Roles of light and serotonin in the regulation of gastrin-releasing peptide and arginine vasopressin output in the hamster SCN circadian clock

European Journal of Neuroscience

Volumn 32, Issue 7, 2010, Pages 1170-1179

  Francl, Jessica M ^a   Kaur, Gagandeep ^a   Glass, J David ^a  

^a KENT STATE UNIVERSITY   (United States)

Author keywords

Glutamate; Microdialysis; Neuropeptide; Photic input; Serotonin; Suprachiasmatic nucleus

Indexed keywords

ARGIPRESSIN; GASTRIN RELEASING PEPTIDE; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CIRCADIAN RHYTHM; CONTROLLED STUDY; DARKNESS; EXPOSURE; HAMSTER; HORMONAL REGULATION; HORMONE RELEASE; LIGHT; LIGHT DARK CYCLE; MALE; MICRODIALYSIS; NERVE CELL; NONHUMAN; PACEMAKER; PHOTOSTIMULATION; PRIORITY JOURNAL; RADIOIMMUNOASSAY; REGULATORY MECHANISM; RETINA; SUPRACHIASMATIC NUCLEUS;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ANIMALS; ARGININE VASOPRESSIN; CIRCADIAN CLOCKS; CRICETINAE; EXCITATORY AMINO ACID AGONISTS; GASTRIN-RELEASING PEPTIDE; LIGHT; MALE; MESOCRICETUS; MICRODIALYSIS; N-METHYLASPARTATE; PHOTIC STIMULATION; SEROTONIN; SEROTONIN RECEPTOR AGONISTS; SUPRACHIASMATIC NUCLEUS; TIME FACTORS;

EID: 78049250531     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07374.x     Document Type: Article

References (84)

1. Abe, H., Rusak, B. & Robertson, H.A. (1991) Photic induction of fos protein in the suprachiasmatic nucleus is inhibited by the NMDA receptor antagonist MK-801. Neurosci. Lett., 127, 9-12.
2. Abe, H., Robertson, H.A. & Rusak, B. (1992) NMDA and non-NMDA receptor antagonists inhibit photic induction of Fos protein in the hamster suprachiasmatic nucleus. Brain Res. Bull., 28, 831-835.
3. Abrahamson, E.E. & Moore, R.Y. (2001) Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res., 916, 172-191.
4. Aida, R., Moriya, T., Araki, M., Akiyama, M., Wada, K., Wada, E. & Shibata, S. (2002) Gastrin-releasing peptide mediates photic entrainable signals to dorsal subsets of suprachiasmatic nucleus via induction of Period gene in mice. Mol. Pharmacol., 61, 26-34.
5. Aioun, J., Chambille, I., Peytevin, J. & Martinet, L. (1998) Neurons containing gastrin-releasing peptide and vasoactive intestinal polypeptide are involved in the reception of the photic signal in the suprachiasmatic nucleus of the Syrian hamster: an immunocytochemical ultrastructural study. Cell Tissue Res., 291, 239-253.
6. Albers, H.E. & Ferris, C.F. (1984) Neuropeptide Y: role in light-dark cycle entrainment of hamster circadian rhythms. Neurosci. Lett., 50, 163-168.
7. Antle, M.C. & Silver, R. (2005) Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci., 28, 145-151.
8. Antle, M.C., Kriegsfeld, L.J. & Silver, R. (2005) Signaling within the master clock of the brain: localized activation of mitogen-activated protein kinase by gastrin-releasing peptide. J. Neurosci., 25, 2447-2454.
9. Belle, M.D.C., Diekman, C.O., Forger, D.B. & Piggins, H.D. (2009) Daily electrical silencing in the mammalian circadian clock. Science, 326, 281-284.
10. Benveniste, H. (1989) Brain microdialysis. J. Neurochem., 52, 1667-1669.
11. Biello, S.M., Janik, D. & Mrosovsky, N. (1994) Neuropeptide Y and behaviorally induced phase shifts. Neuroscience, 62, 273-279.
12. Buijs, R.M. (1996) The anatomical basis for the expression of circadian rhythms: the efferent projections of the suprachiasmatic nucleus. Prog. Brain Res., 111, 229-240.
13. Cagampang, F.R.A., Yang, J., Nakayama, Y., Fukuhara, C. & Inouye, S. (1994) Circadian variation of arginine-vasopressin messenger RNA in the rat suprachiasmatic nucleus. Mol. Brain Res., 24, 179-184.
14. Card, J.P. & Moore, R.Y. (1982) Ventral lateral geniculate nucleus efferents to the rat suprachiasmatic nucleus exhibit avian pancreatic polypeptide-like immunoreactivity. J. Comp. Neurol., 206, 390-396.
15. Castel, M., Feinstein, N., Cohen, S. & Harari, N. (1990) Vasopressinergic innervation of the mouse suprachiasmatic nucleus: an immuno-electron microscopic analysis. J. Comp. Neurol., 298, 172-187.
16. Cayetanot, F., Bentivoglio, M. & Aujard, F. (2005) Arginine-vasopressin and vasointestinal polypeptide rhythms in the suprachiasmatic nucleus of the mouse lemur reveal aging-related alterations of circadian pacemaker neurons in a non-human primate. Eur. J. Neurosci., 22, 902-910.
17. Dardente, H., Poirel, V., Klosen, P., Pévet, P. & Masson-Pévet, M. (2002) Per and neuropeptide expression in the rat suprachiasmatic nuclei: compartmentalization and differential cellular induction by light. Brain Res., 958, 261-271.
18. Dardente, H., Menet, J.S., Challet, E., Tournier, B.B., Pévet, P. & Masson-Pévet, M. (2004) Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents. Mol. Brain Res., 124, 143-151.
19. 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.
20. Dudley, T.E., DiNardo, L.A. & Glass, J.D. (1998) Endogenous regulation of serotonin release in the hamster suprachiasmatic nucleus. J. Neurosci., 18, 5045-5052.
21. Earnest, D.J. & Sladek, C.D. (1987) Circadian rhythms of vasopressin release from individual rat suprachiasmatic explants in vitro. Brain Res., 382, 129-133.
22. Earnest, D.J., DiGiorgio, S. & Olschowka, J.A. (1993) Light induces expression of fos-related proteins within gastrin-releasing peptide neurons in the rat suprachiasmatic nucleus. Brain Res., 627, 205-209.
23. Gamble, K.L., Novak, C.M. & Albers, H.A. (2004) Neuropeptide Y and N-methyl-D-aspartic acid interact within the suprachiasmatic nuclei to alter circadian phase. Neuroscience, 126, 559-565.
24. Gamble, K.L., Allen, G.C., Zhou, T. & McMahon, D.G. (2007) Gastrin-releasing peptide mediates light-like phase resetting of the suprachiasmatic nucleus circadian pacemaker through cAMP response element-binding protein and Per1 activation. J. Neurosci., 27, 12078-12087.
25. 1A mixed agonists/antagonists elicit large-magnitude phase shifts in hamster circadian wheel-running rhythms. Neuroscience, 119, 567-576.
26. Gerkema, M.P., Van der Zee, E.A. & Feitsma, L.E. (1994) Expression of circadian rhythmicity correlates with the number of arginine-vasopressin-immunoreactive cells in the suprachiasmatic nucleus of common voles, Microtus arvalis. Brain Res., 639, 93-101.
27. Gillette, M.U. & Reppert, S.M. (1987) The hypothalamic suprachiasmatic nuclei: circadian patterns of vasopressin secretion and neuronal activity in vitro. Brain Res. Bull., 19, 135-139.
28. Glass, J.D., Grossman, G., Farnbauch, L. & DiNardo, L. (2003) Midbrain raphe modulation of nonphotic circadian clock resetting and 5-HT release in the mammalian suprachiasmatic nucleus. J. Neurosci., 23, 7451-7460.
29. Gunther, O., Landgraf, R., Schuart, J. & Unger, H. (1984) Vasopressin in cerebrospinal fluid (CSF) and plasma of conscious rabbits - circadian variations. Exp. Clin. Endocrinol., 83, 367-369.
30. Hamada, T., LeSauter, J., Lokshin, M., Romero, M.T., Yan, L., Venuti, J.M. & Silver, R. (2003) Calbindin influences response to photic input in suprachiasmatic nucleus. J. Neurosci., 23, 8820-8826.
31. Hamada, T., Antle, M. & Silver, R. (2004) The role of Period1 in nonphotic resetting of the hamster circadian pacemaker in the suprachiasmatic nucleus. Neurosci. Lett., 362, 87-90.
32. Jin, X., Shearman, L.P., Weaver, D.R., Zylka, M.J. & De Vries, G.J. (1999) A molecular mechanism regulating output from the suprachiasmatic circadian clock. Cell, 96, 57-68.
33. Johnson, R.F., Morin, L.P. & Moore, R.Y. (1988) Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Res., 462, 301-312.
34. Johnson, R.F., Moore, R.Y. & Morin, L.P. (1989) Lateral geniculate lesions alter circadian activity rhythms in the hamster. Brain Res. Bull., 22, 411-422.
35. Jolkkonen, J., Tuomisto, L., Van Wimersma Greidanus, T.N. & Riekkinen, P.J. (1988) Vasopressin levels in the cerebrospinal fluids of rats with lesions of the paraventricular and suprachiasmatic nuclei. Neurosci. Lett., 86, 184-188.
36. Kalsbeek, A., Teclemariam-Mesbah, R. & Pévet, P. (1993) Efferent projections of the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus). J. Comp. Neurol., 332, 293-314.
37. Kalsbeek, A., Buijs, R.M., Engelmann, M., Wotjak, C.T. & Landgraf, R. (1995) In vivo measurement of a diurnal variation in vasopressin release in the rat suprachiasmatic nucleus. Brain Res., 682, 75-82.
38. Kalsbeek, A., Van Heerikhuize, J., Wortel, J. & Buijs, R. (1996) A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by time intrahypothalamic administration of the vasopressin V1 antagonist. J. Neurosci., 16, 5555-5565.
39. Kalsbeek, A., Van Heerikhuize, J.J., Wortel, J. & Buijs, R.M. (1998) Restricted daytime feeding modifies suprachiasmatic nucleus vasopressin release in rats. J. Biol. Rhythms, 13, 18-29.
40. Kalsbeek, A., Palm, I.F., La Fleur, S.E., Scheer, F.A.J.L., Perreau-Lenz, S., Ruiter, M., Kreier, F., Cailotto, C. & Buijs, R.M. (2006) SCN outputs and the hypothalamic balance of life. J. Biol. Rhythms, 21, 458-469.
41. Kalsbeek, A., Verhagen, L., Schalij, I., Foppen, E., Saboureau, M., Bothorel, B., Buijs, R. & Pévet, P. (2008) Opposite actions of hypothalamic vasopressin on circadian corticosterone rhythm in nocturnal versus diurnal species. Eur. J. Neursci., 27, 818-827.
42. Karatsoreos, I.N., Yan, L., LeSauter, J. & Silver, R. (2004) Phenotype matters: identification of light-responsive cells in the mouse suprachiasmatic nucleus. J. Neurosci., 24, 68-75.
43. Karatsoreos, I.N., Romeo, R.D., McEwen, B.S. & Silver, R. (2006) Diurnal regulation of the gastrin-releasing peptide receptor in the mouse circadian clock. Eur. J. Neurosci., 23, 1047-1053.
44. Klein, D.C., Moore, R.Y. & Reppert, S.M. (1991) Suprachiasmatic Nucleus: The Mind's Clock. Oxford University Press, New York.
45. 28k cells selectively contact intra-SCN neurons. Neuroscience, 111, 575-585.
46. Li, J.D., Burton, K.J., Zhang, C., Hu, S.B. & Zhou, Q.Y. (2009) Vasopressin receptor V1a regulates circadian rhythms of locomotor activity and expression of clock-controlled genes in the suprachiasmatic nuclei. Am. J. Physiol. Regul. Integr. Comp. Physiol., 296, R824-R830.
47. Marchant, E.G., Watson, N.V. & Mistlberger, R.E. (1997) Both neuropeptide Y and serotonin are necessary for entrainment of circadian rhythms in mice by daily treadmill running schedules. J. Neurosci., 17, 7974-7987.
48. McArthur, A., Coogan, A., Ajpru, S., Sugden, D., Biello, S. & Piggins, H. (2000) Gastrin-releasing peptide phase-shifts suprachiasmatic nuclei neuronal rhythms in vitro. J. Neurosci., 20, 5496-5502.
49. Meyer-Bernstein, E.L. & Morin, L.P. (1996) Differential serotonergic innervation of the suprachiasmatic nucleus and the intergeniculate leaflet and its role in circadian rhythm modulation. J. Neurosci., 16, 2097-2111.
50. Mihai, R., Juss, T.S. & Ingram, C.D. (1994) Suppression of suprachiasmatic nucleus neurone activity with a vasopressin receptor antagonist: possible role for endogenous vasopressin in circadian activity cycles in vitro. Neurosci. Lett., 179, 95-99.
51. Mikkelson, J.D., Larsen, P.J., O' Hare, M.M.T. & Wiegand, S.J. (1991) Gastrin releasing peptide in the rat suprachiasmatic nucleus: an immunohisotchemical, chromatographic and radioimmunological study. Neuroscience, 40, 55-66.
52. Moore, R.Y. (1983) Organization and function of a central nervous system circadian oscillator: the suprachiasmatic hypothalamic nucleus. Fed. Proc., 42, 2783-2789.
53. Moore, R.Y. & Lenn, N.J. (1972) A retinohypothalamic projection in the rat. J. Comp. Neurol., 146, 1-14.
54. Moore, R.Y., Speh, J.C. & Leak, R.K. (2002) Suprachiasmatic nucleus organization. Cell Tissue Res., 309, 89-98.
55. Morin, L.P., Shivers, K.-Y., Blanchard, J.H. & Muscat, L. (2006) Complex organization of mouse and rat suprachiasmatic nucleus. Neuroscience, 137, 1285-1297.
56. Nishino, H. & Koizumi, K. (1977) Responses of neurons in the suprachiasmatic nuclei of the hypothalamus to putative transmitters. Brain Res., 120, 167-172.
57. Palm, I.F., Van Der Beek, E.M., Wiegant, V.M., Buijs, R.M. & Kalsbeek, A. (1999) Vasopressin induces an LH surge in ovariectomized, estradiol-treated rats with lesion of the suprachiasmatic nucleus. Neuroscience, 93, 659-666.
58. Perlow, M.J., Reppert, S.M., Artman, H.A., Fisher, D.A., Seif, S.M. & Robinson, A.G. (1982) Oxytocin, vasopressin, and estrogen-stimulated neurophysin: daily patterns of concentration in cerebrospinal fluid. Science, 216, 1416-1418.
59. Pickard, G.E. (1982) The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection. J. Comp. Neurol., 211, 65-83.
60. Piggins, H.D., Cutler, D.J. & Rusak, B. (1994) Effects of ionophoretically applied bombesin-like peptides on hamster suprachiasmatic nucleus neurons in vitro. Eur. J. Pharmacol., 271, 413-419.
61. Piggins, H.D., Antle, M.C. & Rusak, B. (1995) Neuropeptides phase shift the mammalian circadian pacemaker. J. Neurosci., 15, 5612-5622.
62. Piggins, H.D., Goguen, D. & Rusak, B. (2005) Gastrin-releasing peptide induces c-Fos in the hamster suprachiasmatic nucleus. Neurosci. Lett., 384, 205-210.
63. Rea, M.A. & Pickard, G.E. (2000) Serotonergic modulation of photic entrainment in the Syrian hamster. Biol. Rhythm Res., 31, 284-314.
64. Rea, M.A., Buckley, B. & Lutton, L.M. (1993) Local administration of EAA antagonists blocks light-induced phase shifts and c-fos expression in hamster SCN. J. Physiol., 265, R1191-R1198.
65. Rea, M.A., Glass, J.D. & Colwell, C.S. (1994) Serotonin modulates photic responses in the hamster suprachiasmatic nuclei. J. Neurosci., 14, 3635-3642.
66. Rea, M.A., Barrera, J., Glass, J.D. & Gannon, R.L. (1995) Serotonergic potentiation of photic phase shifts of the circadian activity rhythm. Neuroreport, 6, 1417-1420.
67. Reghunandanan, V. & Reghunandanan, R. (2006) Neurotransmitters of the suprachiasmatic nuclei. J. Circadian Rhythms, 4, 2.
68. Rusak, B. & Zucker, I. (1979) Neural regulation of circadian rhythms. Physiol. Rev.59, 449-526.
69. Schwartz, W.J. & Reppert, S.M. (1985) Neural regulation of the circadian vasopressin rhythm in cerebrospinal fluid: a pre-eminent role for the suprachiasmatic nuclei. J. Neurosci., 5, 2771-2778.
70. Schwartz, W.J., Coleman, R.J. & Reppert, S.M. (1983) A daily vasopressin rhythm in rat cerebrospinal fluid. Brain Res., 263, 105-112.
71. Selim, M., Glass, J.D., Hauser, U.E. & Rea, M.A. (1993) Serotonergic inhibition of light-induced Fos protein expression and extracellular glutamate in the suprachiasmatic nuclei. Brain Res., 621, 181-188.
72. Shibata, S., Oomura, Y., Hattori, K. & Hitoshi, K. (1984) Responses of suprachiasmatic nucleus neurons to optic nerve stimulation in rat hypothalamic slice preparation. Brain Res., 302, 83-89.
73. Shinohara, K., Tominaga, K., Isobe, Y. & Inouye, S.T. (1993) Photic regulation of peptides located in the ventrolateral subdivision of the suprachiasmatic nucleus of the rat: daily variations of vasoactive intestinal polypeptide, gastrin-releasing peptide, and neuropeptide Y. J. Neurosci., 13, 793-800.
74. Shinohara, K., Honma, S., Katsuno, Y., Abe, H. & Honma, K. (1995) Two distinct oscillators in the rat suprachiasmatic nucleus in vitro. Proc. Natl Acad. Sci. USA, 92, 7396-7400.
75. Shinohara, K., Hiruma, H., Funabashi, T. & Kimura, F. (2000) GABAergic modulation of gap junction communication in slice cultures of the rat suprachiasmatic mucleus. Neuroscience, 96, 591-596.
76. Shirakawa, T., Honma, S. & Honma, K. (2001) Multiple oscillators in the suprachiasmatic nucleus. Chronobiol. Int., 18, 371-387.
77. 1A mixed agonist/antagonist NAN-190: intra-suprachiasmatic nucleus pathway. Neuroscience, 153, 571-580.
78. Tanaka, M., Hayashi, S., Tamada, Y., Ikeda, T., Hisa, Y., Takamatsu, T. & Ibata, Y. (1997) Direct retinal projections to GRP neurons in the suprachiasmatic nucleus of the rat. Neuroreport, 8, 2187-2191.
79. Tominaga, K., Shinohara, K., Otori, Y., Fukuhara, C. & Inouye, S.T. (1992) Circadian rhythms of vasopressin content in the suprachiasmatic nucleus of the rat. Neuroreport, 3, 809-812.
80. Van de Kar, L.D. (1991) Neuroendocrine pharmacology of serotonergic (5-HT) neurons. Annu. Rev. Pharmacol. Toxicol., 31, 289-320.
81. Watanabe, K., Koibuchi, N., Ohtake, H. & Yamaoka, S. (1993) Circadian rhythms of vasopressin release in primary cultures of rat suprachiasmatic nucleus. Brain Res., 624, 115-120.
82. Yambe, Y., Arima, H., Kakiya, S., Murase, T. & Oiso, Y. (2002) Diurnal changes in arginine vasopressin gene transcription in the rat suprachiasmatic nucleus. Mol. Brain Res., 104, 132-136.
83. Young, W.S.I., Kovács, K. & Lolait, S.J. (1993) The diurnal rhythm in vasopressin V1a receptor expression in the suprachiasmatic nucleus is not dependent on vasopressin. Endocrinology, 133, 585-590.
84. Zar, J.H. (1983) Biostatistical Analysis. Prentice Hall, Englewood Cliffs, NJ.