Pituitary Adenylate Cyclase Activating Peptide Phase Shifts Circadian Rhythms in a Manner Similar to Light

Overview

Journal J Neurosci

Specialty Neurology

Date 1999 Jul 22

PMID 10414992

Citations 39

Authors

M E Harrington

S Hoque

A Hall

D Golombek

S Biello

Affiliations

Soon will be listed here.

Abstract

The endogenous circadian pacemaker in mammals is located in the suprachiasmatic nuclei (SCN) of the hypothalamus. Various cues can reset circadian rhythm phase, thereby entraining the internal rhythm to the environmental cycle, and these effects can be investigated using an in vitro method to measure phase shifts of the SCN. Although pituitary adenylate cyclase activating peptide (PACAP) is localized in retinal inputs to the SCN, it has been reported to alter clock phase only during the subjective day (Hannibal et al., 1997), whereas light alters phase only in the subjective night. In this study we show that PACAP can reset the clock in the photic pattern during the subjective night when applied in 10 pM to 1 nM doses. This appears to be mediated via a glutamatergic mechanism, possibly by potentiation of NMDA currents as is seen at 10-100 pM. Given at higher doses (>10 nM), PACAP shifts in the subjective day, apparently via activation of adenylate cyclase and increased intracellular cAMP. These results indicate dose and phase specificity of the effects of PACAP, and a new role as a transmitter in the retinohypothalamic tract.

Citing Articles

Dexmedetomidine accelerates photoentrainment and affects sleep structure through the activation of SCN neurons.

Zhang Y, Wang W, Li J, Zhao D, Shu Y, Jia X Commun Biol. 2024; 7(1):1707.

PMID: 39730868 PMC: 11680882. DOI: 10.1038/s42003-024-07430-9.

Comparative Neurology of Circadian Photoreception: The Retinohypothalamic Tract (RHT) in Sighted and Naturally Blind Mammals.

Hannibal J Front Neurosci. 2021; 15:640113.

PMID: 34054403 PMC: 8160255. DOI: 10.3389/fnins.2021.640113.

Ion Channels Controlling Circadian Rhythms in Suprachiasmatic Nucleus Excitability.

Harvey J, Plante A, Meredith A Physiol Rev. 2020; 100(4):1415-1454.

PMID: 32163720 PMC: 7717126. DOI: 10.1152/physrev.00027.2019.

Circulating PACAP peptide and PAC1R genotype as possible transdiagnostic biomarkers for anxiety disorders in women: a preliminary study.

Ross R, Hoeppner S, Hellberg S, ODay E, Rosencrans P, Ressler K Neuropsychopharmacology. 2020; 45(7):1125-1133.

PMID: 31910434 PMC: 7235237. DOI: 10.1038/s41386-020-0604-4.

Pituitary Adenylate Cyclase-Activating Peptide (PACAP)-Glutamate Co-transmission Drives Circadian Phase-Advancing Responses to Intrinsically Photosensitive Retinal Ganglion Cell Projections by Suprachiasmatic Nucleus.

Lindberg P, Mitchell J, Burgoon P, Beaule C, Weihe E, Schafer M Front Neurosci. 2019; 13:1281.

PMID: 31866806 PMC: 6909886. DOI: 10.3389/fnins.2019.01281.

References

Meijer J, Watanabe K, Detari L, De Vries M, Albus H, Treep J . Light entrainment of the mammalian biological clock. Prog Brain Res. 1996; 111:175-90. DOI: 10.1016/s0079-6123(08)60407-0. View

PELLEGRI G, Magistretti P, Martin J . VIP and PACAP potentiate the action of glutamate on BDNF expression in mouse cortical neurones. Eur J Neurosci. 1998; 10(1):272-80. DOI: 10.1046/j.1460-9568.1998.00052.x. View

Harrington M, Hoque S . NPY opposes PACAP phase shifts via receptors different from those involved in NPY phase shifts. Neuroreport. 1997; 8(12):2677-80. DOI: 10.1097/00001756-199708180-00008. View

Shibuya I, Noguchi J, Tanaka K, Harayama N, Inoue U, Kabashima N . PACAP increases the cytosolic Ca2+ concentration and stimulates somatodendritic vasopressin release in rat supraoptic neurons. J Neuroendocrinol. 1998; 10(1):31-42. DOI: 10.1046/j.1365-2826.1998.00168.x. View

Ebling F . The role of glutamate in the photic regulation of the suprachiasmatic nucleus. Prog Neurobiol. 1996; 50(2-3):109-32. DOI: 10.1016/s0301-0082(96)00032-9. View

Martin J, Gasser D, Magistretti P . Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide potentiate c-fos expression induced by glutamate in cultured cortical neurons. J Neurochem. 1995; 65(1):1-9. DOI: 10.1046/j.1471-4159.1995.65010001.x. View

Fukuhara C, Suzuki N, Matsumoto Y, Nakayama Y, Aoki K, Tsujimoto G . Day-night variation of pituitary adenylate cyclase-activating polypeptide (PACAP) level in the rat suprachiasmatic nucleus. Neurosci Lett. 1997; 229(1):49-52. DOI: 10.1016/s0304-3940(97)00415-1. View

Kopp M, Meissl H, Korf H . The pituitary adenylate cyclase-activating polypeptide-induced phosphorylation of the transcription factor CREB (cAMP response element binding protein) in the rat suprachiasmatic nucleus is inhibited by melatonin. Neurosci Lett. 1997; 227(3):145-8. DOI: 10.1016/s0304-3940(97)00312-1. View

Masuo Y, Suzuki N, Matsumoto H, Tokito F, Matsumoto Y, Tsuda M . Regional distribution of pituitary adenylate cyclase activating polypeptide (PACAP) in the rat central nervous system as determined by sandwich-enzyme immunoassay. Brain Res. 1993; 602(1):57-63. DOI: 10.1016/0006-8993(93)90241-e. View

10.

Hannibal J, Ding J, Chen D, Fahrenkrug J, Larsen P, Gillette M . Pituitary adenylate cyclase-activating peptide (PACAP) in the retinohypothalamic tract: a potential daytime regulator of the biological clock. J Neurosci. 1997; 17(7):2637-44. PMC: 6573509. View

11.

Kornhauser J, Ginty D, Greenberg M, Mayo K, Takahashi J . Light entrainment and activation of signal transduction pathways in the SCN. Prog Brain Res. 1996; 111:133-46. DOI: 10.1016/s0079-6123(08)60405-7. View

12.

Stella N, Magistretti P . Vasoactive intestinal peptide (VIP) and pituitary adenylate cyclase-activating polypeptide (PACAP) potentiate the glutamate-evoked release of arachidonic acid from mouse cortical neurons. Evidence for a cAMP-independent mechanism. J Biol Chem. 1996; 271(39):23705-10. DOI: 10.1074/jbc.271.39.23705. View

13.

Spengler D, Waeber C, Pantaloni C, Holsboer F, Bockaert J, Seeburg P . Differential signal transduction by five splice variants of the PACAP receptor. Nature. 1993; 365(6442):170-5. DOI: 10.1038/365170a0. View

14.

Mrosovsky N . A non-photic gateway to the circadian clock of hamsters. Ciba Found Symp. 1995; 183:154-67; discussion 167-74. DOI: 10.1002/9780470514597.ch9. View

15.

Liu G, Madsen B . PACAP38 modulates activity of NMDA receptors in cultured chick cortical neurons. J Neurophysiol. 1997; 78(4):2231-4. DOI: 10.1152/jn.1997.78.4.2231. View

16.

Wu S, Dun N . Potentiation of NMDA currents by pituitary adenylate cyclase activating polypeptide in neonatal rat sympathetic preganglionic neurons. J Neurophysiol. 1997; 78(2):1175-9. DOI: 10.1152/jn.1997.78.2.1175. View

17.

Liu G, Madsen B . Modulatory action of PACAP27 on NMDA receptor channel activity in cultured chick cortical neurons. Brain Res. 1998; 791(1-2):290-4. DOI: 10.1016/s0006-8993(97)01567-9. View

18.

Yada T, Sakurada M, Ihida K, Nakata M, Murata F, Arimura A . Pituitary adenylate cyclase activating polypeptide is an extraordinarily potent intra-pancreatic regulator of insulin secretion from islet beta-cells. J Biol Chem. 1994; 269(2):1290-3. View

19.

Morio H, Tatsuno I, Hirai A, Tamura Y, Saito Y . Pituitary adenylate cyclase-activating polypeptide protects rat-cultured cortical neurons from glutamate-induced cytotoxicity. Brain Res. 1996; 741(1-2):82-8. DOI: 10.1016/s0006-8993(96)00920-1. View

20.

von Gall C, Duffield G, Hastings M, Kopp M, Dehghani F, Korf H . CREB in the mouse SCN: a molecular interface coding the phase-adjusting stimuli light, glutamate, PACAP, and melatonin for clockwork access. J Neurosci. 1998; 18(24):10389-97. PMC: 6793329. View