R-Roscovitine (Seliciclib) prevents DNA damage-induced cyclin A1 upregulation and hinders non-homologous end-joining (NHEJ) DNA repair

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Federico, Mario ^a,b,e   Symonds, Catherine E ^a   Bagella, Luigi ^a,c   Rizzolio, Flavio ^a,d   Fanale, Daniele ^b   Russo, Antonio ^a,b   Giordano, Antonio ^a,d,f  

^a Temple University   (United States)

^b UNIVERSITY OF PALERMO   (Italy)

^c UNIVERSITY OF SASSARI   (Italy)

^d UNIVERSITY OF SIENA   (Italy)

^e UNIVERSITY OF PALERMO   (Italy)

^f SHRO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 7; CYCLIN DEPENDENT KINASE 9; DOXORUBICIN; HISTONE H2AX; ROSCOVITINE; PROTEIN KINASE INHIBITOR; PURINE DERIVATIVE;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DRUG MECHANISM; GENOTOXICITY; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; NON HOMOLOGOUS END JOINING; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; UPREGULATION; DRUG EFFECT; METABOLISM; PH;

CYCLIN A1; DNA DAMAGE; DNA REPAIR; DOXORUBICIN; HYDROGEN-ION CONCENTRATION; PROTEIN KINASE INHIBITORS; PURINES; UP-REGULATION;

EID: 77955100859     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-208     Document Type: Article

References (49)

1. Lapenna S, Giordano A. Cell cycle kinases as therapeutic targets for cancer. Nat Rev Drug Discov 2009, 8:547-566. 10.1038/nrd2907, 19568282.
2. Payton M, Chung G, Yakowec P, Wong A, Powers D, Xiong L, Zhang N, Leal J, Bush TL, Santora V, et al. Discovery and evaluation of dual CDK1 and CDK2 inhibitors. Cancer Res 2006, 66:4299-4308. 10.1158/0008-5472.CAN-05-2507, 16618755.
3. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, et al. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 2008, 26:127-132. 10.1038/nbt1358, 18183025.
4. Benson C, White J, De Bono J, O'Donnell A, Raynaud F, Cruickshank C, McGrath H, Walton M, Workman P, Kaye S, et al. A phase I trial of the selective oral cyclin-dependent kinase inhibitor seliciclib (CYC202; R-Roscovitine), administered twice daily for 7 days every 21 days. Br J Cancer 2007, 96:29-37. 10.1038/sj.bjc.6603509, 2360206, 17179992.
5. Aldoss IT, Tashi T, Ganti AK. Seliciclib in malignancies. Expert Opin Investig Drugs 2009, 18:1957-1965. 10.1517/13543780903418445, 19938906.
6. Maggiorella L, Deutsch E, Frascogna V, Chavaudra N, Jeanson L, Milliat F, Eschwege F, Bourhis J. Enhancement of radiation response by roscovitine in human breast carcinoma in vitro and in vivo. Cancer Res 2003, 63:2513-2517.
7. Deans AJ, Khanna KK, McNees CJ, Mercurio C, Heierhorst J, McArthur GA. Cyclin-dependent kinase 2 functions in normal DNA repair and is a therapeutic target in BRCA1-deficient cancers. Cancer Res 2006, 66:8219-8226. 10.1158/0008-5472.CAN-05-3945, 16912201.
8. Hui AB, Yue S, Shi W, Alajez NM, Ito E, Green SR, Frame S, O'Sullivan B, Liu FF. Therapeutic efficacy of seliciclib in combination with ionizing radiation for human nasopharyngeal carcinoma. Clin Cancer Res 2009, 15:3716-3724. 10.1158/1078-0432.CCR-08-2790, 19470731.
9. Camphausen K, Brady KJ, Burgan WE, Cerra MA, Russell JS, Bull EE, Tofilon PJ. Flavopiridol enhances human tumor cell radiosensitivity and prolongs expression of gammaH2AX foci. Mol Cancer Ther 2004, 3:409-416.
10. Siegel-Lakhai WS, Rodenstein DO, Beijnen JH, Gianella-Borradori A, Schellens JH, Talbot DC. Phase I study of seliciclib (CYC202 or R-roscovitine) in combination with gemcitabine (gem)/cisplatin(cis) in patients with advanced Non-Small Cell Lung Cancer (NSCLC). Journal of Clinical Oncology 2005, 23.
11. Maude SL, Enders GH. Cdk inhibition in human cells compromises chk1 function and activates a DNA damage response. Cancer Res 2005, 65:780-786.
12. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J, Jackson SP. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 2006, 8:37-45. 10.1038/ncb1337, 16327781.
13. Johnson N, Cai D, Kennedy RD, Pathania S, Arora M, Li YC, D'Andrea AD, Parvin JD, Shapiro GI. Cdk1 participates in BRCA1-dependent S phase checkpoint control in response to DNA damage. Mol Cell 2009, 35:327-339. 10.1016/j.molcel.2009.06.036, 19683496.
14. Branzei D, Foiani M. Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol 2008, 9:297-308. 10.1038/nrm2351, 18285803.
15. Wang Y, Prives C. Increased and altered DNA binding of human p53 by S and G2/M but not G1 cyclin-dependent kinases. Nature 1995, 376:88-91. 10.1038/376088a0, 7596441.
16. Ruffner H, Jiang W, Craig AG, Hunter T, Verma IM. BRCA1 is phosphorylated at serine 1497 in vivo at a cyclin-dependent kinase 2 phosphorylation site. Mol Cell Biol 1999, 19:4843-4854. 84283, 10373534.
17. Esashi F, Christ N, Gannon J, Liu Y, Hunt T, Jasin M, West SC. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 2005, 434:598-604. 10.1038/nature03404, 15800615.
18. Mazumder S, Plesca D, Kinter M, Almasan A. Interaction of a cyclin E fragment with Ku70 regulates Bax-mediated apoptosis. Mol Cell Biol 2007, 27:3511-3520. 10.1128/MCB.01448-06, 1899959, 17325036.
19. Hayami R, Sato K, Wu W, Nishikawa T, Hiroi J, Ohtani-Kaneko R, Fukuda M, Ohta T. Down-regulation of BRCA1-BARD1 ubiquitin ligase by CDK2. Cancer Res 2005, 65:6-10.
20. Cerqueira A, Santamaria D, Martinez-Pastor B, Cuadrado M, Fernandez-Capetillo O, Barbacid M. Overall Cdk activity modulates the DNA damage response in mammalian cells. J Cell Biol 2009, 187:773-780. 10.1083/jcb.200903033, 2806328, 19995934.
21. Campaner S, Doni M, Hydbring P, Verrecchia A, Bianchi L, Sardella D, Schleker T, Perna D, Tronnersjo S, Murga M, et al. Cdk2 suppresses cellular senescence induced by the c-myc oncogene. Nat Cell Biol 2010, 12:54-59. sup pp 51-14, 10.1038/ncb2004, 20010815.
22. Mazumder S, Gong B, Almasan A. Cyclin E induction by genotoxic stress leads to apoptosis of hematopoietic cells. Oncogene 2000, 19:2828-2835. 10.1038/sj.onc.1203623, 1189738, 10851086.
23. Wegiel B, Bjartell A, Tuomela J, Dizeyi N, Tinzl M, Helczynski L, Nilsson E, Otterbein LE, Harkonen P, Persson JL. Multiple cellular mechanisms related to cyclin A1 in prostate cancer invasion and metastasis. J Natl Cancer Inst 2008, 100:1022-1036. 10.1093/jnci/djn214, 2467435, 18612129.
24. Yang N, Eijsink JJ, Lendvai A, Volders HH, Klip H, Buikema HJ, van Hemel BM, Schuuring E, van der Zee AG, Wisman GB. Methylation markers for CCNA1 and C13ORF18 are strongly associated with high-grade cervical intraepithelial neoplasia and cervical cancer in cervical scrapings. Cancer Epidemiol Biomarkers Prev 2009, 18:3000-3007. 10.1158/1055-9965.EPI-09-0405, 19843677.
25. Yang R, Morosetti R, Koeffler HP. Characterization of a second human cyclin A that is highly expressed in testis and in several leukemic cell lines. Cancer Res 1997, 57:913-920.
26. Rivera A, Mavila A, Bayless KJ, Davis GE, Maxwell SA. Cyclin A1 is a p53-induced gene that mediates apoptosis, G2/M arrest, and mitotic catastrophe in renal, ovarian, and lung carcinoma cells. Cell Mol Life Sci 2006, 63:1425-1439. 10.1007/s00018-006-5521-5, 16799873.
27. Muller-Tidow C, Ji P, Diederichs S, Potratz J, Baumer N, Kohler G, Cauvet T, Choudary C, van der Meer T, Chan WY, et al. The cyclin A1-CDK2 complex regulates DNA double-strand break repair. Mol Cell Biol 2004, 24:8917-8928. 10.1128/MCB.24.20.8917-8928.2004, 517883, 15456866.
28. Ji P, Baumer N, Yin T, Diederichs S, Zhang F, Beger C, Welte K, Fulda S, Berdel WE, Serve H, Muller-Tidow C. DNA damage response involves modulation of Ku70 and Rb functions by cyclin A1 in leukemia cells. Int J Cancer 2007, 121:706-713. 10.1002/ijc.22634, 17455244.
29. Joshi AR, Jobanputra V, Lele KM, Wolgemuth DJ. Distinct properties of cyclin-dependent kinase complexes containing cyclin A1 and cyclin A2. Biochem Biophys Res Commun 2009, 378:595-599. 10.1016/j.bbrc.2008.11.077, 19056339.
30. Anderson JA, Lewellyn AL, Maller JL. Ionizing radiation induces apoptosis and elevates cyclin A1-Cdk2 activity before but not after the midblastula transition in Xenopus. Mol Biol Cell 1997, 8:1195-1206. 276146, 9243501.
31. Cho NH, Choi YP, Moon DS, Kim H, Kang S, Ding O, Rha SY, Yang YJ, Cho SH. Induction of cell apoptosis in non-small cell lung cancer cells by cyclin A1 small interfering RNA. Cancer Sci 2006, 97:1082-1092. 10.1111/j.1349-7006.2006.00292.x, 16984381.
32. Muller C, Yang R, Beck-von-Peccoz L, Idos G, Verbeek W, Koeffler HP. Cloning of the cyclin A1 genomic structure and characterization of the promoter region. GC boxes are essential for cell cycle-regulated transcription of the cyclin A1 gene. J Biol Chem 1999, 274:11220-11228. 10.1074/jbc.274.16.11220, 10196209.
33. Ambrosini G, Seelman SL, Qin LX, Schwartz GK. The cyclin-dependent kinase inhibitor flavopiridol potentiates the effects of topoisomerase I poisons by suppressing Rad51 expression in a p53-dependent manner. Cancer Res 2008, 68:2312-2320. 10.1158/0008-5472.CAN-07-2395, 18381438.
34. Lu X, Burgan WE, Cerra MA, Chuang EY, Tsai MH, Tofilon PJ, Camphausen K. Transcriptional signature of flavopiridol-induced tumor cell death. Mol Cancer Ther 2004, 3:861-872.
35. Alvi AJ, Austen B, Weston VJ, Fegan C, MacCallum D, Gianella-Borradori A, Lane DP, Hubank M, Powell JE, Wei W, et al. A novel CDK inhibitor, CYC202 (R-roscovitine), overcomes the defect in p53-dependent apoptosis in B-CLL by down-regulation of genes involved in transcription regulation and survival. Blood 2005, 105:4484-4491. 10.1182/blood-2004-07-2713, 15692065.
36. Hsieh WS, Soo R, Peh BK, Loh T, Dong D, Soh D, Wong LS, Green S, Chiao J, Cui CY, et al. Pharmacodynamic effects of seliciclib, an orally administered cell cycle modulator, in undifferentiated nasopharyngeal cancer. Clin Cancer Res 2009, 15:1435-1442. 10.1158/1078-0432.CCR-08-1748, 19228744.
37. MacCallum DE, Melville J, Frame S, Watt K, Anderson S, Gianella-Borradori A, Lane DP, Green SR. Seliciclib (CYC202, R-Roscovitine) induces cell death in multiple myeloma cells by inhibition of RNA polymerase II-dependent transcription and down-regulation of Mcl-1. Cancer Res 2005, 65:5399-5407. 10.1158/0008-5472.CAN-05-0233, 15958589.
38. Bracken AP, Ciro M, Cocito A, Helin K. E2F target genes: unraveling the biology. Trends Biochem Sci 2004, 29:409-417. 10.1016/j.tibs.2004.06.006, 15362224.
39. Iliakis G. Backup pathways of NHEJ in cells of higher eukaryotes: cell cycle dependence. Radiother Oncol 2009, 92:310-315. 10.1016/j.radonc.2009.06.024, 19604590.
40. Caracciolo V, D'Agostino L, Draberova E, Sladkova V, Crozier-Fitzgerald C, Agamanolis DP, de Chadarevian JP, Legido A, Giordano A, Draber P, Katsetos CD. Differential expression and cellular distribution of gamma-tubulin and betaIII-tubulin in medulloblastomas and human medulloblastoma cell lines. J Cell Physiol 2010, 223:519-529.
41. Speit GaH A. The comet assay. DNA repair protocols: Mammalian systems 2006, 314:275-286. Totowa: Humana Press, Henderson DS, 2, [Walker JM (Series Editor) Methods in molecular biology].
42. Collins AR, Dusinska M, Horska A. Detection of alkylation damage in human lymphocyte DNA with the comet assay. Acta Biochimica Polonica 2001, 48:611-614.
43. Norbury CJ, Hickson ID. Cellular responses to DNA damage. Annual Reviews in Pharmacology and Toxicology 2001, 41:367-401.
44. Buck D, Malivert L, de Chasseval R, Barraud A, Fondaneche MC, Sanal O, Plebani A, Stephan JL, Hufnagel M, le Deist F, et al. Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 2006, 124:287-299. 10.1016/j.cell.2005.12.030, 16439204.
45. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy--analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004, 20:307-315. 10.1093/bioinformatics/btg405, 14960456.
46. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264. 10.1093/biostatistics/4.2.249, 12925520.
47. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
48. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001, 125:279-284. 10.1016/S0166-4328(01)00297-2, 11682119.
49. Wettenhall JM, Simpson KM, Satterley K, Smyth GK. affylmGUI: a graphical user interface for linear modeling of single channel microarray data. Bioinformatics 2006, 22:897-899. 10.1093/bioinformatics/btl025, 16455752.