Light-regulated translational control of circadian behavior by eIF4E phosphorylation

Nature Neuroscience

Volumn 18, Issue 6, 2015, Pages 855-862

  Cao, Ruifeng ^a   Gkogkas, Christos G ^b   De Zavalia, Nuria ^c   Blum, Ian D ^d   Yanagiya, Akiko ^a   Tsukumo, Yoshinori ^a   Xu, Haiyan ^e   Lee, Choogon ^f   Storch, Kai Florian ^d   Liu, Andrew C ^e   Amir, Shimon ^c   Sonenberg, Nahum ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c Concordia University ^*  (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e University of Memphis   (United States)

^f FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PER1 PROTEIN; PER2 PROTEIN; CIRCADIAN RHYTHM SIGNALING PROTEIN; PER1 PROTEIN, MOUSE; PER2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; HYPOTHALAMUS; IN VITRO STUDY; LIGHT; LIGHT EXPOSURE; MAMMAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RNA TRANSLATION; RUNNING; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; ANIMAL; ANIMAL BEHAVIOR; BRAIN CHEMISTRY; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; RADIATION RESPONSE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; CIRCADIAN RHYTHM; EUKARYOTIC INITIATION FACTOR-4E; GENE EXPRESSION REGULATION; LIGHT; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; PERIOD CIRCADIAN PROTEINS; PHOSPHORYLATION; SUPRACHIASMATIC NUCLEUS;

EID: 84929947130     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4010     Document Type: Article

References (47)

1. Rosbash, M. The implications of multiple circadian clock origins. PLoS Biol. 7, e62 (2009).
2. Reppert, S.M. & Weaver, D.R. Coordination of circadian timing in mammals. Nature 418, 935-941 (2002).
3. Colwell, C.S. Linking neural activity and molecular oscillations in the SCN. Nat. Rev. Neurosci. 12, 553-569 (2011).
4. Takahashi, J.S., Hong, H.K., Ko, C.H. & McDearmon, E.L. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 9, 764-775 (2008).
5. Herzog, E.D. Neurons and networks in daily rhythms. Nat. Rev. Neurosci. 8, 790-802 (2007).
6. Peirson, S. & Foster, R.G. Melanopsin: another way of signaling light. Neuron 49, 331-339 (2006).
7. Golombek, D.A. & Rosenstein, R.E. Physiology of circadian entrainment. Physiol. Rev. 90, 1063-1102 (2010).
8. Albrecht, U., Sun, Z.S., Eichele, G. & Lee, C.C. A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell 91, 1055-1064 (1997).
9. Shearman, L.P., Zylka, M.J., Weaver, D.R., Kolakowski, L.F. Jr. & Reppert, S.M. Two period homologs: circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron 19, 1261-1269 (1997).
10. Shigeyoshi, Y. et al. Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 91, 1043-1053 (1997).
11. Cao, R., Butcher, G.Q., Karelina, K., Arthur, J.S. & Obrietan, K. Mitogen-And stress-Activated protein kinase 1 modulates photic entrainment of the suprachiasmatic circadian clock. Eur. J. Neurosci. 37, 130-140 (2013).
12. Travnickova-Bendova, Z., Cermakian, N., Reppert, S.M. & Sassone-Corsi, P. Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity. Proc. Natl. Acad. Sci. USA 99, 7728-7733 (2002).
13. Sonenberg, N. & Hinnebusch, A.G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745 (2009).
14. Gingras, A.C., Raught, B. & Sonenberg, N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68, 913-963 (1999).
15. Cao, R. et al. Translational control of entrainment and synchrony of the suprachiasmatic circadian clock by mTOR/4E-BP1 signaling. Neuron 79, 712-724 (2013).
16. Buxade, M., Parra-Palau, J.L. & Proud, C.G. The Mnks: MAP kinase-interacting kinases (MAP kinase signal-integrating kinases). Front. Biosci. 13, 5359-5373 (2008).
17. Ueda, T., Watanabe-Fukunaga, R., Fukuyama, H., Nagata, S. & Fukunaga, R. Mnk2 and Mnk1 are essential for constitutive and inducible phosphorylation of eukaryotic initiation factor 4E but not for cell growth or development. Mol. Cell. Biol. 24, 6539-6549 (2004).
18. Furic, L. et al. eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. Proc. Natl. Acad. Sci. USA 107, 14134-14139 (2010).
19. Obrietan, K., Impey, S. & Storm, D.R. Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat. Neurosci. 1, 693-700 (1998).
20. Kelleher, R.J. III, Govindarajan, A., Jung, H.Y., Kang, H. & Tonegawa, S. Translational control by MAPK signaling in long-Term synaptic plasticity and memory. Cell 116, 467-479 (2004).
21. Favata, M.F. et al. Identification of a novel inhibitor of mitogen-Activated protein kinase kinase. J. Biol. Chem. 273, 18623-18632 (1998).
22. Knauf, U., Tschopp, C. & Gram, H. Negative regulation of protein translation by mitogen-Activated protein kinase-interacting kinases 1 and 2. Mol. Cell. Biol. 21, 5500-5511 (2001).
23. Harbour, V.L., Robinson, B. & Amir, S. Variations in daily expression of the circadian clock protein, PER2, in the rat limbic forebrain during stable entrainment to a long light cycle. J. Mol. Neurosci. 45, 154-161 (2011).
24. Akiyama, M. et al. Inhibition of light-or glutamate-induced mPer1 expression represses the phase shifts into the mouse circadian locomotor and suprachiasmatic firing rhythms. J. Neurosci. 19, 1115-1121 (1999).
25. Albrecht, U., Zheng, B., Larkin, D., Sun, Z.S. & Lee, C.C. MPer1 and mper2 are essential for normal resetting of the circadian clock. J. Biol. Rhythms 16, 100-104 (2001).
26. Hastings, M.H., Field, M.D., Maywood, E.S., Weaver, D.R. & Reppert, S.M. Differential regulation of mPER1 and mTIM proteins in the mouse suprachiasmatic nuclei: new insights into a core clock mechanism. J. Neurosci. 19, RC11 (1999).
27. Yan, L. & Silver, R. Resetting the brain clock: time course and localization of mPER1 and mPER2 protein expression in suprachiasmatic nuclei during phase shifts. Eur. J. Neurosci. 19, 1105-1109 (2004).
28. Cao, R., Li, A., Cho, H.Y., Lee, B. & Obrietan, K. Mammalian target of rapamycin signaling modulates photic entrainment of the suprachiasmatic circadian clock. J. Neurosci. 30, 6302-6314 (2010).
29. Balsalobre, A., Damiola, F. & Schibler, U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93, 929-937 (1998).
30. Lee, C., Etchegaray, J.P., Cagampang, F.R., Loudon, A.S. & Reppert, S.M. Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107, 855-867 (2001).
31. Konicek, B.W. et al. Therapeutic inhibition of MAP kinase interacting kinase blocks eukaryotic initiation factor 4E phosphorylation and suppresses outgrowth of experimental lung metastases. Cancer Res. 71, 1849-1857 (2011).
32. Tischkau, S.A.M.J., Tyan, S.H., Buchanan, G.F. & Gillette, M.U. Ca2+/cAMP response element-binding protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the suprachiasmatic nucleus circadian clock. J. Biol. Chem. 278, 718-723 (2003).
33. Gamble, K.L., Allen, G.C., Zhou, T. & McMahon, D.G. Gastrin-releasing peptide mediates light-like resetting of the suprachiasmatic nucleus circadian pacemaker through cAMP response element-binding protein and Per1 activation. J. Neurosci. 27, 12078-12087 (2007).
34. Ginty, D.D. et al. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260, 238-241 (1993).
35. Jagannath, A. et al. The CRTC1-SIK1 pathway regulates entrainment of the circadian clock. Cell 154, 1100-1111 (2013).
36. Sakamoto, K. et al. Clock and light regulation of the CREB coactivator CRTC1 in the suprachiasmatic circadian clock. J. Neurosci. 33, 9021-9027 (2013).
37. Cheng, H.Y. et al. microRNA modulation of circadian-clock period and entrainment. Neuron 54, 813-829 (2007).
38. Alvarez-Saavedra, M. et al. miRNA-132 orchestrates chromatin remodeling and translational control of the circadian clock. Hum. Mol. Genet. 20, 731-751 (2011).
39. Fustin, J.M. et al. RNA-methylation-dependent RNA processing controls the speed of the circadian clock. Cell 155, 793-806 (2013).
40. Meng, Q.J. et al. Setting clock speed in mammals: the CK1 epsilon tau mutation in mice accelerates circadian pacemakers by selectively destabilizing PERIOD proteins. Neuron 58, 78-88 (2008).
41. Kojima, S. et al. LARK activates posttranscriptional expression of an essential mammalian clock protein, PERIOD1. Proc. Natl. Acad. Sci. USA 104, 1859-1864 (2007).
42. Morf, J. et al. Cold-inducible RNA-binding protein modulates circadian gene expression posttranscriptionally. Science 338, 379-383 (2012).
43. Bradley, S., Narayanan, S. & Rosbash, M. NAT1/DAP5/p97 and atypical translational control in the Drosophila circadian oscillator. Genetics 192, 943-957 (2012).
44. Lim, C. et al. The novel gene twenty-four defines a critical translational step in the Drosophila clock. Nature 470, 399-403 (2011).
45. Lim, C. & Allada, R. ATAXIN-2 activates PERIOD translation to sustain circadian rhythms in Drosophila. Science 340, 875-879 (2013).
46. Zhang, Y., Ling, J., Yuan, C., Dubruille, R. & Emery, P. A role for Drosophila ATX2 in activation of PER translation and circadian behavior. Science 340, 879-882 (2013).
47. Thaben, P.F. & Westermark, P.O. Detecting rhythms in time series with RAIN. J. Biol. Rhythms 29, 391-400 (2014).