Vasoactive intestinal polypeptide precursor mRNA exhibits diurnal variation in the rat suprachiasmatic nuclei

doi:10.1016/0169-328X(93)90049-U

Molecular Brain Research

Volume 20, Issue 3, November 1993, Pages 259-262

https://doi.org/10.1016/0169-328X(93)90049-U Get rights and content

Abstract

Vasoactive intestinal polypeptide (VIP), which is synthesized in the ventrolateral subdivision of the suprachiasmatic nucleus (SCN), the circadian pacemaker in the mammalian brain, is suggested to mediate information on environmental light. Diurnal rhythms of VIP precursor mRNA in the SCN was determined in the present study by Northern blot hybridization with an antisense RNA probe in rats kept under light-dark conditions. VIP precursor mRNA was found most abundant during the dark phase, as light exposure suppressed VIP precursor mRNA. This suppression, however, did not last throughout the light phase and VIP precursor mRNA returned to the level before the onset of light after 8 h in light, suggesting that VIP mRNA responds to photic cues and not to light per se. This is in contrast to the sustained suppression of VIP peptide level in the SCN. It indicates that VIP mRNA is acting at a stage of light information processing upstream to VIP peptide in the circadian pacemaker.

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Cited by (37)

Effects of aging and genotype on circadian rhythms, sleep, and clock gene expression in APPxPS1 knock-in mice, a model for Alzheimer's disease
2012, Experimental Neurology
Citation Excerpt :
Because the sampling times were selected to identify the peak and trough of SCN Per2 expression, which differ from those characterizing the SCN vasopressin expression rhythm, the apparent absence of time of day differences in SCN vasopressin expression in the current study is not surprising. Concerning SCN VIP mRNA expression, time of day variations have been observed in some rodent species (e.g., rats) but not others (e.g., Siberian and Syrian hamsters) (Duncan et al., 1995, 2001; Yang et al., 1993). In mice of the Swiss strain (Charles River) exposed to a light:dark cycle, SCN VIP mRNA expression shows a low amplitude rhythm with an apparent peak at ZT 16 (Dardente et al., 2004).
Profound disruptions of circadian rhythms and sleep/wake cycles constitute a major cause of institutionalization of AD patients. This study investigated whether a rodent model of AD, APP^NLH/NLH/PS-1^P264L/264L (APPxPS1) mice, exhibits circadian alterations. The APPxPS1 mice were generated using CD-1/129 mice and Cre-lox knock-in technology to “humanize” the mouse amyloid (A)β sequence and create a presenilin-1 mutation identified in familial early-onset AD patients. APPxPS1 and WT mice of several ages (~ 4, 11, and 15 months) were monitored for circadian rhythms in wheel running, cage activity, and sleep:wake behavior. After rhythm assessment, the mice were euthanized at zeitgeber time (ZT) 2 or 10 (i.e., 2 or 10 h after lights-on) and brains were dissected. Amyloidβ levels were measured in cortical samples and brain sections of the hypothalamus and hippocampus were prepared and used for in situ hybridization of circadian or neuropeptide genes. The most significant effects of the APPxPS1 transgenes were phase delays of ~ 2 h in the onset of daytime wakefulness bouts (P < 0.005) and peak wakefulness (P < 0.02), potentially relevant to phase delays previously reported in AD patients. However, genotype did not affect the major activity peaks or phases of wheel running, wake, or general movement, which were bimodal with dominant dawn and dusk activity. Expression of Period 2 in the suprachiasmatic nucleus was affected by ZT (P < 0.0001) with a marginal interaction effect of age, genotype, and ZT (P < 0.08). A separate analysis of the old animals indicated a robust interaction between ZT and genotype, as well as main effects of these parameters. Aging also altered sleep (e.g., bout length and amount of daytime sleep) and the amount of wheel running and cage activity. In conclusion, the APPxPS1 knock-in mice exhibit some alterations in their sleep:wake rhythm and clock gene expression, but do not show robust, genotype-related changes in activity rhythms. The prominent daytime activity peaks shown by the background strain complicate the use of these APPxPS1 knock-in mice for investigations of circadian activity rhythms in AD. In addition to this unusual activity pattern, lack of hyperactivity differentiates the APPxPS1 knock-in mice from other transgenic AD models.
Lack of the PAC<inf>1</inf> receptor alters the circadian expression of VIP mRNA in the suprachiasmatic nucleus of mice
2007, Brain Research
PACAP in the retinohypothalamic tract mediates photic information to the suprachiasmatic nucleus via the PAC₁ receptor. The diurnal and circadian VIP mRNA expressions in the suprachiasmatic nucleus of PAC₁−/− and wild type mice were quantified. During light/dark cycles identical VIP mRNA rhythms were found while the oscillation pattern differed between the two types of animals during constant darkness. The results show that the circadian VIP mRNA expression is influenced by the absence of PAC₁ signalling.
Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents
2004, Molecular Brain Research
The suprachiasmatic nuclei (SCN) of the hypothalamus are necessary for coordination of major aspects of circadian rhythmicity in mammals. Although the molecular clock mechanism of the SCN has been a field of intense research during the last decade, the role of the neuropeptides in the SCN, including arginine–vasopressin (AVP), vasoactive intestinal polypeptide (VIP) and gastrin-releasing peptide (GRP), in the clock itself or in circadian organization is still largely unknown. Previous studies mainly performed in the rat have examined the profiles of AVP, VIP and GRP mRNA and peptide levels and suggested that the AVP rhythm is controlled by the circadian clock, whereas those of VIP and GRP are directly dependent on lighting conditions. Here, both daily (i.e., under light–dark cycle [LD]) and circadian (i.e., in constant darkness [DD]) profiles of neuropeptide mRNA were investigated in the SCN of the nocturnal mouse Mus musculus and the diurnal rodent Arvicanthis ansorgei to gain insight into a possible role in circadian organization. Our data show that AVP mRNA exhibits a clear circadian rhythm in the SCN peaking by the end of the subjective day in both species. Contrary to what has been observed in rats, oscillations of VIP and GRP mRNA in the SCN are found to be clock-controlled in mice and A. ansorgei, but with different phases for peak expression. While both VIP and GRP mRNA peak during the middle of the subjective night (i.e., with a 6-h lag compared to AVP mRNA) in mice, they peak almost in phase with AVP mRNA in A. ansorgei. Contrary to what has been reported in the rat, mean levels of VIP and GRP peptide mRNA levels tended to be increased by light in the mice. The different circadian organization of SCN neuropeptides mRNA profiles in both light/dark and constant darkness conditions between mice and A. ansorgei could be related with diurnality.
A brain for all seasons: Cellular and molecular mechanisms of photoperiodic plasticity
2002, Progress in Brain Research
Suprachiasmatic nucleus and intergeniculate leaflet in the diurnal rodent Octodon degus: Retinal projections and immunocytochemical characterization
1999, Neuroscience
The neural connections and neurotransmitter content of the suprachiasmatic nucleus and intergeniculate leaflet have been characterized thoroughly in only a few mammalian species, primarily nocturnal rodents. Few data are available about the neural circadian timing system in diurnal mammals, particularly those for which the formal characteristics of circadian rhythms have been investigated. This paper describes the circadian timing system in the diurnal rodent Octodon degus, a species that manifests robust circadian responses to photic and non-photic (social) zeitgebers. Specifically, this report details: (i) the distribution of six neurotransmitters commonly found in the suprachiasmatic nucleus and intergeniculate leaflet; (ii) the retinohypothalamic tract; (iii) the geniculohypothalamic tract; and (iv) retinogeniculate projections in O. degus. Using immunocytochemistry, neuropeptide Y-immunoreactive, serotonin-immunoreactive and [Met]enkephalin-immunoreactive fibers and terminals were detected in and around the suprachiasmatic nucleus; vasopressin-immunoreactive cell bodies were found in the dorsomedial and ventral suprachiasmatic nucleus; vasoactive intestinal polypeptide-immunoreactive cell bodies were located in the ventral suprachiasmatic nucleus; [Met]enkephalin-immunoreactive cells were located sparsely throughout the suprachiasmatic nucleus; and substance P-immunoreactive fibers and terminals were detected in the rostral suprachiasmatic nucleus and surrounding the nucleus throughout its rostrocaudal dimension. Neuropeptide Y-immunoreactive and [Met]enkephalin-immunoreactive cells were identified in the intergeniculate leaflet and ventral lateral geniculate nucleus, as were neuropeptide Y-immunoreactive, [Met]enkephalin-immunoreactive, serotonin-immunoreactive and substance P-immunoreactive fibers and terminals. The retinohypothalamic tract innervated both suprachiasmatic nuclei equally; in contrast, retinal innervation to the lateral geniculate nucleus, including the intergeniculate leaflet, was almost exclusively contralateral. Bilateral electrolytic lesions that destroyed the intergeniculate leaflet depleted the suprachiasmatic nucleus of virtually all neuropeptide Y- and [Met]enkephalin-stained fibers and terminals, whereas unilateral lesions reduced fiber and terminal staining by approximately half. Thus, [Met]enkephalin-immunoreactive and neuropeptide Y-immunoreactive cells project equally and bilaterally from the intergeniculate leaflet to the suprachiasmatic nucleus via the geniculohypothalamic tract in degus.
This is the first report examining the neural circadian system in a diurnal rodent for which formal circadian properties have been described. The data indicate that the neural organization of the circadian timing system in degus resembles that of the most commonly studied nocturnal rodents, golden hamsters and rats. Armed with such data, one can ascertain differences in the functional organization of the circadian system between diurnal and nocturnal mammals.
Phase dependent response of vasoactive intestinal polypeptide to light and darkness in the suprachiasmatic nucleus
1999, Neuroscience Research
Responsiveness of the vasoactive intestinal polypeptide (VIP) content to light and darkness in the rat suprachiasmatic nucleus (SCN) was examined by enzyme immunoassay of micropunched tissues. VIP content in the SCN has been shown to decrease monotonically in animals maintained in illumination. Decreases in VIP content in the SCN in response to both 6-h light and dark pulses depended on the phase of the circadian cycle when the pulses were applied. Light imposed at circadian time (CT) 18 or CT 22 was more effective in suppressing VIP levels than light exposure of the same intensity imposed at CT 0 or CT 6. Darkness interrupting continuous light was more effective at around CT 0 and less effective at around CT 12. These results suggest that VIP responsiveness to light and darkness in the SCN is regulated by the circadian clock in different ways and are correlated with phase-dependent phase shifts in the activity rhythm after light and dark pulses.

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Short communicationVasoactive intestinal polypeptide precursor mRNA exhibits diurnal variation in the rat suprachiasmatic nuclei

Abstract

Mol. Brain Res.

Neurosci. Lett.

Neurosci. Lett.

FEBS Lett.

Brain Res.

Brain Res.

Mol. Cell. Neurosci.

Immunocytochemical localization of vasoactive intestinal polypeptide-containing cells and processes in the suprachiasmatic nucleus of the rat: light and electron microscopic analysis

J. Neurosci.

Localization of vasopressin-, vasoactive intestinal polypeptide-, peptide histidine isoleucine- and somatostatin-mRNA in rat suprachiasmatic nucleus

Cell Tissue Res.

Photic regulation of Fos-like immunoreactivity in the suprachiasmatic nucleus of the mouse

J. Comp. Neurol.

Neuronal associations in the rat suprachiasmatic nucleus demonstrated by immunoelectron microscopy

J. Comp. Neurol.

Short communication
Vasoactive intestinal polypeptide precursor mRNA exhibits diurnal variation in the rat suprachiasmatic nuclei