Signaling in the mammalian circadian clock: The NO/cGMP pathway

Neurochemistry International

Volumn 45, Issue 6, 2004, Pages 929-936

  Golombek, Diego A ^a   Agostino, Patricia V ^a   Plano, Santiago A ^a   Ferreyra, Gabriela A ^a  

^a UNIVERSIDAD NACIONAL DE QUILMES   (Argentina)

Author keywords

Ca2+ calmodulin dependent kinase; cGMP dependent kinase; Circadian rhythms; Hamster; Nitric oxide synthase; Suprachiasmatic nucleus

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II INHIBITOR; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; GLUTAMIC ACID; GUANYLATE CYCLASE; KT 5823; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHODIESTERASE; PROTEIN INHIBITOR; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE (CALCIUM,CALMODULIN) II; UNCLASSIFIED DRUG;

BIOLOGICAL RHYTHM; BRAIN NERVE CELL; CELLULAR DISTRIBUTION; CIRCADIAN RHYTHM; CONFERENCE PAPER; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; HYPOTHALAMUS; LIGHT DARK CYCLE; NEUROTRANSMISSION; NONHUMAN; ONCOGENE C FOS; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; SUPRACHIASMATIC NUCLEUS;

ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; CYCLIC GMP; GLUTAMIC ACID; HUMANS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS;

CRICETINAE; MAMMALIA;

EID: 4243172345     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2004.03.023     Document Type: Conference Paper

References (59)

1. Agostino P.V., Ferreyra G.A., Murad A.D., Watanabe Y., Golombek D.A. Diurnal, circadian and photic regulation of calcium/calmodulin-protein kinase II and neuronal nitric oxide synthase in the hamster suprachiasmatic nuclei. Neurochem. Int. 44:2004;617-625
2. Aida R., Moriya T., Araki M., Akiyama M., Wada K., Wada E., Shibata S. Gastrin-releasing peptide mediates photic entrainable signals to dorsal subsets of suprachiasmatic nucleus via induction of Period gene in mice. Mol. Pharmacol. 61:2002;26-34
3. Caillol M., Devinoy E., Lacroix M.C., Schirar A. Endothelial and neuronal nitric oxide synthases are present in the suprachiasmatic nuclei of Syrian hamsters and rats. Eur. J. Neurosci. 12:2000;649-661
4. Colbran J.L., Roach P.J., Fiol C.J., Dixon J.E., Andrisani O.M., Corbin J.D. cAMP-dependent protein kinase, but not the cGMP-dependent protein enzyme, rapidly phosphorylates delta-CREB, and a synthetic delta-CREB peptide. Biochem. Cell Biol. 70:1992;1277-1282
5. Colwell C.S. Rhythmic coupling among cells in the suprachiasmatic nucleus. J. Neurobiol. 43:2000;379-388
6. Colwell C.S. NMDA-evoked calcium transients and currents in the suprachiasmatic nucleus: gating by the circadian system. Eur. J. Neurosci. 13:2001;1420-1428
7. Colwell C.S., Menaker M. NMDA as well non-NMDA receptor antagonist can prevent the phase shifting effects of light on the circadian system of the golden hamster. J. Biol. Rhythms. 7:1992;125-136
8. Conti M., Jin S.L. The molecular biology of cyclic nucleotide phosphodiesterases. Prog. Nucleic Acid Res. Mol. Biol. 63:1999;1-38
9. Darlington T.K., Lyons L.C., Hardin P.E., Kay S.A. The period E-box is sufficient to drive circadian oscillation of transcription in vivo. J. Biol. Rhythms. 15:2000;483-490
10. Diaz-Muñoz M., Dent M.A.R., Granados-Fuentes D., Hernández-Cruz A.C.H., Harrington M.E., Aguilar-Roblero R. Circadian modulation of the ryanodine receptor type 2 in the SCN of rodents. Neuroreport. 10:1999;481-486
11. Ding J.M., Chen D., Weber E.T., Faiman L.E., Rea M.A., Gillette M.U. Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. Science. 266:1994;1713-1717
12. Ding M., Buchanan G.F., Tischkau S.A., Chen D., Kuriashkina L., Faiman L.E., Alster J.M., McPherson P.S., Campbell K.P., Gillette M.U. A neuronal ryanodine receptor mediates light-induced phase delays of the circadian clock. Nature. 394:1998;381-384
13. Dunlap J.C. Molecular basis for circadian clocks. Cell. 96:1999;271-290
14. Ebling F.J. The role of glutamate in the photic regulation of the suprachiasmatic nucleus. Prog. Neurobiol. 50:1996;109-132
15. Ferreyra G.A., Cammarota M.P., Golombek D.A. Photic control of nitric oxide synthase activity in the hamster suprachiasmatic nuclei. Brain Res. 797:1998;190-196
16. Ferreyra G.A., Golombek D.A. Rhythmicity of the cGMP-related function in the circadian system. Am. J. Physiol. 280:2001;R1348-R1355
17. +2/calmodulin- dependent protein kinase II in the circadian rhythms controlled by the suprachiasmatic nucleus. Neurosci. Lett. 227:1997;45-48
18. Gambaryan S., Butt E., Marcus K., Glazova M., Palmetshofer A., Guillon G., Smolenski A. cGMP-dependent protein kinase type II regulates basal level of aldosterone production by zona glomerulosa cells without increasing expression of the steroidogenic acute regulatory protein gene. J. Biol. Chem. 278:2003;29640-29648
19. 142 regulates light-induced phase shifts of the circadian clock. Neuron. 34:2002;245-253
20. Gillette M.U. Regulation of entrainment pathways by the suprachiasmatic circadian clock: sensitivities to second messengers. Prog. Brain Res. 111:1996;121-132
21. Ginty D.D., Kornhauser J.M., Thompson M.A., Bading H., Mayo K.E., Takahashi J.S., Greenberg M.E. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science. 260:1993;238-241
22. +2/ calmodulin kinase II, attenuates circadian responses to light. Neuroreport. 5:1994;1638-1640
23. Golombek D.A., Ralph M.R. Circadian responses to light: the calmodulin connection. Neurosci. Lett. 192:1995;101-104
24. Golombek D.A., Ferreyra G.A., Agostino P.V., Murad A.D., Rubio M.F., Pizzio G.A., Katz M.E., Marpegan L., Bekinschtein T.A. From light to genes: moving the hands of the circadian clock. Front. Biosci. 8:2003;56-70
25. Golombek D.A., Ferreyra G.A., Katz M.E., Marpegan L., Fernández Alfonso T., Yannielli P.C. The neurochemical basis of photic entrainment in mammals. Biol. Rhythm Res. 31:2000;56-70
26. Gudi T., Casteel D.E., Vinson C., Boss G.R., Pilz R.B. NO activation of fos promoter elements requires nuclear translocation of G-kinase I and CREB phosphorylation but is independent of MAPkinase activation. Oncogene. 19:2000;6324-6333
27. Gudi T., Hong G.K., Vaandrager A.B., Lohmann S.M., Pilz R.B. Nitric oxide and cGMP regulate gene expression in neuronal and glial cells by activating type II cGMP-dependent protein kinase. FASEB J. 13:1999;2143-2152
28. Klein, D.C., Moore, R.Y., Reppert, S.M., 1991. Suprachiasmatic Nucleus: The Mind's Clock. Oxford University Press, New York.
29. Kriegsfeld L.J., Demas G.E., Lee S.E. Jr., Dawson T.M., Dawson V.L., Nelson R.J. Circadian locomotor analysis of male mice lacking the gene for neuronal nitric oxide synthase (nNOS-/-). J. Biol. Rhythms. 14:1999;20-27
30. Lohmann S.M., Vaandrager A.B., Smolenski A., Walter U., DeJonge H.R. Distinct and specific functions of cGMP-dependent protein kinases. Trends Biochem. Sci. 22:1997;307-312
31. 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. 288:2000;483-492
32. Mathur A., Golombek D.A., Ralph M.R. cGMP-dependent protein kinase inhibitors block light-induced phase advances of circadian rhythms in vivo. Am. J. Physiol. 270:1996;R1031-R1036
33. Meijer J.H., Schwartz W.J. In search of the pathways for light-induced pacemaker resetting in the suprachiasmatic nucleus. J. Biol. Rhythms. 18:2003;235-249
34. Melo L., Golombek D.A., Ralph M.R. Regulation of circadian photic responses by nitric oxide. J. Biol. Rhythms. 12:1997;319-326
35. Michel S., Itri J., Colwell C.S. Excitatory mechanisms in the suprachiasmatic nucleus: the role of AMPA/KA glutamate receptors. J. Neurophysiol. 88:2002;817-828
36. Moore R.Y., Speh J.C., Leak R.K. Suprachiasmatic nucleus organization. Cell Tissue Res. 309:2002;89-98
37. Muñoz E., Baler R. The circadian E-box: when perfect is not good enough. Chronobiol. Int. 20:2003;371-388
38. 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. 274:1999;17748-17756
39. Okamura H., Yamaguchi S., Yagita K. Molecular machinery of the circadian clock in mammals. Cell Tissue Res. 309:2002;47-56
40. Oster H., Werner C., Magnone M.C., Mayser H., Feil R., Seeliger M.W., Hofmann F., Albrecht U. cGMP-dependent protein kinase II modulates mPer1 and mPer2 gene induction and influences phase shifts of the circadian clock. Curr. Biol. 13:2003;725-733
41. Pennartz C.M., Hamstra R., Geurtsen A.M. Enhanced NMDA receptor activity in retinal inputs to the rat suprachiasmatic nucleus during the subjective night. J. Physiol. 532:2001;181-194
42. Pittendrigh, C.S., 1981. In: Aschoff, J. (Ed.), Hanbook of Behavioral Neurobiology: Biological Rhythms, Circadian Systems: Entrainment. Plenum Press, New York, pp. 95-124.
43. Ralph M.R., Hurd M.W., Takeuchi J., Melo L., Mathur A., Golombek D.A. Regulation and integration in the mammalian circadian system. Prog. Brain Res. 111:1996;191-203
44. Reuss S., Decker K., Robeler L., Layes E., Schollmayer A., Spessert L. Nitric oxide synthase in the hypothalamic suprachiasmatic nucleus of rat: evidence from histochemistry, immunohistochemistry and western blot; and colocalization with VIP. Brain Res. 695:1995;257-262
45. Revermann M., Maronde E., Ruth P., Korf H.W. Protein kinase G immunoreaction is colocalized with arginine-vasopressin immunoreaction in the rat suprachiasmatic nucleus. Neurosci. Lett. 334:2002;119-122
46. Scherer-Oppliger T., Leimbacher W., Blau N., Thöny B. Serine19 of human 6-pyruvoyltetrahydropterin synthase Is phosphorylated by cGMP protein Kinase II. J. Biol. Chem. 274:1999;31341-31348
47. Shearman L.P., Sriram S., Weaver D.R., Maywood E.S., Chaves I., Zheng B., Kume K., Lee C.C., van der Horst G.T., Hastings M.H., Reppert S.M. Interacting molecular loops in the mammalian circadian clock. Science. 288:2000;1013-1019
48. Smolenski A., Burkhardt A.M., Eigenthaler M., Butt E., Gambaryan S., Lohmann S.M., Walter U. Functional analysis of cGMP-dependent protein kinases I and II as mediators of NO/cGMP effects. Naunyn-Schmiedeberg's Arch. Pharmacol. 358:1998;134-139
49. Tischkau S.A., Weber E.T., Abbott S.M., Mitchell J.W., Gillette M.U. Circadian clock-controlled regulation of cGMP-protein kinase G in the nocturnal domain. J. Neurosci. 23:2003;7543-7550
50. Toh K.L., Jones C.R., He Y., Eide E.J., Hinz W.A., Virshup D.M., Ptacek L.J., Fu Y.H. An hPer2 phosphorylation site mutation in familiar advanced sleep phase syndrome. Science. 291:2001;1040-1043
51. van den Pol A.N. The hypothalamic suprachiasmatic nucleus of rat: intrinsic anatomy. J. Comp. Neurol. 191:1980;661-702
52. van den Pol A.N., Finkbeiner S.M., Cornell-Bell A.H. Calcium excitability and oscillations in suprachiasmatic nucleus neurons and glia in vitro. J. Neurosci. 12:1992;2648-2664
53. von Gall C., Duffield G.E., Hastings M.H., Koop M.D., Dehghani F., Korf H.W., Stehle J.H. CREB in the mouse SCN: a molecular interface coding the phase-adjusting stimuli light, glutamate, PACAP and melatonin for clockwork access. J. Neurosci. 18:1998;10389-10397
54. Wang H., Morris J.F. Presence of neuronal nitric oxide synthase in the suprachiasmatic nuclei of mouse and rat. Neuroscience. 74:1996;1059-1068
55. Watanabe A., Ono M., Shibata S., Watanabe S. Effect of a nitric oxide synthase inhibitor, N-nitro-L-arginine methyl ester, on light-induced phase delay of circadian wheel-running activity in golden hamsters. Neurosci. Lett. 192:1995;25-28
56. Weber E.T., Gannon R.L., Rea M.A. cGMP-dependent protein kinase inhibitor blocks light-induced phase advances of circadian rhythms in vivo. Neurosci. Lett. 197:1995a;227-230
57. Weber E.T., Gannon R.L., Michel A.M., Gillette M.U., Rea M.A. Nitric oxide synthase inhibitor blocks light-induced phase shifts of the circadian activity rhythm, but not c-fos expression in the suprachiasmatic nucleus of the Syrian hamster. Brain Res. 692:1995b;137-142
58. 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. 14:1995;697-706
59. Wu G.-Y., Deisseroth K., Tsien R.W. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. U.S.A. 98:2001;2808-2813