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REVIEW ARTICLE

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

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Pages 404-415 | Received 13 Apr 2010, Accepted 26 May 2010, Published online: 23 Jun 2010

References

  • Lowrey PL, Takahashi JS. Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet. 2004;5:407–41.
  • Gachon F, Nagoshi E, Brown SA, Ripperger J, Schibler U. The mammalian circadian timing system: from gene expression to physiology. Chromosoma. 2004;113:103–12.
  • Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, . Coordinated transcription of key pathways in the mouse by the circadian clock. Cell. 2002;109:307–20.
  • Dardente H, Cermakian N. Molecular circadian rhythms in central and peripheral clocks in mammals. Chronobiol Int. 2007;24:195–213.
  • McClung CA. Circadian genes, rhythms and the biology of mood disorders. Pharmacol Ther. 2007;114:222–32.
  • Laposky AD, Bass J, Kohsaka A, Turek FW. Sleep and circadian rhythms: key components in the regulation of energy metabolism. FEBS Lett. 2008;582:142–51.
  • Reilly DF, Westgate EJ, FitzGerald GA. Peripheral circadian clocks in the vasculature. Arterioscler Thromb Vasc Biol. 2007;27:1694–705.
  • Filipski E, Li XM, Levi F. Disruption of circadian coordination and malignant growth. Cancer Causes Control. 2006; 17:509–14.
  • Curtis AM, Fitzgerald GA. Central and peripheral clocks in cardiovascular and metabolic function. Ann Med. 2006; 38:552–9.
  • 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: 150–62.
  • 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.
  • Kondratov RV, Kondratova AA, Gorbacheva VY, Vykhovanets OV, Antoch MP. Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 2006;20:1868–73.
  • Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, . Obesity and metabolic syndrome in circadian Clock mutant mice. Science. 2005;308:1043–5.
  • Schibler U, Sassone-Corsi P. A web of circadian pacemakers. Cell. 2002;111:919–22.
  • Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, . Role of the CLOCK protein in the mammalian circadian mechanism. Science. 1998;280: 1564–9.
  • Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, . Mop3 is an essential component of the master circadian pacemaker in mammals. Cell. 2000;103:1009–17.
  • Antoch MP, Song EJ, Chang AM, Vitaterna MH, Zhao Y, Wilsbacher LD, . Functional identification of the mouse circadian Clock gene by transgenic BAC rescue. Cell. 1997;89:655–67.
  • King DP, Zhao Y, Sangoram AM, Wilsbacher LD, Tanaka M, Antoch MP, . Positional cloning of the mouse circadian clock gene. Cell. 1997;89:641–53.
  • Hirayama J, Sassone-Corsi P. Structural and functional features of transcription factors controlling the circadian clock. Curr Opin Genet Dev. 2005;15:548–56.
  • Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, Jin X, . mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell. 1999;98:193–205.
  • Griffin EA Jr, Staknis D, Weitz CJ. Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science. 1999;286:768–71.
  • Sato TK, Panda S, Miraglia LJ, Reyes TM, Rudic RD, McNamara P, . A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron. 2004;43:527–37.
  • Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, . The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell. 2002; 110:251–60.
  • Honma S, Kawamoto T, Takagi Y, Fujimoto K, Sato F, Noshiro M, . Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature. 2002;419:841–4.
  • Harms E, Kivimae S, Young MW, Saez L. Posttranscriptional and posttranslational regulation of clock genes. J Biol Rhythms. 2004;19:361–73.
  • Edmunds LN Jr, Funch RR. Circadian rhythm of cell division in Euglena: effects of random illumination regimen. Science. 1969;165:500–3.
  • 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: 2906–12.
  • Gomes JR, Pereira AA, Barth L, Silva JS, Leite ML, Wille AC, . Circadian variation of the cell proliferation in the jejunal epithelium of rats at weaning phase. Cell Prolif. 2005;38:147–52.
  • 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;57:185–99.
  • Levi F, Filipski E, Iurisci I, Li XM, Innominato P. Cross-talks between circadian timing system and cell division cycle determine cancer biology and therapeutics. Cold Spring Harb Symp Quant Biol. 2007;72:465–75.
  • Hunt T, Sassone-Corsi P. Riding tandem: circadian clocks and the cell cycle. Cell. 2007;129:461–4.
  • Antoch MP, Kondratov RV. Circadian proteins and genotoxic stress response. Circ Res. 2010;106:68–78.
  • Kondratov RV, Antoch MP. Circadian proteins in the regulation of cell cycle and genotoxic stress responses. Trends Cell Biol. 2007;17:311–7.
  • Gery S, Koeffler HP. Circadian rhythms and cancer. Cell Cycle. 2010;9(6):1097–103.
  • Miller BH, McDearmon EL, Panda S, Hayes KR, Zhang J, Andrews JL, . Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci U S A. 2007;104:3342–7.
  • Lin KK, Kumar V, Geyfman M, Chudova D, Ihler AT, Smyth P, . Circadian clock genes contribute to the regulation of hair follicle cycling. PLoS Genet. 2009;5:e1000573.
  • 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 hepatocyte proliferation. J Biol Chem. 2008;283:4535–42.
  • 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: 675–84.
  • Mullenders J, Fabius AW, Madiredjo M, Bernards R, Beijersbergen RL. 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.
  • Antoch MP, Gorbacheva VY, Vykhovanets O, Toshkov IA, Kondratov RV, Kondratova AA, . Disruption of the circadian clock due to the Clock mutation has discrete effects on aging and carcinogenesis. Cell Cycle. 2008;7:1197–204.
  • Taniguchi H, Fernandez AF, Setien F, Ropero S, Ballestar E, Villanueva A, . Epigenetic inactivation of the circadian clock gene BMAL1 in hematologic malignancies. Cancer Res. 2009;69:8447–54.
  • 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.
  • Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, Smith AG, . Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol. 2002;12:540–50.
  • Laiho M, Latonen L. Cell cycle control, DNA damage checkpoints and cancer. Ann Med. 2003;35:391–7.
  • 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.
  • Niida H, Nakanishi M. DNA damage checkpoints in mammals. Mutagenesis. 2006;21:3–9.
  • Khanna KK, Lavin MF, Jackson SP, Mulhern TD. ATM, a central controller of cellular responses to DNA damage. Cell Death Differ. 2001;8:1052–65.
  • Kurz EU, Lees-Miller SP. DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair (Amst). 2004;3:889–900.
  • Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell. 2009;137:413–31.
  • Unsal-Kacmaz K, Mullen TE, Kaufmann WK, Sancar A. Coupling of human circadian and cell cycles by the timeless protein. Mol Cell Biol. 2005;25:3109–16.
  • Gotter AL, Suppa C, Emanuel BS. Mammalian TIMELESS and Tipin are evolutionarily conserved replication fork-associated factors. J Mol Biol. 2007;366:36–52.
  • Oklejewicz M, Destici E, Tamanini F, Hut RA, Janssens R, van der Horst GT. Phase resetting of the mammalian circadian clock by DNA damage. Curr Biol. 2008;18:286–91.
  • Gamsby JJ, Loros JJ, Dunlap JC. A phylogenetically conserved DNA damage response resets the circadian clock. J Biol Rhythms. 2009;24:193–202.
  • Mehra A, Baker CL, Loros JJ, Dunlap JC. Post-translational modifications in circadian rhythms. Trends Biochem Sci. 2009;34:483–90.
  • 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;17:1921–32.
  • Hirayama J, Sahar S, Grimaldi B, Tamaru T, Takamatsu K, Nakahata Y, . CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature. 2007;450:1086–90.
  • Cardone L, Hirayama J, Giordano F, Tamaru T, Palvimo JJ, Sassone-Corsi P. Circadian clock control by SUMOylation of BMAL1. Science. 2005;309:1390–4.
  • Lee J, Lee Y, Lee MJ, Park E, Kang SH, Chung CH, . Dual modification of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex. Mol Cell Biol. 2008;28:6056–65.
  • 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: 17248–54.
  • 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.
  • 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;277:267–71.
  • Spengler ML, Kuropatwinski KK, Schumer M, Antoch MP. A serine cluster mediates BMAL1-dependent CLOCK phosphorylation and degradation. Cell Cycle. 2009;8: 4138–46.
  • Robles MS, Boyault C, Knutti D, Padmanabhan K, Weitz CJ. Identification of RACK1 and protein kinase Calpha as integral components of the mammalian circadian clock. Science. 2010;327:463–6.
  • Doi M, Hirayama J, Sassone-Corsi P. Circadian regulator CLOCK is a histone acetyltransferase. Cell. 2006;125: 497–508.
  • 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;41:81–6.
  • Asher G, Gatfield D, Stratmann M, Reinke H, Dibner C, Kreppel F, . SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell. 2008;134:317–28.
  • Hofman MA, Swaab DF. Living by the clock: the circadian pacemaker in older people. Ageing Res Rev. 2006;5:33–51.
  • Kondratov RV. A role of the circadian system and circadian proteins in aging. Ageing Res Rev. 2007;6:12–27.
  • Ozturk N, Lee JH, Gaddameedhi S, Sancar A. Loss of cryptochrome reduces cancer risk in p53 mutant mice. Proc Natl Acad Sci U S A. 2009;106:2841–6.
  • Green CB, Takahashi JS, Bass J. The meter of metabolism. Cell. 2008;134:728–42.
  • Hardeland R, Coto-Montes A, Poeggeler B. Circadian rhythms, oxidative stress, and antioxidative defense mechanisms. Chronobiol Int. 2003;20:921–62.
  • Kang TH, Reardon JT, Kemp M, Sancar A. Circadian oscillation of nucleotide excision repair in mammalian brain. Proc Natl Acad Sci U S A. 2009;106:2864–7.
  • Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47–95.
  • Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956;11:298–300.
  • Kondratov RV, Vykhovanets O, Kondratova AA, Antoch MP. Antioxidant N-acetyl-L-cysteine ameliorates symptoms of premature aging associated with the deficiency of the circadian protein BMAL1. Aging (Albany NY). 2009;1:979–87.
  • Guarente L, Picard F. Calorie restriction—the SIR2 connection. Cell. 2005;120:473–82.
  • Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, . Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science. 2009;324: 651–4.
  • Schernhammer ES, Kroenke CH, Laden F, Hankinson SE. Night work and risk of breast cancer. Epidemiology. 2006;17:108–11.
  • Davis S, Mirick DK, Stevens RG. Night shift work, light at night, and risk of breast cancer. J Natl Cancer Inst. 2001;93: 1557–62.
  • Hansen J. Increased breast cancer risk among women who work predominantly at night. Epidemiology. 2001;12:74–7.
  • Rafnsson V, Hrafnkelsson J, Tulinius H. Incidence of cancer among commercial airline pilots. Occup Environ Med. 2000;57:175–9.
  • Rafnsson V, Tulinius H, Jonasson JG, Hrafnkelsson J. Risk of breast cancer in female flight attendants: a population-based study (Iceland). Cancer Causes Control. 2001;12:95–101.
  • Pukkala E, Aspholm R, Auvinen A, Eliasch H, Gundestrup M, Haldorsen T, . Incidence of cancer among Nordic airline pilots over five decades: occupational cohort study. BMJ. 2002;325:567.
  • Pukkala E, Aspholm R, Auvinen A, Eliasch H, Gundestrup M, Haldorsen T, . Cancer incidence among 10,211 airline pilots: a Nordic study. Aviat Space Environ Med. 2003; 74:699–706.
  • Krstev S, Baris D, Stewart P, Dosemeci M, Swanson GM, Greenberg RS, . Occupational risk factors and prostate cancer in U.S. blacks and whites. Am J Ind Med. 1998;34: 421–30.
  • Zeegers MP, Friesema IH, Goldbohm RA, van den Brandt PA. A prospective study of occupation and prostate cancer risk. J Occup Environ Med. 2004;46:271–9.
  • Kubo T, Ozasa K, Mikami K, Wakai K, Fujino Y, Watanabe Y, . Prospective cohort study of the risk of prostate cancer among rotating-shift workers: findings from the Japan collaborative cohort study. Am J Epidemiol. 2006;164: 549–55.
  • Pronk A, Ji BT, Shu XO, Xue S, Yang G, Li HL, . Night-shift work and breast cancer risk in a cohort of Chinese women. Am J Epidemiol. 2010;171:953–9.
  • Pukkala E, Auvinen A, Wahlberg G. Incidence of cancer among Finnish airline cabin attendants, 1967–92. BMJ. 1995;311:649–52.
  • Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, Hirayama J, Chen D, . The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell. 2008;134:329–40.
  • Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P. Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science. 2009;324:654–7.
  • Viswanathan AN, Hankinson SE, Schernhammer ES. Night shift work and the risk of endometrial cancer. Cancer Res. 2007;67:10618–22.
  • Schernhammer ES, Laden F, Speizer FE, Willett WC, Hunter DJ, Kawachi I, . Night-shift work and risk of colorectal cancer in the Nurses’ Health Study. J Natl Cancer Inst. 2003;95:825–8.

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