Circadian regulation of cell cycle: Molecular connections between aging and the circadian clock

Annals of Medicine

Volumn 42, Issue 6, 2010, Pages 404-415

  Khapre, Rohini V ^a   Samsa, William E ^a   Kondratov, Roman V ^a  

^a CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

Aging; Cancer; Cell cycle; Circadian clock; Genotoxic stress

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; ATM PROTEIN; ATR PROTEIN; CELL CYCLE PROTEIN; CYCLIN A; CYCLIN B1; CYCLIN D1; CYCLIN D3; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; PROTEIN BCL 2; PROTEIN MDM2; PROTEIN P53; PROTEIN P63;

AGING; BMAL1 GENE; CARCINOGENESIS; CELL CYCLE REGULATION; CELL PROLIFERATION; CIRCADIAN RHYTHM; CRYPTOCHROME GENE; DNA DAMAGE; DNA REPAIR; GENE; GENE EXPRESSION; GENE MUTATION; GENOME; GENOTOXICITY; HUMAN; METABOLIC REGULATION; MOLECULAR CLOCK; OSCILLATION; OXIDATIVE STRESS; PERIOD GENE; PREMATURE AGING; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; TRANSGENIC MOUSE;

AGING; ANIMALS; ARNTL TRANSCRIPTION FACTORS; BIOLOGICAL CLOCKS; CELL CYCLE; CIRCADIAN RHYTHM; CLOCK PROTEINS; DNA DAMAGE; HUMANS; NEOPLASMS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 77955163148     PISSN: 07853890     EISSN: 13652060     Source Type: Journal    
DOI: 10.3109/07853890.2010.499134     Document Type: Review

References (93)

1. Lowrey PL, Takahashi JS. Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet. 2004;5:407-441
2. Gachon F, Nagoshi E, Brown SA, Ripperger J, Schibler U. The mammalian circadian timing system: from gene expression to physiology. Chromosoma. 2004;113:103-112
3. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, et al. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell. 2002;109:307-320
4. Dardente H, Cermakian N. Molecular circadian rhythms in central and peripheral clocks in mammals. Chronobiol Int. 2007;24:195-213.
5. McClung CA. Circadian genes, rhythms and the biology of mood disorders. Pharmacol Ther. 2007;114:222-232
6. Laposky AD, Bass J, Kohsaka A, Turek FW. Sleep and cir-cadian rhythms: key components in the regulation of energy metabolism. FEBS Lett. 2008;582:142-151
7. Reilly DF, Westgate EJ, FitzGerald GA. Peripheral circadian clocks in the vasculature. Arterioscler Thromb Vasc Biol. 2007;27:1694-1705
8. Filipski E, Li XM, Levi F. Disruption of circadian coordination and malignant growth. Cancer Causes Control. 2006; 17:509-514
9. Curtis AM, Fitzgerald GA. Central and peripheral clocks in cardiovascular and metabolic function. Ann Med. 2006; 38:552-559
10. Lowden A, Moreno C, Holmback U, Lennernas M, Tucker P. Eating and shift work\effects on habits, metabolism and performance. Scand J Work Environ Health. 2010;36: 150-162
11. 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.
12. Kondratov RV, Kondratova AA, Gorbacheva VY, Vykhovan-ets OV, Antoch MP. Early aging and age-related pathologies in mice defi cient in BMAL1, the core component of the circadian clock. Genes Dev. 2006;20:1868-1873
13. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDear-mon E, et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science. 2005;308:1043-1045
14. Schibler U, Sassone-Corsi P. A web of circadian pacemakers. Cell. 2002;111:919-922
15. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, et al. Role of the CLOCK protein in the mammalian circadian mechanism. Science. 1998;280: 1564-1569
16. Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Rad-cliffe LA, Hogenesch JB, et al. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell. 2000;103:1009-1017
17. Antoch MP, Song EJ, Chang AM, Vitaterna MH, Zhao Y, Wilsbacher LD, et al. Functional identifi cation of the mouse circadian Clock gene by transgenic BAC rescue. Cell. 1997;89:655-667
18. King DP, Zhao Y, Sangoram AM, Wilsbacher LD, Tanaka M, Antoch MP, et al. Positional cloning of the mouse circadian clock gene. Cell. 1997;89:641-653
19. Hirayama J, Sassone-Corsi P. Structural and functional features of transcription factors controlling the circadian clock. Curr Opin Genet Dev. 2005;15:548-556
20. Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, Jin X, et al. mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell. 1999;98:193-205
21. Griffi n EA Jr, Staknis D, Weitz CJ. Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science. 1999;286:768-771
22. Sato TK, Panda S, Miraglia LJ, Reyes TM, Rudic RD, McNamara P, et al. A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron. 2004;43:527-537
23. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, et al. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell. 2002; 110:251-260 (Pubitemid 34876552)
24. Honma S, Kawamoto T, Takagi Y, Fujimoto K, Sato F, Noshiro M, et al. Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature. 2002;419:841-844
25. Harms E, Kivimae S, Young MW, Saez L. Posttranscriptional and posttranslational regulation of clock genes. J Biol Rhythms. 2004;19:361-373
26. Edmunds LN Jr, Funch RR. Circadian rhythm of cell division in Euglena: effects of random illumination regimen. Science. 1969;165:500-503
27. Chen Z, McKnight SL. A conserved DNA damage response pathway responsible for coupling the cell division cycle to the circadian and metabolic cycles. Cell Cycle. 2007;6: 2906-2912
28. Gomes JR, Pereira AA, Barth L, Silva JS, Leite ML, Wille AC, et al. Circadian variation of the cell proliferation in the jejunal epithelium of rats at weaning phase. Cell Prolif. 2005;38:147-152
29. Potten CS, Owen G, Roberts SA. The temporal and spatial changes in cell proliferation within the irradiated crypts of the murine small intestine. Int J Radiat Biol. 1990;57:185-199
30. Levi F, Filipski E, Iurisci I, Li XM, Innominato P. Crosstalks between circadian timing system and cell division cycle determine cancer biology and therapeutics. Cold Spring Harb Symp Quant Biol. 2007;72:465-475
31. Hunt T, Sassone-Corsi P. Riding tandem: circadian clocks and the cell cycle. Cell. 2007;129:461-464
32. Antoch MP, Kondratov RV. Circadian proteins and genoto-xic stress response. Circ Res. 2010;106:68-78.
33. Kondratov RV, Antoch MP. Circadian proteins in the regulation of cell cycle and genotoxic stress responses. Trends Cell Biol. 2007;17:311-317
34. Gery S, Koeffl er HP. Circadian rhythms and cancer. Cell Cycle. 2010;9(6):1097-1103
35. Miller BH, McDearmon EL, Panda S, Hayes KR, Zhang J, Andrews JL, et al. Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci USA. 2007;104:3342-3347
36. Lin KK, Kumar V, Geyfman M, Chudova D, Ihler AT, Smyth P, et al. Circadian clock genes contribute to the regulation of hair follicle cycling. PLoS Genet. 2009;5:e1000573.
37. Grechez-Cassiau A, Rayet B, Guillaumond F, Teboul M, Delaunay F. The circadian clock component BMAL1 is a critical regulator of p21WAF1/CIP1 expression and hepato-cyte proliferation. J Biol Chem. 2008;283:4535-4542
38. Deng C, Zhang P, Harper JW, Elledge SJ, Leder P. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell. 1995;82: 675-684
39. Mullenders J, Fabius AW, Madiredjo M, Bernards R, Bei-jersbergen RL. A large scale shRNA barcode screen identi-fi es the circadian clock component ARNTL as putative regulator of the p53 tumor suppressor pathway. PLoS One. 2009;4:e4798.
40. Antoch MP, Gorbacheva VY, Vykhovanets O, Toshkov IA, Kondratov RV, Kondratova AA, et al. Disruption of the cir-cadian clock due to the Clock mutation has discrete effects on aging and carcinogenesis. Cell Cycle. 2008;7:1197-1204
41. Taniguchi H, Fernandez AF, Setien F, Ropero S, Ballestar E, Villanueva A, et al. Epigenetic inactivation of the circadian clock gene BMAL1 in hematologic malignancies. Cancer Res. 2009;69:8447-8454
42. 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
43. Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, Smith AG, et al. Circadian cycling of the mouse liver tran-scriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol. 2002;12:540-550
44. Laiho M, Latonen L. Cell cycle control, DNA damage checkpoints and cancer. Ann Med. 2003;35:391-397
45. Li L, Zou L. Sensing, signaling, and responding to DNA damage: organization of the checkpoint pathways in mammalian cells. J Cell Biochem. 2005;94:298-306.
46. Niida H, Nakanishi M. DNA damage checkpoints in mammals. Mutagenesis. 2006;21:3-9.
47. Khanna KK, Lavin MF, Jackson SP, Mulhern TD. ATM, a central controller of cellular responses to DNA damage. Cell Death Differ. 2001;8:1052-1065
48. Kurz EU, Lees-Miller SP. DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair (Amst). 2004;3:889-900.
49. Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell. 2009;137:413-431
50. Unsal-Kacmaz K, Mullen TE, Kaufmann WK, Sancar A. Coupling of human circadian and cell cycles by the timeless protein. Mol Cell Biol. 2005;25:3109-3116
51. Gotter AL, Suppa C, Emanuel BS. Mammalian TIMELESS and Tipin are evolutionarily conserved replication fork-associated factors. J Mol Biol. 2007;366:36-52.
52. Oklejewicz M, Destici E, Tamanini F, Hut RA, Janssens R, van der Horst GT. Phase resetting of the mammalian circa-dian clock by DNA damage. Curr Biol. 2008;18:286-291
53. Gamsby JJ, Loros JJ, Dunlap JC. A phylogenetically conserved DNA damage response resets the circadian clock. J Biol Rhythms. 2009;24:193-202.
54. Mehra A, Baker CL, Loros JJ, Dunlap JC. Post-translational modifi cations in circadian rhythms. Trends Biochem Sci. 2009;34:483-490
55. Kondratov RV, Chernov MV, Kondratova AA, Gorbacheva VY, Gudkov AV, Antoch MP. BMAL1-dependent circadian oscillation of nuclear CLOCK: posttranslational events induced by dimerization of transcriptional activators of the mammalian clock system. Genes Dev. 2003;17:1921-1932
56. Hirayama J, Sahar S, Grimaldi B, Tamaru T, Takamatsu K, Nakahata Y, et al. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature. 2007;450:1086-1090
57. Cardone L, Hirayama J, Giordano F, Tamaru T, Palvimo JJ, Sassone-Corsi P. Circadian clock control by SUMOylation of BMAL1. Science. 2005;309:1390-1394
58. Lee J, Lee Y, Lee MJ, Park E, Kang SH, Chung CH, et al. Dual modifi cation of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex. Mol Cell Biol. 2008;28:6056-6065
59. Eide EJ, Vielhaber EL, Hinz WA, Virshup DM. The circadian regulatory proteins BMAL1 and cryptochromes are substrates of casein kinase Iepsilon. J Biol Chem. 2002;277: 17248-17254
60. Sahar S, Zocchi L, Kinoshita C, Borrelli E, Sassone-Corsi P. Regulation of BMAL1 protein stability and circadian function by GSK3beta-mediated phosphorylation. PLoS One. 2010;5:e8561.
61. Sanada K, Okano T, Fukada Y. Mitogen-activated protein kinase phosphorylates and negatively regulates basic helix-loop-helix-PAS transcription factor BMAL1. J Biol Chem. 2002;277:267-271
62. Spengler ML, Kuropatwinski KK, Schumer M, Antoch MP. A serine cluster mediates BMAL1-dependent CLOCK phosphorylation and degradation. Cell Cycle. 2009;8: 4138-4146
63. Robles MS, Boyault C, Knutti D, Padmanabhan K, Weitz CJ. Identifi cation of RACK1 and protein kinase Calpha as integral components of the mammalian circadian clock. Science. 2010;327:463-466
64. Doi M, Hirayama J, Sassone-Corsi P. Circadian regulator CLOCK is a histone acetyltransferase. Cell. 2006;125: 497-508.
65. Grimaldi B, Nakahata Y, Kaluzova M, Masubuchi S, Sassone-Corsi P. Chromatin remodeling, metabolism and circadian clocks: the interplay of CLOCK and SIRT1. Int J Biochem Cell Biol. 2009;41:81-86
66. Asher G, Gatfi eld D, Stratmann M, Reinke H, Dibner C, Kreppel F, et al. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell. 2008;134:317-328
67. Hofman MA, Swaab DF. Living by the clock: the circadian pacemaker in older people. Ageing Res Rev. 2006;5:33-51.
68. Kondratov RV. A role of the circadian system and circadian proteins in aging. Ageing Res Rev. 2007;6:12-27.
69. Ozturk N, Lee JH, Gaddameedhi S, Sancar A. Loss of cryp-tochrome reduces cancer risk in p53 mutant mice. Proc Natl Acad Sci USA. 2009;106:2841-2846
70. Green CB, Takahashi JS, Bass J. The meter of metabolism. Cell. 2008;134:728-742
71. Hardeland R, Coto-Montes A, Poeggeler B. Circadian rhythms, oxidative stress, and antioxidative defense mechanisms. Chronobiol Int. 2003;20:921-962
72. Kang TH, Reardon JT, Kemp M, Sancar A. Circadian oscillation of nucleotide excision repair in mammalian brain. Proc Natl Acad Sci USA. 2009;106:2864-2867
73. Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47-95.
74. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956;11:298-300.
75. Kondratov RV, Vykhovanets O, Kondratova AA, Antoch MP. Antioxidant N-acetyl-L-cysteine ameliorates symptoms of premature aging associated with the defi ciency of the circadian protein BMAL1. Aging (Albany NY). 2009;1:979-987
76. Guarente L, Picard F. Calorie restriction\the SIR2 connection. Cell. 2005;120:473-482
77. Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, et al. Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science. 2009;324: 651-654
78. Schernhammer ES, Kroenke CH, Laden F, Hankinson SE. Night work and risk of breast cancer. Epidemiology. 2006;17:108-111
79. Davis S, Mirick DK, Stevens RG. Night shift work, light at night, and risk of breast cancer. J Natl Cancer Inst. 2001;93: 1557-1562
80. Hansen J. Increased breast cancer risk among women who work predominantly at night. Epidemiology. 2001;12:74-77 (Pubitemid 32006465)
81. Rafnsson V, Hrafnkelsson J, Tulinius H. Incidence of cancer among commercial airline pilots. Occup Environ Med. 2000;57:175-179
82. Rafnsson V, Tulinius H, Jonasson JG, Hrafnkelsson J. Risk of breast cancer in female fl ight attendants: a population-based study (Iceland). Cancer Causes Control. 2001;12:95-101.
83. Pukkala E, Aspholm R, Auvinen A, Eliasch H, Gundestrup M, Haldorsen T, et al. Incidence of cancer among Nordic airline pilots over five decades: occupational cohort study. BMJ. 2002;325:567.
84. Pukkala E, Aspholm R, Auvinen A, Eliasch H, Gundestrup M, Haldorsen T, et al. Cancer incidence among 10,211 airline pilots: a Nordic study. Aviat Space Environ Med. 2003; 74:699-706.
85. Krstev S, Baris D, Stewart P, Dosemeci M, Swanson GM, Greenberg RS, et al. Occupational risk factors and prostate cancer in U.S. blacks and whites. Am J Ind Med. 1998;34: 421-430 (Pubitemid 28464888)
86. Zeegers MP, Friesema IH, Goldbohm RA, van den Brandt PA. A prospective study of occupation and prostate cancer risk. J Occup Environ Med. 2004;46:271-279
87. Kubo T, Ozasa K, Mikami K, Wakai K, Fujino Y, Watanabe Y, et al. Prospective cohort study of the risk of prostate cancer among rotating-shift workers: fi ndings from the Japan collaborative cohort study. Am J Epidemiol. 2006;164: 549-555
88. Pronk A, Ji BT, Shu XO, Xue S, Yang G, Li HL, et al. Night-shift work and breast cancer risk in a cohort of Chinese women. Am J Epidemiol. 2010;171:953-959
89. Pukkala E, Auvinen A, Wahlberg G. Incidence of cancer among Finnish airline cabin attendants, 1967-1992. BMJ. 1995;311:649-652
90. Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, Hirayama J, Chen D, et al. The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell. 2008;134:329-340
91. 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
92. Viswanathan AN, Hankinson SE, Schernhammer ES. Night shift work and the risk of endometrial cancer. Cancer Res. 2007;67:10618-10622
93. Schernhammer ES, Laden F, Speizer FE, Willett WC, Hunter DJ, Kawachi I, et al. Night-shift work and risk of colorectal cancer in the Nurses ' Health Study. J Natl Cancer Inst. 2003;95:825-828