Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons

Nature Neuroscience

Volumn 8, Issue 4, 2005, Pages 476-483

  Aton, Sara J ^a   Colwell, Christopher S ^b   Harmar, Anthony J ^c   Waschek, James ^b   Herzog, Erik D ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

VASOACTIVE INTESTINAL POLYPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR; CYCLOPEPTIDE; RO 25 1553; RO 25-1553; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 2;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SYNCHRONIZATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DARKNESS; GENE; HORMONE ACTION; MOUSE; NONHUMAN; PHOTOPERIODICITY; PRIORITY JOURNAL; SUPRACHIASMATIC NUCLEUS; VIPR2 GENE; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL; BIOLOGICAL RHYTHM; C57BL MOUSE; CELL CULTURE; CHI SQUARE DISTRIBUTION; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; GENETICS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; METABOLISM; METHODOLOGY; MOTOR ACTIVITY; MOUSE MUTANT; NERVE CELL; NEWBORN; PHYSIOLOGY; TIME;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BIOLOGICAL CLOCKS; CELLS, CULTURED; CHI-SQUARE DISTRIBUTION; CIRCADIAN RHYTHM; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NEURONS; PEPTIDES, CYCLIC; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE, TYPE II; SUPRACHIASMATIC NUCLEUS; TIME FACTORS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 20044362444     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1419     Document Type: Article

References (50)

1. Kalsbeek, A. & Buijs, R.M. Output pathways of the mammalian suprachiasmatic nucleus: coding circadian time by transmitter selection and specific targeting. Cell Tissue Res. 309, 109-118 (2002).
2. Reppert, S.M. & Weaver, D.R. Coordination of circadian timing in mammals. Nature 418, 935-941 (2002).
3. Van Gelder, R.N., Herzog, E.D., Schwartz, W.J. & Taghert, P.M. Circadian rhythms: in the loop at last. Science 300, 1534-1535 (2003).
4. 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, 697-706 (1995).
5. Herzog, E.D., Takahashi, J.S. & Block, G.D. Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nat. Neurosci. 1, 708-713 (1998).
6. Honma, S., Shirakawa, T., Katsuno, Y., Namihira, M. & Honma, K. I. Circadian periods of single suprachiasmatic neurons in rats. Neurosci. Lett. 250, 157-160 (1998).
7. Yamaguchi, S. et al. Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 302, 1408-1412 (2003).
8. Quintero, J.E., Kuhlman, S.J. & McMahon, D.G. The biological clock nucleus: a multiphasic oscillator network regulated by light. J. Neurosci. 23, 8070-8076 (2003).
9. Schaap, J. et al. Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding. Proc. Natl. Acad. Sci. USA 100, 15994-15999 (2003).
10. Herzog, E.D., Geusz, M.E., Khalsa, S.B.S., Straume, M. & Block, G.D. Circadian rhythms in mouse suprachiasmatic nucleus explants on multimicroelectrode plates. Brain Res. 757, 285-290 (1997).
11. Liu, C. & Reppert, S.M. GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 25, 123-128 (2000).
12. Colwell, C.S. Rhythmic coupling among cells in the suprachiasmatic nucleus. J. Neurobiol. 43, 379-388 (2000).
13. Long, M.A., Jutras, M.J., Connors, B.W. & Burwell, R.D. Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat. Neurosci. 8, 61-66 (2005).
14. Jiang, Z.G., Yang, Y.Q. & Allen, C.N. Tracer and electrical coupling of rat suprachiasmatic nucleus neurons. Neuroscience 77, 1059-1066 (1997).
15. Nakamura, W., Honma, S., Shirakawa, T. & Honma, K.-I. Regional pacemakers composed of multiple oscillator neurons in the rat suprachiasmatic nucleus. Eur. J. Neurosci. 14, 666-674 (2001).
16. Herzog, E.D., Aton, S.J., Numano, R., Sakaki, Y. & Tei, H. Temporal precision in the mammalian circadian system: a reliable clock from less reliable neurons. J. Biol. Rhythms 19, 35-46 (2004).
17. Abrahamson, E.E. & Moore, R.Y. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res. 916, 172-191 (2001).
18. Cutler, D.J. et al. The mouse VPAC2 receptor confers suprachiasmatic nuclei cellular rhythmicity and responsiveness to vasoactive intestinal polypeptide in vitro. Eur. J. Neurosci. 17, 197-204 (2003).
19. Reed, H.E. et al. Effects of vasoactive intestinal polypeptide on neurones of the rat suprachiasmatic nuclei in vitro. J. Neuroendocrinol. 14, 639-646 (2002).
20. Cagampang, F.R., Sheward, W.J., Harmar, A.J., Piggins, H.D. & Coen, C.W. Circadian changes in the expression of vasoactive intestinal peptide 2 receptor mRNA in the rat suprachiasmatic nuclei. Brain Res. Mol. Brain Res. 54, 108-112 (1998).
21. Piggins, H.D., Antle, M.C. & Rusak, B. Neuropeptides phase shift the mammalian circadian pacemaker. J. Neurosci. 15, 5612-5622 (1995).
22. Watanabe, K., Vanecek, J. & Yamaoka, S. In vitro entrapment of the circadian rhythm of vasopressin-releasing cells in suprachiasmatic nucleus by vasoactive intestinal polypeptide. Brain Res. 877, 361-366 (2000).
23. Reed, H.E., Meyer-Spasche, A., Cutler, D.J., Coen, C.W. & Piggins, H.D. Vasoactive intestinal polypeptide (VIP) phase-shifts the rat suprachiasmatic nucleus clock in vitro. Eur. J. Neurosci. 13, 839-843 (2001).
24. Nielsen, H.S., Hannibal, J. & Fahrenkrug, J. Vasoactive intestinal polypeptide induces per1 and per2 gene expression in the rat suprachiasmatic nucleus late at night. Eur. J. Neurosci. 15, 570-574 (2002).
25. van den Pol, A.N. & Gores, T. Synaptic relationships between neurons containing vasopressin, gastrin-releasing peptide, vasoactive intestinal polypeptide, and glutamate decarboxylase immunoreactivity in the suprachiasmatic nucleus: dual ultrastructural immunocytochemistry with gold- substituted silver peroxidase. J. Comp. Neurol. 252, 507-521 (1986).
26. Daikoku, S., Hisano, S. & Kagotani, Y. Neuronal associations in the rat suprachiasmatic nucleus demonstrated by immunoelectron microscopy. J. Comp. Neurol. 325, 559-571 (1992).
27. Shen, S. et al. Overexpression of the human VPAC2 receptor in the suprachiasmatic nucleus alters the circadian phenotypeof mice. Proc. Natl. Acad. Sci. USA 97, 11575-11580 (2000).
28. Hughes, A.T., Fahey, B., Cutler, D.J., Coogan, A.N. & Piggins, H.D. Aberrant gating of photic input to the suprachiasmatic circadian pacemaker of mice lacking the VPAC2 receptor. J. Neurosci. 24, 3522-3526 (2004).
29. Harmar, A.J. et al. The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 109, 497-508 (2002).
30. Colwell, C.S. et al. Disrupted circadian rhythms in VIP and PHI deficient mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R939-R949 (2003).
31. Itri, J., Michel, S., Waschek, J.A. & Colwell, C.S. Circadian rhythm in inhibitory synaptic transmission in the mouse suprachiasmatic nucleus. J. Neurophysiol. 92, 311-319 (2004).
32. Honma, S., Nakamura, W., Shirakawa, T. & Honma, K. Diversity in the circadian periods of single neurons of the rat suprachiasmatic nucleus depends on nuclear structure and intrinsic period. Neurosci. Lett. 358, 173-176 (2004).
33. Moody, T.W., Hill, J.M. & Jensen, R.T. VIP as a trophic factor in the CNS and cancer cells. Peptides 24, 163-177 (2003).
34. Kallo, I. et al. Transgenic approach reveals expression of the VPAC2 receptor in phenotypically defined neurons in the mouse suprachiasmatic nucleus and in its efferent target sites. Eur. J Neurosci 19, 2201-2211 (2004).
35. Peng, Y., Stoleru, D., Levine, J.D., Hall, J.C. & Rosbash, M. Drosophila free-running rhythms require intercellular communication. PLoS Biol. 1, E13 (2003).
36. Lin, Y., Stormo, G.D. & Taghert, P.H. The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J. Neurosci. 24, 7951-7957 (2004).
37. Deboer, T., Vansteensel, M.J., Detari, L. & Meijer, J.H. Sleep states alter activity of suprachiasmatic nucleus neurons. Nat. Neurosci. 10, 1086-1090 (2003).
38. Mistlberger, R.E. Effects of daily schedules of forced activity on free-running rhythms in the rat. J. Biol. Rhythms 6, 71-80 (1991).
39. Shinohara, K., Honma, S., Katsuno, Y., Abe, H. & Honma, K.-I. Two distinct oscillators in the rat suprachiasmatic nucleus in vitro. Proc. Natl. Acad. Sci. USA 92, 7396-7400 (1995).
40. Ban, Y., Shigeyoshi, Y. & Okamura, H. Development of vasoactive intestinal peptide mRNA rhythm in the rat suprachiasmatic nucleus. J. Neurosci. 17, 3920-3931 (1997).
41. Dardente, H. et al. Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents. Brain Res. Mol. Brain Res. 124, 143-151 (2004).
42. 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 199, 7728-7733 (2002).
43. Akiyama, M., Minami, Y., Nakajima, T., Moriya, T. & Shibata, S. Calcium and pituitary adenylate cyclase-activating polypeptide induced expression of circadian clock gene mPer1 in the mouse cerebellar granule cell culture. J. Neurochem. 78, 499-508 (2001).
44. Itri, J. & Colwell, C.S. Regulation of inhibitory synaptic transmission by vasoactive intestinal peptide (VIP) in the mouse suprachiasmatic nucleus. J. Neurophysiol. 90, 1589-1597 (2003).
45. 2- m single suprachiasmatic nucleus neurons. Neuron 38, 253-263 (2003).
46. Granados-Fuentes, D., Saxena, M.T., Prolo, L.M., Aton, S.J. & Herzog, E.D. Olfactory bulb neurons express functional, entramable Circadian rhythms. Eur. J. Neurosci. 19, 898-906 (2004).
47. Banker, G. & Goslin, K. in Culturing Nerve Cells (eds. Banker, G. & Goslin, K.) 75-118 (MIT Press, Cambridge, Massachusetts, USA, 1991).
48. Potter, S.M. & DeMarse, T.B. A new approach to neural cell culture for long-term studies. J. Neurosci. Methods 110, 17-24 (2001).
49. Sokolove, P.G. & Bushell, W.N. The chi square penodogram: its utility for analysis of Circadian rhythms. J. Theor. Biol. 72, 131-160 (1978).
50. Batschelet, E. in Mathematics in Biology (eds. Sibson, R. & Cohen, J.E.) 31-54 (Academic, New York, 1981).