Translational control of entrainment and synchrony of the suprachiasmatic circadian clock by mTOR/4E-BP1 signaling

Neuron

Volumn 79, Issue 4, 2013, Pages 712-724

  Cao, Ruifeng ^a   Robinson, Barry ^b   Xu, Haiyan ^c   Gkogkas, Christos ^a   Khoutorsky, Arkady ^a   Alain, Tommy ^a   Yanagiya, Akiko ^a   Nevarko, Tatiana ^a   Liu, AndrewC ^c   Amir, Shimon ^b   Sonenberg, Nahum ^a  

^a MCGILL UNIVERSITY   (Canada)

^b and Applied Physiology   (Canada)

^c University of Memphis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CIRCADIAN RHYTHM; CONTROLLED STUDY; EIF4EBP1 GENE; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; EMBRYO; ENZYME ACTIVITY; ENZYME REGULATION; GENE; GENE INACTIVATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA TRANSLATION; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS;

ANIMALS; ANTHRAQUINONES; BUTADIENES; CARRIER PROTEINS; CELL LINE, TUMOR; CIRCADIAN RHYTHM; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; INDOLES; LIGHT; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRILES; PERIOD CIRCADIAN PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PURINES; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SIROLIMUS; SUPRACHIASMATIC NUCLEUS; TOR SERINE-THREONINE KINASES; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84882626496     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.06.026     Document Type: Article

References (73)

1. Abraham U., Granada A.E., Westermark P.O., Heine M., Kramer A., Herzel H. Coupling governs entrainment range of circadian clocks. Mol. Syst. Biol. 2010, 6:438.
2. Abrahamson E.E., Moore R.Y. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res. 2001, 916:172-191.
3. Albus H., Vansteensel M.J., Michel S., Block G.D., Meijer J.H. A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr. Biol. 2005, 15:886-893.
4. Amir S., Lamont E.W., Robinson B., Stewart J. A circadian rhythm in the expression of PERIOD2 protein reveals a novel SCN-controlled oscillator in the oval nucleus of the bed nucleus of the stria terminalis. J.Neurosci. 2004, 24:781-790.
5. An, S. (2011a). The Roles of Vasoactive Intestinal Polypeptide in Circadian Entrainment of Suprachiasmatic Nucleus. Doctoral dissertation, Washington University in St. Louis: ProQuest/UMI. (pqid:2342376571.).
6. An S., Irwin R.P., Allen C.N., Tsai C., Herzog E.D. Vasoactive intestinal polypeptide requires parallel changes in adenylate cyclase and phospholipase C to entrain circadian rhythms to a predictable phase. J.Neurophysiol. 2011, 105:2289-2296.
7. An S., Tsai C., Ronecker J., Bayly A., Herzog E.D. Spatiotemporal distribution of vasoactive intestinal polypeptide receptor 2 inmouse suprachiasmatic nucleus. J.Comp. Neurol. 2012, 520:2730-2741.
8. Antle M.C., Silver R. Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci. 2005, 28:145-151.
9. Aton S.J., Herzog E.D. Come together, right...now: synchronization of rhythms in a mammalian circadian clock. Neuron 2005, 48:531-534.
10. Aton S.J., Colwell C.S., Harmar A.J., Waschek J., Herzog E.D. Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat. Neurosci. 2005, 8:476-483.
11. Bradley S., Narayanan S., Rosbash M. NAT1/DAP5/p97 and atypical translational control in the Drosophila Circadian Oscillator. Genetics 2012, 192:943-957.
12. Cao R., Obrietan K. mTOR Signaling and Entrainment of the Mammalian Circadian Clock. Mol Cell Pharmacol 2010, 2:125-130.
13. Cao R., Lee B., Cho H.Y., Saklayen S., Obrietan K. Photic regulation of the mTOR signaling pathway in the suprachiasmatic circadian clock. Mol. Cell. Neurosci. 2008, 38:312-324.
14. Cao R., Li A., Cho H.Y. mTOR signaling in epileptogenesis: too much of a good thing?. J.Neurosci. 2009, 29:12372-12373.
15. 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. 2010, 30:6302-6314.
16. Cao R., Anderson F.E., Jung Y.J., Dziema H., Obrietan K. Circadian regulation of mammalian target of rapamycin signaling in the mouse suprachiasmatic nucleus. Neuroscience 2011, 181:79-88.
17. Colwell C.S., Michel S., Itri J., Rodriguez W., Tam J., Lelievre V., Hu Z., Liu X., Waschek J.A. Disrupted circadian rhythms in VIP- and PHI-deficient mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 285:R939-R949.
18. Costa-Mattioli M., Sossin W.S., Klann E., Sonenberg N. Translational control of long-lasting synaptic plasticity and memory. Neuron 2009, 61:10-26.
19. Cota D., Proulx K., Smith K.A., Kozma S.C., Thomas G., Woods S.C., Seeley R.J. Hypothalamic mTOR signaling regulates food intake. Science 2006, 312:927-930.
20. Cutler D.J., Haraura M., Reed H.E., Shen S., Sheward W.J., Morrison C.F., Marston H.M., Harmar A.J., Piggins H.D. The mouse VPAC2 receptor confers suprachiasmatic nuclei cellular rhythmicity and responsiveness to vasoactive intestinal polypeptide invitro. Eur. J. Neurosci. 2003, 17:197-204.
21. Daan S., Pittendrigh C.S. A Functional Analysis of Circadian Pacemakers in Nocturnal Rodents III. Heavy Water and Constant Light: Homeostasis of Frequency?. J.Comp. Physiol. 1976, 106:253-266.
22. Davidson A.J., Castanon-Cervantes O., Leise T.L., Molyneux P.C., Harrington M.E. Visualizing jet lag in the mouse suprachiasmatic nucleus and peripheral circadian timing system. Eur. J. Neurosci. 2009, 29:171-180.
23. de la Iglesia H.O., Cambras T., Schwartz W.J., Díez-Noguera A. Forced desynchronization of dual circadian oscillators within the rat suprachiasmatic nucleus. Curr. Biol. 2004, 14:796-800.
24. Dowling R.J., Topisirovic I., Alain T., Bidinosti M., Fonseca B.D., Petroulakis E., Wang X., Larsson O., Selvaraj A., Liu Y., et al. mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 2010, 328:1172-1176.
25. Field M.D., Maywood E.S., O'Brien J.A., Weaver D.R., Reppert S.M., Hastings M.H. Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of the circadian clockwork and resetting mechanisms. Neuron 2000, 25:437-447.
26. Gingras A.C., Gygi S.P., Raught B., Polakiewicz R.D., Abraham R.T., Hoekstra M.F., Aebersold R., Sonenberg N. Regulation of4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev. 1999, 13:1422-1437.
27. Gkogkas C.G., Khoutorsky A., Ran I., Rampakakis E., Nevarko T., Weatherill D.B., Vasuta C., Yee S., Truitt M., Dallaire P., et al. Autism-related deficits via dysregulated eIF4E-dependent translational control. Nature 2013, 493:371-377.
28. Gozes I., Brenneman D.E. VIP: molecular biology and neurobiological function. Mol. Neurobiol. 1989, 3:201-236.
29. Gozes I., Lilling G., Glazer R., Ticher A., Ashkenazi I.E., Davidson A., Rubinraut S., Fridkin M., Brenneman D.E. Superactive lipophilic peptides discriminate multiple vasoactive intestinal peptide receptors. J.Pharmacol. Exp. Ther. 1995, 273:161-167.
30. Harmar A.J., Marston H.M., Shen S., Spratt C., West K.M., Sheward W.J., Morrison C.F., Dorin J.R., Piggins H.D., Reubi J.C., et al. The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 2002, 109:497-508.
31. 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. 1999, 19:RC11.
32. Herzog E.D., Takahashi J.S., Block G.D. Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nat. Neurosci. 1998, 1:708-713.
33. Hood S., Cassidy P., Cossette M.P., Weigl Y., Verwey M., Robinson B., Stewart J., Amir S. Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors. J.Neurosci. 2010, 30:14046-14058.
34. Jouffe C., Cretenet G., Symul L., Martin E., Atger F., Naef F., Gachon F. The circadian clock coordinates ribosome biogenesis. PLoS Biol. 2013, 11:e1001455.
35. Khan S.K., Xu H., Ukai-Tadenuma M., Burton B., Wang Y., Ueda H.R., Liu A.C. Identification of a novel cryptochrome differentiating domain required for feedback repression in circadian clock function. J.Biol. Chem. 2012, 287:25917-25926.
36. Kornhauser J.M., Nelson D.E., Mayo K.E., Takahashi J.S. Regulation of jun-B messenger RNA and AP-1 activity by light and a circadian clock. Science 1992, 255:1581-1584.
37. Laplante M., Sabatini D.M. mTOR signaling in growth control anddisease. Cell 2012, 149:274-293.
38. Lee C. Protein extraction from mammalian tissues. Methods Mol. Biol. 2007, 362:385-389.
39. Liu C., Reppert S.M. GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 2000, 25:123-128.
40. Liu A.C., Lewis W.G., Kay S.A. Mammalian circadian signaling networks and therapeutic targets. Nat. Chem. Biol. 2007, 3:630-639.
41. Liu A.C., Welsh D.K., Ko C.H., Tran H.G., Zhang E.E., Priest A.A., Buhr E.D., Singer O., Meeker K., Verma I.M., et al. Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 2007, 129:605-616.
42. Long M.A., Jutras M.J., Connors B.W., Burwell R.D. Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat. Neurosci. 2005, 8:61-66.
43. Maywood E.S., Reddy A.B., Wong G.K., O'Neill J.S., O'Brien J.A., McMahon D.G., Harmar A.J., Okamura H., Hastings M.H. Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr. Biol. 2006, 16:599-605.
44. Maywood E.S., Chesham J.E., O'Brien J.A., Hastings M.H. A diversity of paracrine signals sustains molecular circadian cycling in suprachiasmatic nucleus circuits. Proc. Natl. Acad. Sci. USA 2011, 108:14306-14311.
45. Meyer-Spasche A., Piggins H.D. Vasoactive intestinal polypeptide phase-advances the rat suprachiasmatic nuclei circadian pacemaker invitro via protein kinase A and mitogen-activated protein kinase. Neurosci. Lett. 2004, 358:91-94.
46. Nagano M., Adachi A., Nakahama K., Nakamura T., Tamada M., Meyer-Bernstein E., Sehgal A., Shigeyoshi Y. An abrupt shift in the day/night cycle causes desynchrony in the mammalian circadian center. J.Neurosci. 2003, 23:6141-6151.
47. Nakamura W., Yamazaki S., Takasu N.N., Mishima K., Block G.D. Differential response of Period 1 expression within the suprachiasmatic nucleus. J.Neurosci. 2005, 25:5481-5487.
48. Nielsen H.S., Hannibal J., Fahrenkrug J. Vasoactive intestinal polypeptide induces per1 and per2 gene expression in the rat suprachiasmatic nucleus late at night. Eur. J. Neurosci. 2002, 15:570-574.
49. Obrietan K., Impey S., Storm D.R. Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat. Neurosci. 1998, 1:693-700.
50. Ohta H., Yamazaki S., McMahon D.G. Constant light desynchronizes mammalian clock neurons. Nat. Neurosci. 2005, 8:267-269.
51. Piggins H.D., Antle M.C., Rusak B. Neuropeptides phase shift the mammalian circadian pacemaker. J.Neurosci. 1995, 15:5612-5622.
52. Reddy A.B., Field M.D., Maywood E.S., Hastings M.H. Differential resynchronisation of circadian clock gene expression within thesuprachiasmatic nuclei of mice subjected to experimental jet lag. J.Neurosci. 2002, 22:7326-7330.
53. Reed H.E., Meyer-Spasche A., Cutler D.J., Coen C.W., Piggins H.D. Vasoactive intestinal polypeptide (VIP) phase-shifts the rat suprachiasmatic nucleus clock invitro. Eur. J. Neurosci. 2001, 13:839-843.
54. Reppert S.M., Weaver D.R. Coordination of circadian timing in mammals. Nature 2002, 418:935-941.
55. Rohling J.H., vanderLeest H.T., Michel S., Vansteensel M.J., Meijer J.H. Phase resetting of the mammalian circadian clock relies on a rapid shift of a small population of pacemaker neurons. PLoS ONE 2011, 6:e25437.
56. Rosbash M. The implications of multiple circadian clock origins. PLoS Biol. 2009, 7:e62.
57. Rosbash M., Bradley S., Kadener S., Li Y., Luo W., Menet J.S., Nagoshi E., Palm K., Schoer R., Shang Y., Tang C.H. Transcriptional feedback and definition of the circadian pacemaker in Drosophila and animals. Cold Spring Harb. Symp. Quant. Biol. 2007, 72:75-83.
58. Sauer B., Henderson N. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc. Natl. Acad. Sci. USA 1988, 85:5166-5170.
59. Shen S., Spratt C., Sheward W.J., Kallo I., West K., Morrison C.F., Coen C.W., Marston H.M., Harmar A.J. Overexpression of the human VPAC2 receptor in the suprachiasmatic nucleus alters the circadian phenotype of mice. Proc. Natl. Acad. Sci. USA 2000, 97:11575-11580.
60. Sonenberg N., Hinnebusch A.G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009, 136:731-745.
61. Takahashi Y., Okamura H., Yanaihara N., Hamada S., Fujita S., Ibata Y. Vasoactive intestinal peptide immunoreactive neurons in the rat suprachiasmatic nucleus demonstrate diurnal variation. Brain Res. 1989, 497:374-377.
62. 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. 2008, 9:764-775.
63. To T.L., Henson M.A., Herzog E.D., Doyle F.J. A molecular model for intercellular synchronization in the mammalian circadian clock. Biophys. J. 2007, 92:3792-3803.
64. Topisirovic I., Sonenberg N. mRNA translation and energy metabolism in cancer: the role of the MAPK and mTORC1 pathways. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:355-367.
65. Tsukiyama-Kohara K., Poulin F., Kohara M., DeMaria C.T., Cheng A., Wu Z., Gingras A.C., Katsume A., Elchebly M., Spiegelman B.M., et al. Adipose tissue reduction in mice lacking the translational inhibitor 4E-BP1. Nat. Med. 2001, 7:1128-1132.
66. vanderLeest H.T., Rohling J.H., Michel S., Meijer J.H. Phase shifting capacity of the circadian pacemaker determined by the SCN neuronal network organization. PLoS ONE 2009, 4:e4976.
67. Waschek J.A., Hsu C.M., Eiden L.E. Lineage-specific regulation of the vasoactive intestinal peptide gene in neuroblastoma cells is conferred by 5.2 kilobases of 5'-flanking sequence. Proc. Natl. Acad. Sci. USA 1988, 85:9547-9551.
68. Welsh D.K., Logothetis D.E., Meister M., Reppert S.M. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 1995, 14:697-706.
69. Welsh D.K., Takahashi J.S., Kay S.A. Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 2010, 72:551-577.
70. Yamaguchi S., Isejima H., Matsuo T., Okura R., Yagita K., Kobayashi M., Okamura H. Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 2003, 302:1408-1412.
71. Yamazaki S., Numano R., Abe M., Hida A., Takahashi R., Ueda M., Block G.D., Sakaki Y., Menaker M., Tei H. Resetting central and peripheral circadian oscillators in transgenic rats. Science 2000, 288:682-685.
72. Yoo S.H., Yamazaki S., Lowrey P.L., Shimomura K., Ko C.H., Buhr E.D., Siepka S.M., Hong H.K., Oh W.J., Yoo O.J., et al. PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. USA 2004, 101:5339-5346.
73. Zheng X., Sehgal A. AKT and TOR signaling set the pace of the circadian pacemaker. Curr. Biol. 2010, 20:1203-1208.