Post-translational Modifications are Required for Circadian Clock Regulation in Vertebrates

Author(s): Yoshimi Okamoto-Uchida, Junko Izawa, Akari Nishimura, Atsuhiko Hattori, Nobuo Suzuki, Jun Hirayama*.

Journal Name: Current Genomics

Volume 20 , Issue 5 , 2019

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Graphical Abstract:


Circadian clocks are intrinsic, time-tracking systems that bestow upon organisms a survival advantage. Under natural conditions, organisms are trained to follow a 24-h cycle under environmental time cues such as light to maximize their physiological efficiency. The exact timing of this rhythm is established via cell-autonomous oscillators called cellular clocks, which are controlled by transcription/ translation-based negative feedback loops. Studies using cell-based systems and genetic techniques have identified the molecular mechanisms that establish and maintain cellular clocks. One such mechanism, known as post-translational modification, regulates several aspects of these cellular clock components, including their stability, subcellular localization, transcriptional activity, and interaction with other proteins and signaling pathways. In addition, these mechanisms contribute to the integration of external signals into the cellular clock machinery. Here, we describe the post-translational modifications of cellular clock regulators that regulate circadian clocks in vertebrates.

Keywords: Circadian clock, cellular clock, clock protein, post-translational modification, transcription, clock gene.

Takahashi, J.S. Transcriptional architecture of the mammalian circadian clock. Nat. Rev. Genet., 2017, 18(3), 164-179.
[] [PMID: 27990019]
Okamura, H. Clock genes in cell clocks: Roles, actions, and mysteries. J. Biol. Rhythms, 2004, 19(5), 388-399.
[] [PMID: 15534319]
Sahar, S.; Sassone-Corsi, P. Metabolism and cancer: The circadian clock connection. Nat. Rev. Cancer, 2009, 9(12), 886-896.
[] [PMID: 19935677]
Uchida, Y.; Hirayama, J.; Nishina, H. A common origin: Signaling similarities in the regulation of the circadian clock and DNA damage responses. Biol. Pharm. Bull., 2010, 33(4), 535-544.
[] [PMID: 20410582]
Reppert, S.M.; Weaver, D.R. Coordination of circadian timing in mammals. Nature, 2002, 418(6901), 935-941.
[] [PMID: 12198538]
Schibler, U.; Sassone-Corsi, P. A web of circadian pacemakers. Cell, 2002, 111(7), 919-922.
[] [PMID: 12507418]
Dunlap, J.C. Molecular bases for circadian clocks. Cell, 1999, 96(2), 271-290.
[] [PMID: 9988221]
DeBruyne, J.P.; Weaver, D.R.; Reppert, S.M. CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat. Neurosci., 2007, 10(5), 543-545.
[] [PMID: 17417633]
Hirayama, J.; Sassone-Corsi, P. Structural and functional features of transcription factors controlling the circadian clock. Curr. Opin. Genet. Dev., 2005, 15(5), 548-556.
[] [PMID: 16095901]
Gallego, M.; Virshup, D.M. Post-translational modifications regulate the ticking of the circadian clock. Nat. Rev. Mol. Cell Biol., 2007, 8(2), 139-148.
[] [PMID: 17245414]
Yoshitane, H.; Honma, S.; Imamura, K.; Nakajima, H.; Nishide, S.Y.; Ono, D.; Kiyota, H.; Shinozaki, N.; Matsuki, H.; Wada, N.; Doi, H.; Hamada, T.; Honma, K.; Fukada, Y. JNK regulates the photic response of the mammalian circadian clock. EMBO Rep., 2012, 13(5), 455-461.
[] [PMID: 22441692]
Ma, Y.T.; Luo, H.; Guan, W.J.; Zhang, H.; Chen, C.; Wang, Z.; Li, J.D. O-GlcNAcylation of BMAL1 regulates circadian rhythms in NIH3T3 fibroblasts. Biochem. Biophys. Res. Commun., 2013, 431(3), 382-387.
[] [PMID: 23337503]
Kaasik, K.; Kivimäe, S.; Allen, J.J.; Chalkley, R.J.; Huang, Y.; Baer, K.; Kissel, H.; Burlingame, A.L.; Shokat, K.M.; Ptáček, L.J.; Fu, Y.H. Glucose sensor O-GlcNAcylation coordinates with phosphorylation to regulate circadian clock. Cell Metab., 2013, 17(2), 291-302.
[] [PMID: 23395175]
Lowrey, P.L.; Shimomura, K.; Antoch, M.P.; Yamazaki, S.; Zemenides, P.D.; Ralph, M.R.; Menaker, M.; Takahashi, J.S. Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science, 2000, 288(5465), 483-492.
[] [PMID: 10775102]
Toh, K.L.; Jones, C.R.; He, Y.; Eide, E.J.; Hinz, W.A.; Virshup, D.M.; Ptácek, L.J.; Fu, Y.H. An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science, 2001, 291(5506), 1040-1043.
[] [PMID: 11232563]
Xu, Y.; Padiath, Q.S.; Shapiro, R.E.; Jones, C.R.; Wu, S.C.; Saigoh, N.; Saigoh, K.; Ptácek, L.J.; Fu, Y.H. Functional consequences of a CKIdelta mutation causing familial advanced sleep phase syndrome. Nature, 2005, 434(7033), 640-644.
[] [PMID: 15800623]
Ebisawa, T.; Uchiyama, M.; Kajimura, N.; Mishima, K.; Kamei, Y.; Katoh, M.; Watanabe, T.; Sekimoto, M.; Shibui, K.; Kim, K.; Kudo, Y.; Ozeki, Y.; Sugishita, M.; Toyoshima, R.; Inoue, Y.; Yamada, N.; Nagase, T.; Ozaki, N.; Ohara, O.; Ishida, N.; Okawa, M.; Takahashi, K.; Yamauchi, T. Association of structural polymorphisms in the human period3 gene with delayed sleep phase syndrome. EMBO Rep., 2001, 2(4), 342-346.
[] [PMID: 11306557]
Akashi, M.; Tsuchiya, Y.; Yoshino, T.; Nishida, E. Control of intracellular dynamics of mammalian period proteins by casein kinase I epsilon (CKIepsilon) and CKIdelta in cultured cells. Mol. Cell. Biol., 2002, 22(6), 1693-1703.
[] [PMID: 11865049]
Takano, A.; Isojima, Y.; Nagai, K. Identification of mPer1 phosphorylation sites responsible for the nuclear entry. J. Biol. Chem., 2004, 279(31), 32578-32585.
[] [PMID: 15148313]
Yagita, K.; Yamanaka, I.; Koinuma, S.; Shigeyoshi, Y.; Uchiyama, Y. Mini screening of kinase inhibitors affecting period-length of mammalian cellular circadian clock. Acta Histochem. Cytochem., 2009, 42(3), 89-93.
[] [PMID: 19617956]
Kon, N.; Sugiyama, Y.; Yoshitane, H.; Kameshita, I.; Fukada, Y. Cell-based inhibitor screening identifies multiple protein kinases important for circadian clock oscillations. Commun. Integr. Biol., 2015, 8(4) e982405
[] [PMID: 26478783]
Maier, B.; Wendt, S.; Vanselow, J.T.; Wallach, T.; Reischl, S.; Oehmke, S.; Schlosser, A.; Kramer, A. A large-scale functional RNAi screen reveals a role for CK2 in the mammalian circadian clock. Genes Dev., 2009, 23(6), 708-718.
[] [PMID: 19299560]
Tamaru, T.; Hirayama, J.; Isojima, Y.; Nagai, K.; Norioka, S.; Takamatsu, K.; Sassone-Corsi, P. CK2alpha phosphorylates BMAL1 to regulate the mammalian clock. Nat. Struct. Mol. Biol., 2009, 16(4), 446-448.
[] [PMID: 19330005]
Uchida, Y.; Osaki, T.; Yamasaki, T.; Shimomura, T.; Hata, S.; Horikawa, K.; Shibata, S.; Todo, T.; Hirayama, J.; Nishina, H. Involvement of stress kinase mitogen-activated protein kinase kinase 7 in regulation of mammalian circadian clock. J. Biol. Chem., 2012, 287(11), 8318-8326.
[] [PMID: 22267733]
Kon, N.; Yoshikawa, T.; Honma, S.; Yamagata, Y.; Yoshitane, H.; Shimizu, K.; Sugiyama, Y.; Hara, C.; Kameshita, I.; Honma, K.; Fukada, Y. CaMKII is essential for the cellular clock and coupling between morning and evening behavioral rhythms. Genes Dev., 2014, 28(10), 1101-1110.
[] [PMID: 24831701]
Top, D.; Harms, E.; Syed, S.; Adams, E.L.; Saez, L. GSK-3 and CK2 kinases converge on timeless to regulate the master clock. Cell Rep., 2016, 16(2), 357-367.
[] [PMID: 27346344]
Zhang, E.E.; Liu, A.C.; Hirota, T.; Miraglia, L.J.; Welch, G.; Pongsawakul, P.Y.; Liu, X.; Atwood, A.; Huss, J.W., III; Janes, J.; Su, A.I.; Hogenesch, J.B.; Kay, S.A. A genome-wide RNAi screen for modifiers of the circadian clock in human cells. Cell, 2009, 139(1), 199-210.
[] [PMID: 19765810]
Wada, T.; Stepniak, E.; Hui, L.; Leibbrandt, A.; Katada, T.; Nishina, H.; Wagner, E.F.; Penninger, J.M. Antagonistic control of cell fates by JNK and p38-MAPK signaling. Cell Death Differ., 2008, 15(1), 89-93.
[] [PMID: 17762881]
Asaoka, Y.; Nishina, H. Diverse physiological functions of MKK4 and MKK7 during early embryogenesis. J. Biochem., 2010, 148(4), 393-401.
[] [PMID: 20801953]
Yamasaki, T.; Kawasaki, H.; Nishina, H. Diverse roles of JNK and MKK pathways in the brain. J. Signal Transduct., 2012, 2012459265
[] [PMID: 22496975]
Yamasaki, T.; Kawasaki, H.; Arakawa, S.; Shimizu, K.; Shimizu, S.; Reiner, O.; Okano, H.; Nishina, S.; Azuma, N.; Penninger, J.M.; Katada, T.; Nishina, H. Stress-activated protein kinase MKK7 regulates axon elongation in the developing cerebral cortex. J. Neurosci., 2011, 31(46), 16872-16883.
[] [PMID: 22090513]
Yamasaki, T.; Deki-Arima, N.; Kaneko, A.; Miyamura, N.; Iwatsuki, M.; Matsuoka, M.; Fujimori-Tonou, N.; Okamoto-Uchida, Y.; Hirayama, J.; Marth, J.D.; Yamanashi, Y.; Kawasaki, H.; Yamanaka, K.; Penninger, J.M.; Shibata, S.; Nishina, H. Age-dependent motor dysfunction due to neuron-specific disruption of stress-activated protein kinase MKK7. Sci. Rep., 2017, 7(1), 7348.
[] [PMID: 28779160]
Pizzio, G.A.; Hainich, E.C.; Ferreyra, G.A.; Coso, O.A.; Golombek, D.A. Circadian and photic regulation of ERK, JNK and p38 in the hamster SCN. Neuroreport, 2003, 14(11), 1417-1419.
[] [PMID: 12960755]
Chansard, M.; Molyneux, P.; Nomura, K.; Harrington, M.E.; Fukuhara, C. c-Jun N-terminal kinase inhibitor SP600125 modulates the period of mammalian circadian rhythms. Neuroscience, 2007, 145(3), 812-823.
[] [PMID: 17270352]
Terman, M.; Remé, C.E.; Wirz-Justice, A. The visual input stage of the mammalian circadian pacemaking system: II. The effect of light and drugs on retinal function. J. Biol. Rhythms, 1991, 6(1), 31-48.
[] [PMID: 1773078]
Carpenter, G.A.; Grossberg, S. A neural theory of circadian rhythms: Aschoff’s rule in diurnal and nocturnal mammals. Am. J. Physiol., 1984, 247(6 Pt 2), R1067-R1082.
[PMID: 6542316]
Müller, S.; Hoege, C.; Pyrowolakis, G.; Jentsch, S. SUMO, ubiquitin’s mysterious cousin. Nat. Rev. Mol. Cell Biol., 2001, 2(3), 202-210.
[] [PMID: 11265250]
Gill, G. Post-translational modification by the small ubiquitin-related modifier SUMO has big effects on transcription factor activity. Curr. Opin. Genet. Dev., 2003, 13(2), 108-113.
[] [PMID: 12672486]
Cardone, L.; Hirayama, J.; Giordano, F.; Tamaru, T.; Palvimo, J.J.; Sassone-Corsi, P. Circadian clock control by SUMOylation of BMAL1. Science, 2005, 309(5739), 1390-1394.
[] [PMID: 16109848]
Lee, J.; Lee, Y.; Lee, M.J.; Park, E.; Kang, S.H.; Chung, C.H.; Lee, K.H.; Kim, K. Dual modification of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex. Mol. Cell. Biol., 2008, 28(19), 6056-6065.
[] [PMID: 18644859]
Shen, M.; Kawamoto, T.; Yan, W.; Nakamasu, K.; Tamagami, M.; Koyano, Y.; Noshiro, M.; Kato, Y. Molecular characterization of the novel basic helix-loop-helix protein DEC1 expressed in differentiated human embryo chondrocytes. Biochem. Biophys. Res. Commun., 1997, 236(2), 294-298.
[] [PMID: 9240428]
Fujimoto, K.; Shen, M.; Noshiro, M.; Matsubara, K.; Shingu, S.; Honda, K.; Yoshida, E.; Suardita, K.; Matsuda, Y.; Kato, Y. Molecular cloning and characterization of DEC2, a new member of basic helix-loop-helix proteins. Biochem. Biophys. Res. Commun., 2001, 280(1), 164-171.
[] [PMID: 11162494]
Honma, S.; Kawamoto, T.; Takagi, Y.; Fujimoto, K.; Sato, F.; Noshiro, M.; Kato, Y.; Honma, K. Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature, 2002, 419(6909), 841-844.
[] [PMID: 12397359]
Hong, Y.; Xing, X.; Li, S.; Bi, H.; Yang, C.; Zhao, F.; Liu, Y.; Ao, X.; Chang, A.K.; Wu, H. SUMOylation of DEC1 protein regulates its transcriptional activity and enhances its stability. PLoS One, 2011, 6(8)e23046
[] [PMID: 21829689]
Cheung, P.; Allis, C.D.; Sassone-Corsi, P. Signaling to chromatin through histone modifications. Cell, 2000, 103(2), 263-271.
[] [PMID: 11057899]
Peterson, C.L.; Laniel, M.A. Histones and histone modifications. Curr. Biol., 2004, 14(14), R546-R551.
[] [PMID: 15268870]
Kouzarides, T. Chromatin modifications and their function. Cell, 2007, 128(4), 693-705.
[] [PMID: 17320507]
Strahl, B.D.; Allis, C.D. The language of covalent histone modifications. Nature, 2000, 403(6765), 41-45.
[] [PMID: 10638745]
Li, B.; Carey, M.; Workman, J.L. The role of chromatin during transcription. Cell, 2007, 128(4), 707-719.
[] [PMID: 17320508]
Ripperger, J.A.; Schibler, U. Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat. Genet., 2006, 38(3), 369-374.
[] [PMID: 16474407]
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(6105), 349-354.
[] [PMID: 22936566]
Sahar, S.; Sassone-Corsi, P. The epigenetic language of circadian clocks. Handb. Exp. Pharmacol., 2013, (217), 29-44.
[] [PMID: 23604474]
Doi, M.; Hirayama, J.; Sassone-Corsi, P. Circadian regulator CLOCK is a histone acetyltransferase. Cell, 2006, 125(3), 497-508.
[] [PMID: 16678094]
Hirayama, J.; Sahar, S.; Grimaldi, B.; Tamaru, T.; Takamatsu, K.; Nakahata, Y.; Sassone-Corsi, P. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature, 2007, 450(7172), 1086-1090.
[] [PMID: 18075593]
Hata, S.; Hirayama, J.; Kajiho, H.; Nakagawa, K.; Hata, Y.; Katada, T.; Furutani-Seiki, M.; Nishina, H. A novel acetylation cycle of transcription co-activator yes-associated protein that is downstream of Hippo pathway is triggered in response to SN2 alkylating agents. J. Biol. Chem., 2012, 287(26), 22089-22098.
[] [PMID: 22544757]
Brunet, A.; Sweeney, L.B.; Sturgill, J.F.; Chua, K.F.; Greer, P.L.; Lin, Y.; Tran, H.; Ross, S.E.; Mostoslavsky, R.; Cohen, H.Y.; Hu, L.S.; Cheng, H.L.; Jedrychowski, M.P.; Gygi, S.P.; Sinclair, D.A.; Alt, F.W.; Greenberg, M.E. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science, 2004, 303(5666), 2011-2015.
[] [PMID: 14976264]
Luo, J.; Nikolaev, A.Y.; Imai, S.; Chen, D.; Su, F.; Shiloh, A.; Guarente, L.; Gu, W. Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell, 2001, 107(2), 137-148.
[] [PMID: 11672522]
Nakahata, Y.; Kaluzova, M.; Grimaldi, B.; Sahar, S.; Hirayama, J.; Chen, D.; Guarente, L.P.; Sassone-Corsi, P. The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell, 2008, 134(2), 329-340.
[] [PMID: 18662547]
Asher, G.; Gatfield, D.; Stratmann, M.; Reinke, H.; Dibner, C.; Kreppel, F.; Mostoslavsky, R.; Alt, F.W.; Schibler, U. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell, 2008, 134(2), 317-328.
[] [PMID: 18662546]
Bellet, M.M.; Nakahata, Y.; Boudjelal, M.; Watts, E.; Mossakowska, D.E.; Edwards, K.A.; Cervantes, M.; Astarita, G.; Loh, C.; Ellis, J.L.; Vlasuk, G.P.; Sassone-Corsi, P. Pharmacological modulation of circadian rhythms by synthetic activators of the deacetylase SIRT1. Proc. Natl. Acad. Sci. USA, 2013, 110(9), 3333-3338.
[] [PMID: 23341587]
Hanover, J.A.; Krause, M.W.; Love, D.C. Bittersweet memories: Linking metabolism to epigenetics through O-GlcNAcylation. Nat. Rev. Mol. Cell Biol., 2012, 13(5), 312-321.
[] [PMID: 22522719]
Hart, G.W.; Slawson, C.; Ramirez-Correa, G.; Lagerlof, O. Cross talk between O-GlcNAcylation and phosphorylation: Roles in signaling, transcription, and chronic disease. Annu. Rev. Biochem., 2011, 80, 825-858.
[] [PMID: 21391816]
Li, M.D.; Ruan, H.B.; Hughes, M.E.; Lee, J.S.; Singh, J.P.; Jones, S.P.; Nitabach, M.N.; Yang, X. O-GlcNAc signaling entrains the circadian clock by inhibiting BMAL1/CLOCK ubiquitination. Cell Metab., 2013, 17(2), 303-310.
[] [PMID: 23395176]
Asher, G.; Reinke, H.; Altmeyer, M.; Gutierrez-Arcelus, M.; Hottiger, M.O.; Schibler, U. Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell, 2010, 142(6), 943-953.
[] [PMID: 20832105]
Schmutz, I.; Ripperger, J.A.; Baeriswyl-Aebischer, S.; Albrecht, U. The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors. Genes Dev., 2010, 24(4), 345-357.
[] [PMID: 20159955]
Grimaldi, B.; Bellet, M.M.; Katada, S.; Astarita, G.; Hirayama, J.; Amin, R.H.; Granneman, J.G.; Piomelli, D.; Leff, T.; Sassone-Corsi, P. PER2 controls lipid metabolism by direct regulation of PPARγ. Cell Metab., 2010, 12(5), 509-520.
[] [PMID: 21035761]
Wang, M.; Zhong, Z.; Zhong, Y.; Zhang, W.; Wang, H. The zebrafish period2 protein positively regulates the circadian clock through mediation of retinoic acid receptor (RAR)-related orphan receptor α (Rorα). J. Biol. Chem., 2015, 290(7), 4367-4382.
[] [PMID: 25544291]
Peek, C.B.; Levine, D.C.; Cedernaes, J.; Taguchi, A.; Kobayashi, Y.; Tsai, S.J.; Bonar, N.A.; McNulty, M.R.; Ramsey, K.M.; Bass, J. Circadian clock interaction with HIF1α mediates oxygenic metabolism and anaerobic glycolysis in skeletal muscle. Cell Metab., 2017, 25(1), 86-92.
[] [PMID: 27773696]
Wu, Y.; Tang, D.; Liu, N.; Xiong, W.; Huang, H.; Li, Y.; Ma, Z.; Zhao, H.; Chen, P.; Qi, X.; Zhang, E.E. Reciprocal regulation between the circadian clock and hypoxia signaling at the genome level in mammals. Cell Metab., 2017, 25(1), 73-85.
[] [PMID: 27773697]
Kondratov, R.V.; Kondratova, A.A.; Gorbacheva, V.Y.; Vykhovanets, O.V.; Antoch, M.P. Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev., 2006, 20(14), 1868-1873.
[] [PMID: 16847346]
Nakahata, Y.; Yasukawa, S.; Khaidizar, F.D.; Shimba, S.; Matsui, T.; Bessho, Y. Bmal1-deficient mouse fibroblast cells do not provide premature cellular senescence in vitro. Chronobiol. Int., 2018, 35(5), 730-738.
[] [PMID: 29372841]
Ong, A.L.C.; Ramasamy, T.S. Role of Sirtuin1-p53 regulatory axis in aging, cancer and cellular reprogramming. Ageing Res. Rev., 2018, 43, 64-80.
[] [PMID: 29476819]
Kondratov, R.V.; Gorbacheva, V.Y.; Antoch, M.P. The role of mammalian circadian proteins in normal physiology and genotoxic stress responses. Curr. Top. Dev. Biol., 2007, 78, 173-216.
[] [PMID: 17338917]
Hirayama, J.; Cho, S.; Sassone-Corsi, P. Circadian control by the reduction/oxidation pathway: Catalase represses light-dependent clock gene expression in the zebrafish. Proc. Natl. Acad. Sci. USA, 2007, 104(40), 15747-15752.
[] [PMID: 17898172]
Osaki, T.; Uchida, Y.; Hirayama, J.; Nishina, H. Diphenyleneiodonium chloride, an inhibitor of reduced nicotinamide adenine dinucleotide phosphate oxidase, suppresses light-dependent induction of clock and DNA repair genes in zebrafish. Biol. Pharm. Bull., 2011, 34(8), 1343-1347.
[] [PMID: 21804230]
Pagano, C.; Siauciunaite, R.; Idda, M.L.; Ruggiero, G.; Ceinos, R.M.; Pagano, M.; Frigato, E.; Bertolucci, C.; Foulkes, N.S.; Vallone, D. Evolution shapes the responsiveness of the D-box enhancer element to light and reactive oxygen species in vertebrates. Sci. Rep., 2018, 8(1), 13180.
[] [PMID: 30181539]
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(5643), 255-259.
[] [PMID: 12934012]
Dekens, M.P.; Santoriello, C.; Vallone, D.; Grassi, G.; Whitmore, D.; Foulkes, N.S. Light regulates the cell cycle in zebrafish. Curr. Biol., 2003, 13(23), 2051-2057.
[] [PMID: 14653994]
Tsuchiya, Y.; Akashi, M.; Matsuda, M.; Goto, K.; Miyata, Y.; Node, K.; Nishida, E. Involvement of the protein kinase CK2 in the regulation of mammalian circadian rhythms. Sci. Signal., 2009, 2(73), ra26.
[] [PMID: 19491384]
Meggio, F.; Pinna, L.A. One-thousand-and-one substrates of protein kinase CK2? FASEB J., 2003, 17(3), 349-368.
[] [PMID: 12631575]
Gorospe, M.; de Cabo, R. AsSIRTing the DNA damage response. Trends Cell Biol., 2008, 18(2), 77-83.
[] [PMID: 18215521]

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Year: 2019
Page: [332 - 339]
Pages: 8
DOI: 10.2174/1389202919666191014094349
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