Functional genomics identify Birc5/Survivin as a candidate gene involved in the chronotoxicity of cyclin-dependent kinase inhibitors

Cell Cycle

Volumn 13, Issue 6, 2014, Pages 984-991

  Siffroi Fernandez, Sandrine ^a   Dulong, Sandrine ^b,c   Li, Xiao Mei ^b,c   Filipski, Elisabeth ^b,c   Grećhez Cassiau, Aline ^a   Peteri Brun̈back, Brigitta ^a   Meijer, Laurent ^d   Lev́i, Francis ^b,c,e   Teboul, Michèle ^a   Delaunay, Franck ^a  

^a CENTRE DE BIOCHIMIE   (France)

^b INSERM   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d STATION BIOLOGIQUE   (France)

^e HÔPITAL PAUL BROUSSE   (France)

Author keywords

Birc5; Cell cycle; Circadian clock; Colon mucosa; Cyclin dependent kinase inhibitor; Seliciclib

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; SMALL INTERFERING RNA; SURVIVIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL DIVISION; CIRCADIAN RHYTHM; COLON MUCOSA; CONTROLLED STUDY; DRUG SENSITIVITY; EPITHELIUM CELL; FUNCTIONAL GENOMICS; GENE EXPRESSION; GENE IDENTIFICATION; MALE; MITOSIS; MOUSE; MUCOSA CELL; NONHUMAN;

BIRC5; CELL CYCLE; CIRCADIAN CLOCK; COLON MUCOSA; CYCLIN-DEPENDENT KINASE INHIBITOR; SELICICLIB;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL CYCLE; CELL LINE, TUMOR; CIRCADIAN RHYTHM; COLON; CYCLIN-DEPENDENT KINASES; INHIBITOR OF APOPTOSIS PROTEINS; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; MITOSIS; PROTEIN KINASE INHIBITORS; PURINES; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; TRANSCRIPTOME;

EID: 84897980275     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.27868     Document Type: Article

References (55)

1. Doherty CJ, Kay SA. Circadian control of global gene expression patterns. Annu Rev Genet 2010; 44:419-44; PMID:20809800; http://dx.doi.org/10.1146/ annurev-genet-102209-163432
2. Hastings MH, Reddy AB, Maywood ES. A clockwork web: circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 2003; 4:649-61; PMID:12894240; http://dx.doi.org/10.1038/nrn1177
3. Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, et al. PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 2004; 101:5339-46; PMID:14963227; http://dx.doi.org/10.1073/pnas.0308709101
4. Lowrey PL, Takahashi JS. Genetics of circadian rhythms in Mammalian model organisms. Adv Genet 2011; 74:175-230; PMID:21924978; http://dx.doi.org/10. 1016/B978-0-12-387690-4.00006-4
5. Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, Okamura H. Control mechanism of the circadian clock for timing of cell division in vivo. Science 2003; 302:255-9; PMID:12934012; http://dx.doi.org/10.1126/science.1086271
6. Spörl F, Korge S, Jürchott K, Wunderskirchner M, Schellenberg K, Heins S, Specht A, Stoll C, Klemz R, Maier B, et al. Krüppel-like factor 9 is a circadian transcription factor in human epidermis that controls proliferation of keratinocytes. Proc Natl Acad Sci USA 2012; 109:10903-8; PMID:22711835; http://dx.doi.org/10.1073/pnas.1118641109
7. Granda TG, Liu XH, Smaaland R, Cermakian N, Filipski E, Sassone-Corsi P, Lévi F. Circadian regulation of cell cycle and apoptosis proteins in mouse bone marrow and tumor. FASEB J 2005; 19:304-6; PMID:15545298
8. Kennedy MF, Tutton PJ, Barkla DH. Comparison of the circadian variation in cell proliferation in normal and neoplastic colonic epithelial cells. Cancer Lett 1985; 28:169-75; PMID:4052987; http://dx.doi.org/10.1016/0304-3835(85) 90072-2
9. Bjarnason GA, Jordan R. Circadian variation of cell proliferation and cell cycle protein expression in man: clinical implications. Prog Cell Cycle Res 2000; 4:193-206; PMID:10740826; http://dx.doi.org/10.1007/978-1-4615-4253-7-17
10. Miller BH, McDearmon EL, Panda S, Hayes KR, Zhang J, Andrews JL, Antoch MP, Walker JR, Esser KA, Hogenesch JB, et al. Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci USA 2007; 104:3342-7; PMID:17360649; http://dx.doi.org/10.1073/pnas.0611724104
11. Gréchez-Cassiau A, Rayet B, Guillaumond F, Teboul M, Delaunay F. The circadian clock component BMAL1 is a critical regulator of p21WAF1/CIP1 expression and hepatocyte proliferation. J Biol Chem 2008; 283:4535-42; PMID:18086663; http://dx.doi.org/10.1074/jbc.M705576200
12. Gery S, Komatsu N, Baldjyan L, Yu A, Koo D, Koeffler HP. The circadian gene per1 plays an important role in cell growth and DNA damage control in human cancer cells. Mol Cell 2006; 22:375-82; PMID:16678109; http://dx.doi.org/10. 1016/j.molcel.2006.03.038
13. Kowalska E, Ripperger JA, Hoegger DC, Bruegger P, Buch T, Birchler T, Mueller A, Albrecht U, Contaldo C, Brown SA. NONO couples the circadian clock to the cell cycle. Proc Natl Acad Sci USA 2013; 110:1592-9; PMID:23267082; http://dx.doi.org/10.1073/pnas.1213317110
14. Innominato PF, Focan C, Gorlia T, Moreau T, Garufi C, Waterhouse J, Giacchetti S, Coudert B, Iacobelli S, Genet D, et al.; Chronotherapy Group of the European Organization for Research and Treament of Cancer. Circadian rhythm in rest and activity: a biological correlate of quality of life and a predictor of survival in patients with metastatic colorectal cancer. Cancer Res 2009; 69:4700-7; PMID:19470769; http://dx.doi.org/10.1158/0008-5472.CAN-08-4747
15. monographs I. Painting, firefighting, and shiftwork. Eval Carcinog Risks Hum 2010; 98:9-764
16. Fu L, Pelicano H, Liu J, Huang P, Lee C. The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 2002; 111:41-50; PMID:12372299; http://dx.doi.org/10.1016/S0092-8674(02)00961-3
17. Filipski E, Delaunay F, King VM, Wu MW, Claustrat B, Gréchez- Cassiau A, Guettier C, Hastings MH, Francis L. Effects of chronic jet lag on tumor progression in mice. Cancer Res 2004; 64:7879-85; PMID:15520194; http://dx.doi.org/10.1158/0008-5472.CAN-04-0674
18. Levi F, Schibler U. Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol 2007; 47:593-628; PMID:17209800; http://dx.doi.org/10.1146/annurev.pharmtox.47.120505.105208
19. Lévi F, Okyar A, Dulong S, Innominato PF, Clairambault J. Circadian timing in cancer treatments. Annu Rev Pharmacol Toxicol 2010; 50:377-421; PMID:20055686; http://dx.doi.org/10.1146/annurev.pharmtox.48.113006. 094626
20. Ahowesso C, Li XM, Zampera S, Peteri-Brunbäck B, Dulong S, Beau J, Hossard V, Filipski E, Delaunay F, Claustrat B, et al. Sex and dosing-time dependencies in irinotecan-induced circadian disruption. Chronobiol Int 2011; 28:458-70; PMID:21721861; http://dx.doi.org/10.3109/07420528.2011.569043
21. Kennedy MF, Tutton PJ, Barkla DH. Adrenergic factors regulating cell division in the colonic crypt epithelium during carcinogenesis and in colonic adenoma and adenocarcinoma. Br J Cancer 1985; 52:383-90; PMID:4041364; http://dx.doi.org/10.1038/bjc.1985.205
22. Malumbres M, Barbacid M. Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer 2009; 9:153-66; PMID:19238148; http://dx.doi.org/10. 1038/nrc2602
23. Marra G, Anti M, Percesepe A, Armelao F, Ficarelli R, Coco C, Rinelli A, Vecchio FM, D'Arcangelo E. Circadian variations of epithelial cell proliferation in human rectal crypts. Gastroenterology 1994; 106:982-7; PMID:8144003
24. Sherman H, Froy O. Expression of human beta-defensin 1 is regulated via c-Myc and the biological clock. Mol Immunol 2008; 45:3163-7; PMID:18433872; http://dx.doi.org/10.1016/j.molimm.2008.03.004
25. Iurisci I, Filipski E, Sallam H, Harper F, Guettier C, Maire I, Hassan M, Iacobelli S, Lévi F. Liver circadian clock, a pharmacologic target of cyclin-dependent kinase inhibitor seliciclib. Chronobiol Int 2009; 26:1169-88; PMID:19731111
26. Iurisci I, Filipski E, Reinhardt J, Bach S, Gianella-Borradori A, Iacobelli S, Meijer L, Lévi F. Improved tumor control through circadian clock induction by Seliciclib, a cyclin-dependent kinase inhibitor. Cancer Res 2006; 66:10720-8; PMID:17108108; http://dx.doi.org/10.1158/0008-5472.CAN-06-2086
27. Hoogerwerf WA, Hellmich HL, Cornélissen G, Halberg F, Shahinian VB, Bostwick J, Savidge TC, Cassone VM. Clock gene expression in the murine gastrointestinal tract: endogenous rhythmicity and effects of a feeding regimen. Gastroenterology 2007; 133:1250-60; PMID:17919497; http://dx.doi.org/10.1053/j. gastro.2007.07.009
28. Sládek M, Rybová M, Jindráková Z, Zemanová Z, Polidarová L, Mrnka L, O'Neill J, Pácha J, Sumová A. Insight into the circadian clock within rat colonic epithelial cells. Gastroenterology 2007; 133:1240-9; PMID:17675004; http://dx.doi.org/10. 1053/j.gastro.2007.05.053
29. Hoogerwerf WA, Sinha M, Conesa A, Luxon BA, Shahinian VB, Cornélissen G, Halberg F, Bostwick J, Timm J, Cassone VM. Transcriptional profiling of mRNA expression in the mouse distal colon. Gastroenterology 2008; 135:2019-29; PMID:18848557; http://dx.doi.org/10.1053/j.gastro.2008.08.048
30. Okyar A, Piccolo E, Ahowesso C, Filipski E, Hossard V, Guettier C, La Sorda R, Tinari N, Iacobelli S, Lévi F. Strain- and sex-dependent circadian changes in abcc2 transporter expression: implications for irinotecan chronotolerance in mouse ileum. PLoS One 2011; 6:e20393; PMID:21674030; http://dx.doi.org/10.1371/journal.pone.0020393
31. Koike N, Yoo SH, Huang HC, Kumar V, Lee C, Kim TK, Takahashi JS. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 2012; 338:349-54; PMID:22936566; http://dx.doi.org/10.1126/ science.1226339
32. Plikus MV, Vollmers C, de la Cruz D, Chaix A, Ramos R, Panda S, Chuong CM. Local circadian clock gates cell cycle progression of transient amplifying cells during regenerative hair cycling. Proc Natl Acad Sci USA 2013; 110:E2106-15; PMID:23690597; http://dx.doi.org/10.1073/pnas.1215935110
33. Khapre RV, Kondratova AA, Susova O, Kondratov RV. Circadian clock protein BMAL1 regulates cellular senescence in vivo. Cell Cycle 2011; 10:4162-9; PMID:22101268; http://dx.doi.org/10.4161/cc.10.23.18381
34. Innominato PF, Lévi FA, Bjarnason GA. Chronotherapy and the molecular clock: Clinical implications in oncology. Adv Drug Deliv Rev 2010; 62:979-1001; PMID:20600409; http://dx.doi.org/10.1016/j.addr.2010.06.002
35. Narasimamurthy R, Hatori M, Nayak SK, Liu F, Panda S, Verma IM. Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc Natl Acad Sci USA 2012; 109:12662-7; PMID:22778400; http://dx.doi.org/10.1073/pnas.1209965109
36. Spengler ML, Kuropatwinski KK, Comas M, Gasparian AV, Fedtsova N, Gleiberman AS, Gitlin II, Artemicheva NM, Deluca KA, Gudkov AV, et al. Core circadian protein CLOCK is a positive regulator of NFκB-mediated transcription. Proc Natl Acad Sci USA 2012; 109:E2457-65; PMID:22895791; http://dx.doi.org/10.1073/pnas.1206274109
37. Bellet MM, Zocchi L, Sassone-Corsi P. The RelB subunit of NFκB acts as a negative regulator of circadian gene expression. Cell Cycle 2012; 11:3304-11; PMID:22894897; http://dx.doi.org/10.4161/cc.21669
38. Mauro C, Leow SC, Anso E, Rocha S, Thotakura AK, Tornatore L, Moretti M, De Smaele E, Beg AA, Tergaonkar V, et al. NFκB controls energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration. Nat Cell Biol 2011; 13:1272-9; PMID:21968997; http://dx.doi.org/10.1038/ncb2324
39. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j.cell.2011.02.013
40. Hu Y, Spengler ML, Kuropatwinski KK, Comas-Soberats M, Jackson M, Chernov MV, Gleiberman AS, Fedtsova N, Rustum YM, Gudkov AV, et al. Selenium is a modulator of circadian clock that protects mice from the toxicity of a chemotherapeutic drug via upregulation of the core clock protein, BMAL1. Oncotarget 2011; 2:1279-90; PMID:22249125
41. Le Tourneau C, Faivre S, Laurence V, Delbaldo C, Vera K, Girre V, Chiao J, Armour S, Frame S, Green SR, et al. Phase I evaluation of seliciclib (R-roscovitine), a novel oral cyclin-dependent kinase inhibitor, in patients with advanced malignancies. Eur J Cancer 2010; 46:3243-50; PMID:20822897; http://dx.doi.org/10.1016/j.ejca.2010.08.001
42. Bettayeb K, Oumata N, Echalier A, Ferandin Y, Endicott JA, Galons H, Meijer L. CR8, a potent and selective, roscovitine-derived inhibitor of cyclin-dependent kinases. Oncogene 2008; 27:5797-807; PMID:18574471; http://dx.doi.org/10.1038/onc.2008.191
43. Nutley BP, Raynaud FI, Wilson SC, Fischer PM, Hayes A, Goddard PM, McClue SJ, Jarman M, Lane DP, Workman P. Metabolism and pharmacokinetics of the cyclin-dependent kinase inhibitor R-roscovitine in the mouse. Mol Cancer Ther 2005; 4:125-39; PMID:15657360
44. Altieri DC. Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer 2008; 8:61-70; PMID:18075512; http://dx.doi.org/10. 1038/nrc2293
45. Altieri DC. New wirings in the survivin networks. Oncogene 2008; 27:6276-84; PMID:18931693; http://dx.doi.org/10.1038/onc.2008.303
46. Rödel F, Sprenger T, Kaina B, Liersch T, Rödel C, Fulda S, Hehlgans S. Survivin as a prognostic/predictive marker and molecular target in cancer therapy. Curr Med Chem 2012; 19:3679-88; PMID:22680927; http://dx.doi.org/10.2174/092986712801661040
47. Church DN, Talbot DC. Survivin in solid tumors: rationale for development of inhibitors. Curr Oncol Rep 2012; 14:120-8; PMID:22234703; http://dx.doi.org/10.1007/s11912-012-0215-2
48. Zhao J, Tenev T, Martins LM, Downward J, Lemoine NR. The ubiquitin-proteasome pathway regulates survivin degradation in a cell cycle-dependent manner. J Cell Sci 2000; 113:4363-71; PMID:11069780
49. Tsukahara T, Tanno Y, Watanabe Y. Phosphorylation of the CPC by Cdk1 promotes chromosome bi-orientation. Nature 2010; 467:719-23; PMID:20739936; http://dx.doi.org/10.1038/nature09390
50. Meijer L, Bettayeb K, Galons H. (R)-Roscovitin (CYC202, Seliciclib). In: Smith PJ, Yue EW, eds. Inhibitors of Cyclin-dependentKinases as Anti-tumor Agents: CRC, 2006:187-225.
51. Guha M, Altieri DC. Survivin as a global target of intrinsic tumor suppression networks. Cell Cycle 2009; 8:2708-10; PMID:19717980; http://dx.doi.org/10.4161/cc.8.17.9457
52. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001; 98:5116-21; PMID:11309499; http://dx.doi.org/10.1073/pnas.091062498
53. Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4:44-57; PMID:19131956; http://dx.doi.org/10.1038/nprot.2008.211
54. Oumata N, Ferandin Y, Meijer L, Galon H. Practical Synthesis of Roscovitine and CR8. Org Process Res Dev 2009; 13:641-4; http://dx.doi.org/10. 1021/op800284k
55. Bingham C, Arbogast B, Guillaume GC, Lee JK, Halberg F. Inferential statistical methods for estimating and comparing cosinor parameters. Chronobiologia 1982; 9:397-439; PMID:7168995