors induce premature sister chromatid separation and override the mitotic spindle assembly checkpoint. Cancer Res. 67 (2007) 6360-6367
96. Dowling M., Voong K.R., Kim M., Keutmann M.K., Harris E., and Kao G.D. Mitotic spindle checkpoint inactivation by trichostatin a defines a mechanism for increasing cancer cell killing by microtubule-disrupting agents. Cancer Biol. Ther. 4 (2005) 197-206
97. Shin H.J., Baek K.H., Jeon A.H., Kim S.J., Jang K.L., Sung Y.C., Kim C.M., and Lee C.W. Inhibition of histone deacetylase activity increases chromosomal instability by the aberrant regulation of mitotic checkpoint activation. Oncogene 22 (2003) 3853-3858
98. Michel L., Diaz-Rodriguez E., Narayan G., Hernando E., Murty V.V., and Benezra R. Complete loss of the tumor suppressor MAD2 causes premature cyclin B degradation and mitotic failure in human somatic cells. Proc. Natl. Acad. Sci. USA 101 (2004) 4459-4464
99. Michel L.S., Liberal V., Chatterjee A., Kirchwegger R., Pasche B., Gerald W., Dobles M., Sorger P.K., Murty V.V., and Benezra R. MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409 (2001) 355-359
100. Kienitz A., Vogel C., Morales I., Muller R., and Bastians H. Partial downregulation of MAD1 causes spindle checkpoint inactivation and aneuploidy, but does not confer resistance towards taxol. Oncogene 24 (2005) 4301-4310
101. Carvalho A., Carmena M., Sambade C., Earnshaw W.C., and Wheatley S.P. Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J. Cell Sci. 116 (2003) 2987-2998
102. Lens S.M., Wolthuis R.M., Klompmaker R., Kauw J., Agami R., Brummelkamp T., Kops G., and Medema R.H. Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension. EMBO J. 22 (2003) 2934-2947
103. Morrow C.J., Tighe A., Johnson V.L., Scott M.I., Ditchfield C., and Taylor S.S. Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20. J. Cell Sci. 118 (2005) 3639-3652
104. Xu W.S., Perez G., Ngo L., Gui C.Y., and Marks P.A. Induction of polyploidy by histone deacetylase inhibitor: a pathway for antitumor effects. Cancer Res. 65 (2005) 7832-7839
105. Qiu L., Burgess A., Fairlie D.P., Leonard H., Parsons P.G., and Gabrielli B.G. Histone deacetylase inhibitors trigger a G2 checkpoint in normal cells that is defective in tumor cells. Mol. Biol. Cell 11 (2000) 2069-2083
106. Mikhailov A., Shinohara M., and Rieder C.L. Topoisomerase II and histone deacetylase inhibitors delay the G2/M transition by triggering the p38 MAPK checkpoint pathway. J. Cell Biol. 166 (2004) 517-526
107. Iwanaga Y., Chi Y.H., Miyazato A., Sheleg S., Haller K., Peloponese Jr. J.M., Li Y., Ward J.M., Benezra R., and Jeang K.T. Heterozygous deletion of mitotic arrest-deficient protein 1 (MAD1) increases the incidence of tumors in mice. Cancer Res. 67 (2007) 160-166
108. Weaver B.A., and Cleveland D.W. Aneuploidy: instigator and inhibitor of tumorigenesis. Cancer Res. 67 (2007) 10103-10105
109. Weaver B.A., Silk A.D., Montagna C., Verdier-Pinard P., and Cleveland D.W. Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell 11 (2007) 25-36
110. Kim T.Y., Bang Y.J., and Robertson K.D. Histone deacetylase inhibitors for cancer therapy. Epigenetics 1 (2006) 14-23