A Gq-Ca2+ Axis controls circuit-level encoding of circadian time in the suprachiasmatic nucleus

Neuron

Volumn 78, Issue 4, 2013, Pages 714-728

  Brancaccio, Marco ^a   Maywood, ElizabethS ^a   Chesham, JohannaE ^a   Loudon, AndrewS I ^b   Hastings, MichaelH ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CRE RECOMBINASE; CYCLIC AMP; GUANINE NUCLEOTIDE BINDING PROTEIN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN; VASOACTIVE INTESTINAL POLYPEPTIDE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; BRAIN NERVE CELL; BRAIN SLICE; CALCIUM CELL LEVEL; CIRCADIAN RHYTHM; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; CYTOSOL; FEEDBACK SYSTEM; FLUORESCENCE; GENETIC TRANSDUCTION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; ANIMAL; CALCIUM SIGNALING; IN VITRO STUDY; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; SECOND MESSENGER; TRANSGENIC MOUSE;

ANIMALS; CALCIUM SIGNALING; CIRCADIAN CLOCKS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEEDBACK, PHYSIOLOGICAL; GTP-BINDING PROTEIN ALPHA SUBUNITS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; VASOACTIVE INTESTINAL PEPTIDE;

MLCS; MLOWN;

EID: 84878450313     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.03.011     Document Type: Article

References (45)

1. 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.
2. Armbruster B.N., Li X., Pausch M.H., Herlitze S., Roth B.L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl. Acad. Sci. USA 2007, 104:5163-5168.
3. Atkinson S.E., Maywood E.S., Chesham J.E., Wozny C., Colwell C.S., Hastings M.H., Williams S.R. Cyclic AMP signaling control of action potential firing rate and molecular circadian pacemaking in the suprachiasmatic nucleus. J.Biol. Rhythms 2011, 26:210-220.
4. 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.
5. Bito H., Deisseroth K., Tsien R.W. Ca2+-dependent regulation in neuronal gene expression. Curr. Opin. Neurobiol. 1997, 7:419-429.
6. Brancaccio M., Pivetta C., Granzotto M., Filippis C., Mallamaci A. Emx2 and Foxg1 inhibit gliogenesis and promote neuronogenesis. Stem Cells 2010, 28:1206-1218.
7. Butler M.P., Silver R. Basis of robustness and resilience in the suprachiasmatic nucleus: individual neurons form nodes in circuits that cycle daily. J.Biol. Rhythms 2009, 24:340-352.
8. 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.
9. Dickson L., Finlayson K. VPAC and PAC receptors: From ligands to function. Pharmacol. Ther. 2009, 121:294-316.
10. Doi M., Ishida A., Miyake A., Sato M., Komatsu R., Yamazaki F., Kimura I., Tsuchiya S., Kori H., Seo K., et al. Circadian regulation of intracellular G-protein signalling mediates intercellular synchrony and rhythmicity in the suprachiasmatic nucleus. Nat. Comm. 2011, 2:327.
11. Dorostkar M.M., Dreosti E., Odermatt B., Lagnado L. Computational processing of optical measurements of neuronal and synaptic activity in networks. J.Neurosci. Methods 2010, 188:141-150.
12. Enoki R., Ono D., Hasan M.T., Honma S., Honma K. Single-cell resolution fluorescence imaging of circadian rhythms detected with a Nipkow spinning disk confocal system. J.Neurosci. Methods 2012, 207:72-79.
13. 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.
14. Fustin J.M., O'Neill J.S., Hastings M.H., Hazlerigg D.G., Dardente H. Cry1 circadian phase invitro: wrapped up with an E-box. J.Biol. Rhythms 2009, 24:16-24.
15. Garner A.R., Rowland D.C., Hwang S.Y., Baumgaertel K., Roth B.L., Kentros C., Mayford M. Generation of a synthetic memory trace. Science 2012, 335:1513-1516.
16. 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.
17. Harrisingh M.C., Wu Y., Lnenicka G.A., Nitabach M.N. Intracellular Ca2+ regulates free-running circadian clock oscillation invivo. J.Neurosci. 2007, 27:12489-12499.
18. Hastings M.H., Reddy A.B., Maywood E.S. A clockwork web: circadian timing in brain and periphery, in health and disease. Nat. Rev. Neurosci. 2003, 4:649-661.
19. Hastings M.H., O'Neill J.S., Maywood E.S. Circadian clocks: regulators of endocrine and metabolic rhythms. J.Endocrinol. 2007, 195:187-198.
20. Hastings M.H., Maywood E.S., O'Neill J.S. Cellular circadian pacemaking and the role of cytosolic rhythms. Curr. Biol. 2008, 18:R805-R815.
21. Hong J.H., Jeong B., Min C.H., Lee K.J. Circadian waves of cytosolic calcium concentration and long-range network connections in rat suprachiasmatic nucleus. Eur. J. Neurosci. 2012, 35:1417-1425.
22. Ikeda M., Sugiyama T., Wallace C.S., Gompf H.S., Yoshioka T., Miyawaki A., Allen C.N. Circadian dynamics of cytosolic and nuclear Ca2+ insingle suprachiasmatic nucleus neurons. Neuron 2003, 38:253-263.
23. Inagaki N., Honma S., Ono D., Tanahashi Y., Honma K. Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. Proc. Natl. Acad. Sci. USA 2007, 104:7664-7669.
24. Ko C.H., Yamada Y.R., Welsh D.K., Buhr E.D., Liu A.C., Zhang E.E., Ralph M.R., Kay S.A., Forger D.B., Takahashi J.S. Emergence of noise-induced oscillations in the central circadian pacemaker. PLoS Biol. 2010, 8:e1000513.
25. Kori H., Kawamura Y., Masuda N. Structure of cell networks critically determines oscillation regularity. J.Theor. Biol. 2012, 297:61-72.
26. 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.
27. Low-Zeddies S.S., Takahashi J.S. Chimera analysis of the Clock mutation in mice shows that complex cellular integration determines circadian behavior. Cell 2001, 105:25-42.
28. Lundkvist G.B., Kwak Y., Davis E.K., Tei H., Block G.D. A calcium flux is required for circadian rhythm generation in mammalian pacemaker neurons. J.Neurosci. 2005, 25:7682-7686.
29. 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.
30. 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.
31. Mizrak D., Ruben M., Myers G.N., Rhrissorrakrai K., Gunsalus K.C., Blau J. Electrical activity can impose time of day on the circadian transcriptome of pacemaker neurons. Curr. Biol. 2012, 22:1871-1880.
32. Mohawk J.A., Takahashi J.S. Cell autonomy and synchrony of suprachiasmatic nucleus circadian oscillators. Trends Neurosci. 2011, 34:349-358.
33. O'Neill J.S., Maywood E.S., Chesham J.E., Takahashi J.S., Hastings M.H. cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 2008, 320:949-953.
34. Obrietan K., Impey S., Smith D., Athos J., Storm D.R. Circadian regulation of cAMP response element-mediated gene expression in the suprachiasmatic nuclei. J.Biol. Chem. 1999, 274:17748-17756.
35. Rogan S.C., Roth B.L. Remote control of neuronal signaling. Pharmacol. Rev. 2011, 63:291-315.
36. Shaywitz A.J., Greenberg M.E. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 1999, 68:821-861.
37. 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.
38. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
39. Tian L., Hires S.A., Mao T., Huber D., Chiappe M.E., Chalasani S.H., Petreanu L., Akerboom J., McKinney S.A., Schreiter E.R., et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 2009, 6:875-881.
40. Tian L., Hires S.A., Looger L.L. Imaging neuronal activity with genetically encoded calcium indicators. Cold Spring Harb. Protoc. 2012, 2012:647-656.
41. 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 2002, 99:7728-7733.
42. Welsh D.K., Takahashi J.S., Kay S.A. Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 2010, 72:551-577.
43. 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.
44. Yizhar O., Fenno L.E., Davidson T.J., Mogri M., Deisseroth K. Optogenetics in neural systems. Neuron 2011, 71:9-34.
45. 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.