Day and night variations in the repair of ionizing-radiation-induced DNA damage in mouse splenocytes

DNA Repair

Volumn 28, Issue , 2015, Pages 37-47

  Palombo, Philipp ^a   Moreno Villanueva, Maria ^a   Mangerich, Aswin ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Circadian rhythm; DNA repair; FADU assay; Gene profiling; Ionizing radiation; Molecular clock; QPCR

Indexed keywords

DOUBLE STRANDED DNA; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE PROGRESSION; CELL ISOLATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; EXCISION REPAIR; GENE EXPRESSION; GENE EXPRESSION PROFILING; IONIZING RADIATION; LIGHT DARK CYCLE; MOUSE; NONHUMAN; OSCILLATION; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SPLEEN CELL; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; RADIATION RESPONSE; SPLEEN; X RAY;

MAMMALIA; MUS;

ANIMALS; CIRCADIAN RHYTHM; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION; MICE; RNA, MESSENGER; SPLEEN; X-RAYS;

EID: 84923331798     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2015.02.002     Document Type: Article

References (59)

1. Dallmann R., Brown S.A., Gachon F. Chronopharmacology: new insights and therapeutic implications. Annu. Rev. Pharmacol. Toxicol. 2014, 54:339-361.
2. Ripperger J.A., Jud C., Albrecht U. The daily rhythm of mice. FEBS Lett. 2011, 585:1384-1392.
3. Robinson I., Reddy A.B. Molecular mechanisms of the circadian clockwork in mammals. FEBS Lett. 2014, 588:2477-2483.
4. Storch K.F., Lipan O., Leykin I., Viswanathan N., Davis F.C., Wong W.H., Weitz C.J. Extensive and divergent circadian gene expression in liver and heart. Nature 2002, 417:78-83.
5. Koike N., Yoo S.H., Huang H.C., Kumar V., Lee C., Kim T.K., Takahashi J.S. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 2012, 338:349-354.
6. Miller B.H., McDearmon E.L., Panda S., Hayes K.R., Zhang J., Andrews J.L., Antoch M.P., Walker J.R., Esser K.A., Hogenesch J.B., Takahashi J.S. Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3342-3347.
7. Oishi K., Miyazaki K., Kadota K., Kikuno R., Nagase T., Atsumi G., Ohkura N., Azama T., Mesaki M., Yukimasa S., Kobayashi H., Iitaka C., Umehara T., Horikoshi M., Kudo T., Shimizu Y., Yano M., Monden M., Machida K., Matsuda J., Horie S., Todo T., Ishida N. Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J. Biol. Chem. 2003, 278:41519-41527.
8. Panda S., Antoch M.P., Miller B.H., Su A.I., Schook A.B., Straume M., Schultz P.G., Kay S.A., Takahashi J.S., Hogenesch J.B. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 2002, 109:307-320.
9. Bass J. Circadian topology of metabolism. Nature 2012, 491:348-356.
10. Antoch M.P., Kondratov R.V. Circadian proteins and genotoxic stress response. Circ. Res. 2010, 106:68-78.
11. Thompson C.L., Sancar A. Photolyase/cryptochrome blue-light photoreceptors use photon energy to repair DNA and reset the circadian clock. Oncogene 2002, 21:9043-9056.
12. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 2001, 411:366-374.
13. Gery S., Komatsu N., Baldjyan L., Yu A., Koo D., Koeffler H.P. The circadian gene per1 plays an important role in cell growth and DNA damage control in human cancer cells. Mol. Cell 2006, 22:375-382.
14. Cotta-Ramusino C., McDonald E.R., Hurov K., Sowa M.E., Harper J.W., Elledge S.J. A DNA damage response screen identifies RHINO, a 9-1-1 and TopBP1 interacting protein required for ATR signaling. Science 2011, 332:1313-1317.
15. Kang T.-H., Leem S.-H. Modulation of ATR-mediated DNA damage checkpoint response by cryptochrome 1. Nucleic Acids Res. 2014, 42(7):4427-4434.
16. Antoch M.P., Kondratov R.V. Pharmacological modulators of the circadian clock as potential therapeutic drugs: focus on genotoxic/anticancer therapy. Handb Exp. Pharmacol. 2013, 289-309.
17. Masri S., Cervantes M., Sassone-Corsi P. The circadian clock and cell cycle: interconnected biological circuits. Curr. Opin. Cell Biol. 2013, 25:730-734.
18. Sancar A., Lindsey-Boltz L.A., Kang T.H., Reardon J.T., Lee J.H., Ozturk N. Circadian clock control of the cellular response to DNA damage. FEBS Lett. 2010, 584:2618-2625.
19. Kang T.H., Reardon J.T., Kemp M., Sancar A. Circadian oscillation of nucleotide excision repair in mammalian brain. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2864-2867.
20. Kang T.H., Lindsey-Boltz L.A., Reardon J.T., Sancar A. Circadian control of XPA and excision repair of cisplatin-DNA damage by cryptochrome and HERC2 ubiquitin ligase. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4890-4895.
21. Gaddameedhi S., Selby C.P., Kaufmann W.K., Smart R.C., Sancar A. Control of skin cancer by the circadian rhythm. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18790-18795.
22. Unsal-Kacmaz K., Mullen T.E., Kaufmann W.K., Sancar A. Coupling of human circadian and cell cycles by the timeless protein. Mol. Cell. Biol. 2005, 25:3109-3116.
23. Yang X., Wood P.A., Hrushesky W.J. Mammalian TIMELESS is required for ATM-dependent CHK2 activation and G2/M checkpoint control. J. Biol. Chem. 2010, 285:3030-3034.
24. Chou D.M., Elledge S.J. Tipin and Timeless form a mutually protective complex required for genotoxic stress resistance and checkpoint function. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18143-18147.
25. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
26. Laranjeiro R., Tamai T.K., Peyric E., Krusche P., Ott S., Whitmore D. Cyclin-dependent kinase inhibitor p20 controls circadian cell-cycle timing. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6835-6840.
27. 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, 283:4535-4542.
28. Mullenders J., Fabius A.W.M., Madiredjo M., Bernards R., Beijersbergen R.L. A large scale shRNA barcode screen identifies the circadian clock component ARNTL as putative regulator of the p53 tumor suppressor pathway. PLoS One 2009, 4:e4798.
29. 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, 302:255-259.
30. Plikus M.V., Vollmers C., de la Cruz D., Chaix A., Ramos R., Panda S., Chuong C.M. Local circadian clock gates cell cycle progression of transient amplifying cells during regenerative hair cycling. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E2106-E2115.
31. 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.
32. Kelleher F.C., Rao A., Maguire A. Circadian molecular clocks and cancer. Cancer Lett. 2014, 342:9-18.
33. Kruisbeek A.M. Isolation of mouse mononuclear cells. Current Protocols in Immunology 2001, John Wiley & Sons, Inc, New York.
34. Moreno-Villanueva M., Eltze T., Dressler D., Bernhardt J., Hirsch C., Wick P., von Scheven G., Lex K., Bürkle A. The automated FADU-assay, a potential high-throughput in vitro method for early screening of DNA breakage. ALTEX 2011, 28:295-303.
35. Moreno-Villanueva M., Pfeiffer R., Sindlinger T., Leake A., Muller M., Kirkwood T.B., Bürkle A. A modified and automated version of the 'Fluorimetric Detection of Alkaline DNA Unwinding' method to quantify formation and repair of DNA strand breaks. BMC Biotechnol. 2009, 9:39.
36. Franceschini A., Szklarczyk D., Frankild S., Kuhn M., Simonovic M., Roth A., Lin J., Minguez P., Bork P., von Mering C., Jensen L.J. STRING v9.1: protein-protein interaction networks with increased coverage and integration. Nucleic Acids Res. 2013, 41:D808-D815.
37. Wang C., Gong B., Bushel P.R., Thierry-Mieg J., Thierry-Mieg D., Xu J., Fang H., Hong H., Shen J., Su Z., Meehan J., Li X., Yang L., Li H., Labaj P.P., Kreil D.P., Megherbi D., Gaj S., Caiment F., van Delft J., Kleinjans J., Scherer A., Devanarayan V., Wang J., Yang Y., Qian H.-R., Lancashire L.J., Bessarabova M., Nikolsky Y., Furlanello C., Chierici M., Albanese D., Jurman G., Riccadonna S., Filosi M., Visintainer R., Zhang K.K., Li J., Hsieh J.-H., Svoboda D.L., Fuscoe J.C., Deng Y., Shi L., Paules R.S., Auerbach S.S., Tong W. The concordance between RNA-seq and microarray data depends on chemical treatment and transcript abundance. Nat. Biotechnol. 2014, 32:926-932.
38. Morath J., Moreno-Villanueva M., Hamuni G., Kolassa S., Ruf-Leuschner M., Schauer M., Elbert T., Bürkle A., Kolassa I.T. Effects of psychotherapy on DNA strand break accumulation originating from traumatic stress. Psychothe. Psychosom. 2014, 83:289-297.
39. Mangerich A., Herbach N., Hanf B., Fischbach A., Popp O., Moreno-Villanueva M., Bruns O.T., Bürkle A. Inflammatory and age-related pathologies in mice with ectopic expression of human PARP-1. Mech. Ageing Dev. 2010, 131:389-404.
40. Geyfman M., Kumar V., Liu Q., Ruiz R., Gordon W., Espitia F., Cam E., Millar S.E., Smyth P., Ihler A., Takahashi J.S., Andersen B. Brain and muscle Arnt-like protein-1 (BMAL1) controls circadian cell proliferation and susceptibility to UVB-induced DNA damage in the epidermis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:11758-11763.
41. Liu S., Cai Y., Sothern R.B., Guan Y., Chan P. Chronobiological analysis of circadian patterns in transcription of seven key clock genes in six peripheral tissues in mice. Chronobiol. Int. 2007, 24:793-820.
42. Silver A.C., Arjona A., Hughes M.E., Nitabach M.N., Fikrig E. Circadian expression of clock genes in mouse macrophages, dendritic cells, and B cells. Brain, Behav., Immun. 2012, 26:407-413.
43. DeBruyne J.P., Weaver D.R., Reppert S.M. CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat. Neurosci. 2007, 10:543-545.
44. Bertolucci C., Cavallari N., Colognesi I., Aguzzi J., Chen Z., Caruso P., Foa A., Tosini G., Bernardi F., Pinotti M. Evidence for an overlapping role of CLOCK and NPAS2 transcription factors in liver circadian oscillators. Mol. Cell. Biol. 2008, 28:3070-3075.
45. Dudley C.A., Erbel-Sieler C., Estill S.J., Reick M., Franken P., Pitts S., McKnight S.L. Altered patterns of sleep and behavioral adaptability in NPAS2-deficient mice. Science 2003, 301:379-383.
46. Scheiermann C., Kunisaki Y., Frenette P.S. Circadian control of the immune system. Nat. Rev. Immunol. 2013, 13:190-198.
47. Curtis A.M., Bellet M.M., Sassone-Corsi P., O'Neill L.A. Circadian clock proteins and immunity. Immunity 2014, 40:178-186.
48. Keller M., Mazuch J., Abraham U., Eom G.D., Herzog E.D., Volk H.-D., Kramer A., Maier B. A circadian clock in macrophages controls inflammatory immune responses. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:21407-21412.
49. Nguyen T.T., Mattick J.S., Yang Q., Orman M.A., Ierapetritou M.G., Berthiaume F., Androulakis I.P. Bioinformatics analysis of transcriptional regulation of circadian genes in rat liver. BMC Bioinf. 2014, 15:83.
50. Pizarro A., Hayer K., Lahens N.F., Hogenesch J.B. CircaDB: a database of mammalian circadian gene expression profiles. Nucleic Acids Res. 2013, 41:D1009-D1013.
51. Curtin N.J. DNA repair dysregulation from cancer driver to therapeutic target. Nat. Rev. Cancer 2012, 12:801-817.
52. Di L.J., Fernandez A.G., De Siervi A., Longo D.L., Gardner K. Transcriptional regulation of BRCA1 expression by a metabolic switch. Nat. Struct. Mol. Biol. 2010, 17:1406-1413.
53. Arias-Lopez C., Lazaro-Trueba I., Kerr P., Lord C.J., Dexter T., Iravani M., Ashworth A., Silva A. p53 modulates homologous recombination by transcriptional regulation of the RAD51 gene. EMBO Rep. 2006, 7:219-224.
54. Nakahata Y., Sahar S., Astarita G., Kaluzova M., Sassone-Corsi P. Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 2009, 324:654-657.
55. Marchenay C., Cellarier E., Levi F., Rolhion C., Kwiatkowski F., Claustrat B., Madelmont J.C., Chollet P. Circadian variation in O6-alkylguanine-DNA alkyltransferase activity in circulating blood mononuclear cells of healthy human subjects. Int. J. Cancer 2001, 91:60-66.
56. Sahar S., Sassone-Corsi P. Circadian clock and breast cancer: a molecular link. Cell Cycle 2007, 6:1329-1331.
57. Innominato P.F., Levi F.A., Bjarnason G.A. Chronotherapy and the molecular clock: clinical implications in oncology. Adv. Drug Deliv. Rev. 2010, 62:979-1001.
58. Van Dycke K.C., Nijman R.M., Wackers P.F., Jonker M.J., Rodenburg W., van Oostrom C.T., Salvatori D.C., Breit T.M., van Steeg H., Luijten M., van der Horst G.T. A day and night difference in the response of the hepatic transcriptome to cyclophosphamide treatment. Arch. Toxicol. 2015, 89(2):221-231.
59. Levi F., Okyar A., Dulong S., Innominato P.F., Clairambault J. Circadian timing in cancer treatments. Annu. Rev. Pharmacol. Toxicol. 2010, 50:377-421.