Role for the NR2B subunit of the N-methyl-D-aspartate receptor in mediating light input to the circadian system

European Journal of Neuroscience

Volumn 27, Issue 7, 2008, Pages 1771-1779

  Wang, L M ^a   Schroeder, A ^a   Loh, D ^a   Smith, D ^a   Lin, K ^a   Han, J H ^a   Michel, S ^a,c   Hummer, D L ^b   Ehlen, J C ^b,d   Albers, H E ^b   Colwell, C S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d MOREHOUSE SCHOOL OF MEDICINE   (United States)

Author keywords

Ca2+; Circadian rhythms; Fura2; Ifenprodil; Mice; Suprachiasmatic nucleus; Syrian hamsters

Indexed keywords

IFENPRODIL; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DRUG INHIBITION; EXPERIMENTAL TEST; HAMSTER; LOCOMOTION; MALE; MOUSE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; RETINA GANGLION CELL; SUPRACHIASMATIC NUCLEUS; WESTERN BLOTTING;

ANIMALS; CIRCADIAN RHYTHM; CRICETINAE; MALE; MESOCRICETUS; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PHOTIC STIMULATION; PIPERIDINES; PROTEIN SUBUNITS; RECEPTORS, N-METHYL-D-ASPARTATE; SUPRACHIASMATIC NUCLEUS;

EID: 41549144804     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06144.x     Document Type: Article

References (58)

1. Abe, H. Rusak, B. (1994) Physiological mechanisms regulating photic induction of Fos-like protein in hamster suprachiasmatic nucleus. Neurosci. Biobehav. Rev., 18, 531 536.
2. Aguilar-Roblero, R., Mercado, C., Alamilla, J., Laville, A. Díaz-Muñoz, M. (2007) Ryanodine receptor Ca2+-release channels are an output pathway for the circadian clock in the rat suprachiasmatic nuclei. Eur. J. Neurosci., 26, 575 582.
3. Berson, D.M. (2003) Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci., 26, 314 320.
4. 2+-dependent regulation in neuronal gene expression. Curr. Opin. Neurobiol., 7, 419 429.
5. Castel, M., Belenky, M., Cohen, S., Ottersen, O.P. Storm-Mathisen, J. (1993) Glutamate-like immunoreactivity in retinal terminals of the mouse suprachiasmatic nucleus. Eur. J. Neurosci., 5, 368 381.
6. Cermakian, N. Sassone-Corsi, P. (2002) Environmental stimulus perception and control of circadian clocks. Curr. Opin. Neurobiol., 12, 359 365.
7. Chen, B. Pourcho, R.G. (1995) Morphological diversity and glutamate immunoreactivity of retinal terminals in the suprachiasmatic nucleus of the cat. J. Comp. Neurol., 361, 108 118.
8. Colwell, C.S. (2000) Circadian modulation of calcium levels in cells in the suprachiasmatic nucleus. Eur. J. Neurosci., 12, 571 576.
9. Colwell, C.S. (2001) NMDA-evoked calcium transients and currents in the suprachiasmatic nucleus: Gating by the circadian system. Eur. J. Neurosci., 13, 1420 1428.
10. Colwell, C.S. Menaker, M. (1992) NMDA as well as non-NMDA receptor antagonists can prevent the phase-shifting effects of light on the circadian system of the golden hamster. J. Biol. Rhythms, 7, 125 136.
11. Colwell, C.S., Whitmore, D., Michel, S. Block, G.D. (1994) Calcium plays a central role in phase shifting the ocular circadian pacemaker of Aplysia. J. Comp. Physiol., 175, 415 423.
12. Crosio, C., Cermakian, N., Allis, C.D. Sassone-Corsi, P. (2000) Light induces chromatin modification in cells of the mammalian circadian clock. Nat. Neurosci., 3, 1241 1247.
13. Cull-Candy, S., Brickley, S. Farrant, M. (2001) NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol., 11, 327 335.
14. Ding, J.M., Chen, D., Weber, E.T., Faiman, L.E., Rea, M.A. Gillette, M.U. (1994) Resetting the biological clock: Mediation of nocturnal circadian shifts by glutamate and NO. Science, 266, 1713 1717.
15. Ding, J.M., Faiman, L.E., Hurst, W.J., Kuriashkina, L.R. Gillette, M.U. (1997) Resetting the biological clock: mediation of nocturnal CREB phosphorylation via light, glutamate, and nitric oxide. J. Neurosci., 17, 667 675.
16. Gannon, R.L. Rea, M.A. (1993) Glutamate receptor immunoreactivity in the rat suprachiasmatic nucleus. Brain Res., 622, 337 342.
17. Gannon, R.L. Rea, M.A. (1994) In situ hybridization of antisense mRNA oligonucleotides for AMPA, NMDA and metabotropic glutamate receptor subtypes in the rat suprachiasmatic nucleus at different phases of the circadian cycle. Brain Res. Mol. Brain Res., 23, 338 344.
18. Gau, D., Lemberger, T., von Gall, C., Kretz, O., Le Minh, N., Gass, P., Schmid, W., Schibler, U., Korf, H.W. Schuetz, G. (2002) Phosphorylation of CREB Ser142 regulates light-induced phase shifts of the circadian clock. Neuron, 34, 245 253.
19. Gillette, M.U. Mitchell, J.W. (2002) Signaling in the suprachiasmatic nucleus: selectively responsive and integrative. Cell Tissue Res., 309, 99 107.
20. Hastings, M.H. Herzog, E.D. (2004) Clock genes, oscillators, and cellular networks in the suprachiasmatic nuclei. J. Biol. Rhythms, 19, 400 413.
21. Ishida, N., Matsui, M., Mitsui, Y. Mishina, M. (1994) Circadian expression of NMDA receptor mRNAs, epsilon 3 and zeta 1, in the suprachiasmatic nucleus of rat brain. Neurosci. Lett., 166, 211 215.
22. Jiang, Z.G., Yang, Y., Liu, Z.P. Allen, C.N. (1997) Membrane properties and synaptic inputs of suprachiasmatic nucleus neurons in rat brain slices. J. Physiol., 499, 141 159.
23. Khalsa, S.B., Ralph, M.R. Block, G.D. (1993) The role of extracellular calcium in generating and in phase-shifting the Bulla ocular circadian rhythm. J. Biol. Rhythms, 8, 125 139.
24. Kim, Y.I. Dudek, F.E. (1991) Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: excitatory synaptic mechanisms. J. Physiol., 444, 269 287.
25. Kim, D.Y., Choi, H.J., Kim, J.S., Kim, Y.S., Jeong, D.U., Shin, H.C., Kim, M.J., Han, H.C., Hong, S.K. Kim, Y.I. (2005) Voltage-gated calcium channels play crucial roles in the glutamate-induced phase shifts of the rat suprachiasmatic circadian clock. Eur. J. Neurosci., 21, 1215 1222.
26. Kim, Y.I., Choi, H.J. Colwell, C.S. (2006) Brain-derived neurotrophic factor regulation of N-methyl-D-aspartate receptor-mediated synaptic currents in suprachiasmatic nucleus neurons. J. Neurosci. Res., 84, 1512 1520.
27. Kornhauser, J.M., Mayo, K.E. Takahashi, J.S. (1996) Light, immediate-early genes, and circadian rhythms. Behav. Genet., 26, 221 240.
28. Levine, E.S. Kolb, J.E. (2000) Brain-derived neurotrophic factor increases activity of NR2B-containing N-methyl-D-aspartate receptors in excised patches from hippocampal neurons. J. Neurosci. Res., 62, 357 362.
29. Lin, S.Y., Wu, K., Levine, E.S., Mount, H.T., Suen, P.C. Black, I.B. (1998) BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res. Mol. Brain Res., 55, 20 27.
30. Loftis, J.M. Janowsky, A. (2003) The N-methyl-D-aspartate receptor subunit NR2B: localization, functional properties, regulation, and clinical implications. Pharmacol. Ther., 97, 55 85.
31. Lopez de Armentia, M. Sah, P. (2003) Development and subunit composition of synaptic NMDA receptors in the amygdala: NR2B synapses in the adult central amygdala. J. Neurosci., 23, 6876 6883.
32. Lundkvist, G.B., Kwak, Y., Davis, E.K., Tei, H. Block, G.D. (2005) A calcium flux is required for circadian rhythm generation in mammalian pacemaker neurons. J. Neurosci., 25, 7682 7686.
33. Matsushita, T., Amagai, Y., Terai, K., Kojima, T., Obinata, M. Hashimoto, S. (2006) A novel neuronal cell line derived from the ventrolateral region of the suprachiasmatic nucleus. Neuroscience, 140, 849 856.
34. McBain, C.J. Mayer, M.L. (1994) N-methyl-D-aspartic acid receptor structure and function. Physiol. Rev., 74, 723 760.
35. McMahon, D.G. Block, G.D. (1987) The Bulla ocular circadian pacemaker. I. Pacemaker neuron membrane potential controls phase through a calcium-dependent mechanism. J. Comp. Physiol., 161, 335 346.
36. Meijer, J.H. Schwartz, W.J. (2003) In search of the pathways for light-induced pacemaker resetting in the suprachiasmatic nucleus. J. Biol. Rhythms, 18, 235 249.
37. Michel, S., Itri, J. Colwell, C.S. (2002) Excitatory mechanisms in the suprachiasmatic nucleus: The role of AMPA/KA glutamate receptors. J. Neurophysiol., 88, 817 828.
38. Mikkelsen, J.D., Larsen, P.J. Ebling, F.J. (1993) Distribution of N-methyl d-aspartate (NMDA) receptor mRNAs in the rat suprachiasmatic nucleus. Brain Res., 632, 329 333.
39. Mintz, E.M., Marvel, C.L., Gillespie, C.F., Price, K.M. Albers, H.E. (1999) Activation of NMDA receptors in the suprachiasmatic nucleus produces light-like phase shifts of the circadian clock in vivo. J. Neurosci., 19, 5124 5130.
40. Miyake, S., Sumi, Y., Yan, L., Takekida, S., Fukuyama, T., Ishida, Y., Yamaguchi, S., Yagita, K. Okamura, H. (2000) Phase-dependent responses of Per1 and Per2 genes to a light-stimulus in the suprachiasmatic nucleus of the rat. Neurosci. Lett., 294, 41 44.
41. Morin, L.P. Allen, C.N. (2006) The circadian visual system. Brain Res. Rev., 51, 1 60.
42. Moriya, T., Horikawa, K., Akiyama, M. Shibata, S. (2000) Correlative association between N-methyl-D-aspartate receptor-mediated expression of period genes in the suprachiasmatic nucleus and phase shifts in behavior with photic entrainment of clock in hamsters. Mol. Pharmacol., 58, 1554 1562.
43. Neyton, J. Paoletti, P. (2006) Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach. J. Neurosci., 26, 1331 1333.
44. Obrietan, K., Impey, S. Storm, D.R. (1998) Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat. Neurosci., 1, 693 700.
45. C, and NMDA receptor subunit expression in the suprachiasmatic nucleus and other brain regions. Brain Res. Mol. Brain Res., 28, 239 250.
46. Pennartz, C.M.A., Hamstra, R. Geurtsen, A.M.S. (2001) Enhanced NMDA receptor activity in retinal inputs to the rat suprachiasmatic nucleus during the subjective night. J. Physiol. (Camb.), 532, 181 194.
47. Quinlan, E.M., Olstein, D.H. Bear, M.F. (1999) Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc. Natl Acad. Sci. U.S.A., 96, 12 876 12 880.
48. Rachline, J., Perin-Dureau, F., Le Goff, A., Neyton, J. Paoletti, P. (2005) The micromolar zinc-binding domain on the NMDA receptor subunit NR2B. J. Neurosci., 25, 308 317.
49. Roenneberg, T., Daan, S. Merrow, M. (2003) The art of entrainment. J. Biol. Rhythms, 18, 183 194.
50. Shibata, S. Moore, R.Y. (1993) Neuropeptide Y and optic chiasm stimulation affect suprachiasmatic nucleus circadian function in vitro. Brain Res., 615, 95 100.
51. Shibata, S., Watanabe, A., Hamada, T., Ono, M. Watanabe, S. (1994) N-methyl-D-aspartate induces phase shifts in circadian rhythm of neuronal activity of rat SCN in vitro. Am. J. Physiol., 267, R360 R64.
52. 2+/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.
53. Travnickova-Bendova, Z., Cermakian, N., Reppert, S.M. Sassone-Corsi, P. (2002) Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity. Proc. Natl Acad. Sci. U.S.A., 99, 7728 7733.
54. de Vries, M.J., Treep, J.A. Meijer, J.H. (1994) Electrical stimulation of the anterior optic chiasm mimics the phase shifting effects of light on the circadian activity rhythm of the Syrian hamster. Biol. Rhythms Res., 25, 211 213.
55. West, A.E., Chen, W.G., Dalva, M.B., Dolmetsch, R.E., Kornhauser, J.M., Shaywitz, A.J., Takasu, M.A., Tao, X. Greenberg, M.E. (2001) Calcium regulation of neuronal gene expression. Proc. Natl Acad. Sci. U.S.A., 98, 11 024 11 031.
56. Williams, K. (1993) Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol. Pharmacol., 44, 851 859.
57. Williams, K. (2001) Ifenprodil, a novel NMDA receptor antagonist: site and mechanism of action. Curr. Drug Targets, 2, 285 298.
58. Yan, L., Takekida, S., Shigeyoshi, Y. Okamura, H. (1999) Per1 and Per2 gene expression in the rat suprachiasmatic nucleus: circadian profile and the compartment-specific response to light. Neuroscience, 94, 141 150.