Gastrin-releasing peptide promotes suprachiasmatic nuclei cellular rhythmicity in the absence of vasoactive intestinal polypeptide-VPAC2 receptor signaling

Journal of Neuroscience

Volumn 25, Issue 48, 2005, Pages 11155-11164

  Brown, Timothy M ^a   Hughes, Alun T ^a   Piggins, Hugh D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

BB2 receptor; Circadian; Electrophysiology; Entrainment; Hypothalamus; VIP

Indexed keywords

GASTRIN RELEASING PEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE ANTAGONIST; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN SLICE; CELL ACTIVITY; CIRCADIAN RHYTHM; CONTROLLED STUDY; ELECTRIC ACTIVITY; ELECTROPHYSIOLOGY; FEMALE; HORMONE ACTION; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RECEPTOR BLOCKING; RHYTHM; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; TRANSGENIC MOUSE;

ANIMALS; FEMALE; GASTRIN-RELEASING PEPTIDE; MALE; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; NEURONS; PERIODICITY; RECEPTORS, BOMBESIN; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE, TYPE II; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 30644473370     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3821-05.2005     Document Type: Article

References (54)

1. 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.
2. 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.
3. Albers HE, Liou S-Y, Stopa EG, Zoeller RT (1991) Interaction of colocalized neuropeptides: functional significance in the circadian timing system. J Neurosci 11:846-851.
4. Antle MC, Kriegsfeld LJ, 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.
5. Aton SJ, Colwell CS, Harmar AJ, Waschek J, Herzog ED (2005) Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat Neurosci 8:476-483.
6. Bouskila Y, Dudek FE (1993) Neuronal synchronization without calciumdependent synaptic transmission in the hypothalamus. Proc Natl Acad Sci USA 90:3207-3210.
7. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM, Zhou QY (2002) Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417:405-410.
8. Colwell CS (2000) Rhythmic coupling among cells in the suprachiasmatic nucleus. J Neurobiol 43:379-388.
9. Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, Lelievre V, Hu Z, Liu X, Waschek JA (2003) Disrupted circadian rhythms in VIP- and PHIdeficient mice. Am J Physiol Regul Intergr Comp Physiol 285:R939-R949.
10. 2 receptor confers suprachiasmatic nuclei cellular rhythmicity and responsiveness to vasoactive intestinal polypeptide in vitro. Eur J Neurosci 17:197-204.
11. Deboer T, Vansteensel MJ, Detari L, Meijer JH (2003) Sleep states alter activity of suprachiasmatic nucleus neurons. Nat Neurosci 6:1086-1090.
12. Edgar DM, DementWC (1991) Regularly scheduled voluntary exercise synchronizes the mouse circadian clock. Am J Physiol Regul Intergr Comp Physiol 261:R929-R933.
13. Gribkoff VK, Pieschl RL, Wisialowski TA, van den Pol AN, Yocca FD (1998) Phase shifting of circadian rhythms and depression of neuronal activity in the rat suprachiasmatic nucleus by neuropeptide Y: mediation by different receptor subtypes. J Neurosci 18:3014-3022.
14. Hannibal J, Fahrenkrug J (2003) Circadian rhythm regulation: a central role for the neuropeptide vasoactive intestinal polypeptide. Am J Physiol Regul Integr Comp Physiol 285:R935-R936.
15. Harmar AJ, Marston HM, Shen S, Spratt C, West KM, Sheward WJ, Morrison CF, Dorin JR, Piggins HD, Reubi JC, Kelly JS, Maywood ES, Hastings MH (2002) The VPAC2 receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 109:497-508.
16. Herzog ED, Takahashi JS, Block GD (1998) Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nat Neurosci 1:708-713.
17. Herzog ED, Aton SJ, Numano R, Sakaki Y, TeiH (2004) Temporal precision in the mammalian circadian system: a reliable clock from less reliable neurons. J Biol Rhythms 19:35-46.
18. 2 receptor. J Neurosci 24:3522-3526.
19. Jiang ZG, Yang YQ, Allen CN (1997) Tracer and electrical coupling of rat suprachiasmatic nucleus neurons. Neuroscience 77:1059-1066.
20. Jobst EE, Robinson DW, Allen CN (2004) Potential pathways for intercellular communication within the calbindin subnucleus of the hamster suprachiasmatic nucleus. Neuroscience 123:87-99.
21. Kawamoto K, Nagano M, Kanda F, Chihara K, Shigeyoshi Y, Okamura H (2003) Two types of VIP neuronal components in rat suprachiasmatic nucleus. J Neurosci Res 74:852-857.
22. Lin Y, Stormo GD, Taghert PH (2004) The neuropeptide pigmentdispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci 24:7951-7957.
23. Liu C, Reppert SM (2000) GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 25:123-128.
24. Long MA, Jutras MJ, Connors BW, Burwell RD (2005) Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat Neurosci 8:61-66.
25. Lundkvist GB, Kwak Y, Davis EK, Tei H, Block GD (2005) A calcium flux is required for circadian rhythm generation in mammalian pacemaker neurons. J Neurosci 25:7682-7686.
26. Maywood ES, Mrosovsky N, Field MD, Hastings MH (1999) Rapid downregulation of mammalian period genes during behavioral resetting of the circadian clock. Proc Natl Acad Sci USA 96:15211-15216.
27. Marchant EG, Mistlberger RE (1996) Entrainment and phase shifting of circadian rhythms in mice b forced treadmill running. Physiol Behav 60:657-663.
28. McArthur AJ, Coogan AN, Ajpru S, Sugden D, Biello SM, PigginsHD (2000) Gastrin-releasing peptide phase-shifts suprachiasmatic nuclei neuronal rhythms in vitro. J Neurosci 20:5496-5502.
29. Moreno D, Gourlet P, De Neef P, Cnudde J, Waelbroeck M, Robberecht P (2000) Development of selective agonists and antagonists for the human vasoactive intestinal polypeptide VPAC(2) receptor. Peptides 21:1543-1549.
30. Mori K, Miyazato M, Ida T, Murakami N, Serino R, Ueta Y, Kojima M, Kangawa K (2005) Identification of neuromedin S and its possible role in the mammalian circadian oscillator system. EMBO J 24:325-335.
31. Mrugala M, Zlomanczuk P, Jagota A, Schwartz WJ (2000) Rhythmic multiunit neural activity in slices of hamster suprachiasmatic nucleus reflect prior photoperiod. Am J Physiol Regul Intergr Comp Physiol 278:R987-R994.
32. Nitabach MN, Blau J, Holmes TC (2002) Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109:485-495.
33. Peng Y, Stoleru D, Levine JD, Hall JC, Rosbash M (2003) Drosophila free-running rhythms require intercellular communication. PLoS Biology 1:32-40.
34. Piggins HD, Cutler DJ (2003) The roles of vasoactive intestinal polypeptide in the mammalian circadian clock. J Endocrinol 177:7-15.
35. Piggins HD, Rusak B (1993) Electrophysiological effects of pressure-ejected bombesin-like peptides on hamster suprachiasmatic neurons in vitro. J Neuroendocrinol 5:575-581.
36. Piggins HD, Cutler DJ, Rusak B (1994) Effects of ionophoretically applied bombesin-like peptides on hamster suprachiasmatic nucleus neurons in vitro. Eur J Pharmacol 271:413-419.
37. Piggins HD, Antle MC, Rusak B (1995) Neuropeptides phase-shift the hamster circadian pacemaker. J Neurosci 15:5612-5622.
38. Piggins HD, Goguen D, Rusak B (2005) Gastrin-releasing peptide induces c-Fos in the hamster suprachiasmatic nucleus. Neurosci Lett 384:205-210.
39. Quintero JE, Kuhlman SJ, McMahon DG (2003) The biological clock nucleus: a multiphasic oscillator network regulated by light. J Neurosci 23:8070-8076.
40. Reed HE, Meyer-Spasche A, Cutler DJ, Coen CW, Piggins HD (2001) Vasoactive intestinal polypeptide phase-shifts the rat suprachiasmatic circadian clock in vitro. Eur J Neurosci 13:839-845.
41. Renn SC, Park JH, Rosbash M, Hall JC, Taghert PH (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99:791-802.
42. Reynolds T, Pinnock RD (1997) Neuromedin C decreases potassium conductance and increases a non-specific conductance in rat suprachiasmatic neurones in brain slices in vitro. Brain Res 750:67-80.
43. Romijn HJ, Sluiter AA, Pool CW, Wortel J, Buijs RM (1996) Differences in colocalization between Fos and PHI, GRP, VIP and VP in neurons of the rat suprachiasmatic nucleus after a light stimulus during the phase delay versus the phase advance period of the night. J Comp Neurol 372:1-8.
44. Romijn HJ, Sluiter AA, Wortel J, Van Uum JF, Buijs RM (1998) Immunocytochemical evidence for a diurnal rhythm of neurons showing colocalization of VIP with GRP in the rat suprachiasmatic nucleus. J Comp Neurol 391:397-405.
45. Schaap J, Meijer JH (2001) Opposing effects of behavioural activity and light on neurons of the suprachiasmatic nucleus. Eur J Neurosci 13:1955-1962.
46. Schaap J, Albus H, VanderLeest HT, Eilers PH, Detari L, Meijer JH (2003) Heterogeneity of rhythmic suprachiasmatic nucleus neurons: implications for circadian waveform and photoperiodic encoding. Proc Natl Acad Sci USA 100:15994-15999.
47. Schmahl C, Bohmer G (1997) Effects of excitatory amino acids and neuropeptide Y on the discharge activity of suprachiasmatic neurons in rat brain slices. Brain Res 746:151-163.
48. Shirakawa T, Honma S, Katsuno Y, Oguchi H, Honma K-I (2000) Synchronization of circadian firing rhythms in cultured rat surprachiasmatic neurons. Eur J Neurosci 12:2833-2838.
49. Sokolove PG, BushellWN (1978) The chi square periodogram: its utility for analysis of circadian rhythms. J Theor Biol 72:131-160.
50. Van den Pol AN, ObrietanK (2002) Short circuiting the circadian clock. Nat Neurosci 7:616-618.
51. Welsh DK, Logothetis DE, Meister M, Reppert SM (1995) Individual neurons from dissociated rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14:697-706.
52. Yamaguchi S, Isejima H, Matsuo T, Okura R, Yagita K, Kobayashi M, Okamura H (2003) Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 302:1408-1412.
53. Yamazaki S, Kerbeshian MC, Hocker CG, Block GD, Menaker M (1998) Rhythmic properties of the hamster suprachiasmatic nucleus in vivo. J Neurosci 18:10709-10723.
54. Zoeller RT, Broyles B, Earley J, Anderson ER, Albers HE (1992) Cellular levels of messenger ribonucleic acids encoding vasoactive intestinal peptide and gastrin-releasing peptide in neurons of the suprachiasmatic nucleus exhibit distinct 24-hour rhythms. J Neuroendocrinol 4:119-124.