Localization of vasoactive intestinal peptide and peptide histidine isoleucine immunoreactivity and mRNA within the rat suprachiasmatic nucleus

Stopa, Edward G.; Minamitani, Naoto; Jonassen, Julie A.; King, Joan C.; Wolfe, Hubert J.; Mobtaker, H.; Albers, H. Elliott

doi:10.1016/0169-328x(88)90041-1

Cited by 51 publications

(22 citation statements)

References 19 publications

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“…The pattern of VIP gene expression we observed in males is consistent with the results of previous studies showing that VIP mRNA (36,(41)(42)(43) and peptide concentrations in the SCN (44,45) decrease after lights on. The finding that VIP mRNA levels in the SCN of males are lower than those in females during the light phase of the cycle is also consistent with work showing that hypothalamic peptide concentrations are lower in males than in females during the middle of the day (46).…”

Section: Discussionsupporting

confidence: 81%

“…A total of 52 sections (26 slides) containing the SCN were collected from each animal. Ten sections (5 slides) containing the midportion of the SCN (ϳ288 -384 m caudal from rostral border of the SCN) were chosen for in situ hybridization because the majority of VIP-containing neurons are located in this region (35,36), and AVP is also highly expressed in this part of the SCN (37). Of the 5 slides chosen for each animal, 3 slides (every other slide) were processed for VIP, and the other 2 slides were processed for AVP in situ hybridization.…”

Section: In Situ Hybridizationmentioning

confidence: 99%

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Sex Differences in the Daily Rhythm of Vasoactive Intestinal Polypeptide But Not Arginine Vasopressin Messenger Ribonucleic Acid in the Suprachiasmatic Nuclei¹

et al. 1998

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The timing of the preovulatory surge of LH in female rodents is tightly coupled to the environmental light/dark cycle. This coupling is mediated by the circadian pacemaker located in the suprachiasmatic nuclei (SCN). Studies indicate that vasoactive intestinal polypeptide (VIP) and arginine vasopressin (AVP), which are synthesized in the SCN, transmit circadian information from the SCN to GnRH neurons, thereby regulating the timing of the LH surge. However, to date, the rhythmic expression of these two peptides in the SCN has only been examined in males. The pattern of VIP expression in males is difficult to reconcile with its role in the LH surge. The purpose of the present study was to assess the rhythm of VIP messenger RNA (mRNA) levels in the SCN of female rats under several endocrine conditions. We compared this rhythm to that in males and to AVP mRNA rhythms in all experimental groups. In all groups of females, VIP mRNA levels were rhythmic, with peak expression occurring during the light phase and a nadir occurring during the dark phase. The rhythm was approximately 12 h out of phase compared with that in males. The rhythmic expression of AVP mRNA in the SCN was virtually identical in all groups of animals. Based on these results, we conclude that 1) the rhythm of VIP seen in the SCN of females during the day may serve as a facilitory signal from the SCN to GnRH neurons; 2) the sex-specific pattern of VIP mRNA does not depend on estradiol; and 3) AVP gene expression within the SCN is not sexually differentiated or altered by estradiol. (Endocrinology 139: 4189 -4196, 1998) T HE SYNCHRONIZATION of numerous neurochemical and hormonal events is necessary for ovulation and the induction of behavioral receptivity in many female species. In rodents, these physiological events are tightly coupled to the environmental light/dark (LD) cycle, so that when circulating estrogen levels are high, such as on the day of proestrus, an ovulatory surge of LH occurs at a very specific time in relationship to the LD cycle (1, 2). The timing of behavioral receptivity also is tightly coupled to the LD cycle in female rodents and occurs only at a specific time on the evening of proestrus (3). Synchronization of ovulation and behavior is important for maximizing reproductive success.Numerous studies have demonstrated that a circadian pacemaker controls the timing of the LH surge (4) and receptive behavior (3), and insures that these rhythms are tightly coupled to the environmental LD cycle. First, treatment with pentobarbital on the morning of proestrus blocks the preovulatory surge of LH. However, a LH surge occurs at the predicted time on the following day, indicating that a daily neurochemical signal is responsible for generating LH surges (5). Second, female rodents housed in LD cycles of varying lengths (i.e. 21-24 h) vary the lengths of their reproductive cycle, such that a single estrous cycle is exactly 4 times the length of the LD cycle to which the animals are exposed (6). Furthermore, animals housed in the a...

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Section: Discussionsupporting

confidence: 81%

Section: In Situ Hybridizationmentioning

confidence: 99%

Sex Differences in the Daily Rhythm of Vasoactive Intestinal Polypeptide But Not Arginine Vasopressin Messenger Ribonucleic Acid in the Suprachiasmatic Nuclei¹

et al. 1998

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“…Conversely, under LD conditions, daily rhythms were observed for VIP that decrease under diurnal lighting conditions, for precursor mRNA, from which VIP and PHI are derived (Stopa et al 1988) and for GRP, which increases during light exposure Shinohara et al 1993;Okamura and Ibata 1994;Inouye and Shibata 1994;Albers et al 1990;Yang et al 1993). These events are brought about by the neurons located in the ventral and lateral-ventral parts of the SCN, which colocalize VIP and PHI and, as far as some of them are concerned, also synthesize GRP (Okamura et al 1986;Romijn et al 1996Romijn et al , 1998A et al 1998).…”

Section: Discussionmentioning

confidence: 94%

Neurons that express the AMPA receptor GluR2/3 subunits in suprachiasmatic nuclei of Syrian hamsters colocalize either vasoactive intestinal peptide, peptide histidine isoleucine or gastrin-releasing peptide

Peytevin¹,

Aı̈oun²,

Chambille³

2000

Cell and Tissue Research

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In mammals, many circadian rhythms are driven by a clock located inside the suprachiasmatic nucleus of the hypothalamus. They are synchronized to environmental light-dark cycles by information coming directly from the retina via glutamatergic afferents. In rodents, retinal fibres make direct synaptic contacts with neurons synthesizing vasoactive intestinal peptide and gastrin-releasing peptide. These two neuropeptides, administered alone or combined with the peptide histidine isoleucine, phase-shift the clock in the same way that light does. Using ICC and light and electron microscopy, our study demonstrates that subunits 2 and 3 of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid-type glutamatergic receptors are colocalized in neurons expressing one or other of these three neuropeptides. Double-labelled neurons were located in the ventral and lateral ventral parts and near the symmetrical plane of the intermediate and caudal thirds of the nucleus. In light microscopy, brown and granular blue stainings of chromogens revealing both antigens were easily identifiable and spatially separated in perikarya. In electron microscopy, almost all the cells observed in these zones expressed the receptor subunits. A few labelled dendritic profiles, some of them post-synaptic, were observed; axon terminals were always unlabelled. Colocalization with vasoactive intestinal peptide and gastrin-releasing peptide was confirmed by the immunogold technique in perikarya and some dendrites. The present study suggests that peptidergic neurons expressing the AMPA receptors are involved in photic entrainment of the clock by the retina without excluding some glutamatergic information coming from other hypothalamic nuclei.

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“…Lesion studies (Johnson et al, 19881, SCN islands (Inouye and Kawamura, 1979), transplantation of the nucleus (DeCoursey and Buggy, 1989;Drucker-Colin et al, 1984;Earnest et al, 1989;Lehman et al, 19871, and in vitro SCN slice preparations (Earnest and Sladek, 1986;Gilette and Reppert, 19871, as well as dissociated cell preparations (Murakami et al, 1991;Silver et al, 1990), have all strengthened the view that the nucleus itself is a circadian pacemaker. Immunocytochemical and in situ hybridization histochemical studies have shown that the SCN contains several populations of intrinsic neurons (Albers et al, 1990;Card et al, 1981;Card and Moore, 1984;Gozes et al, 1989;Moore, 1983;Okamura et al, 1986;Stopa et al, 1988;Van den Pol and Tsujimoto, 1985; Van den Pol and Gorcs, 19861, containing vasopressin (VP;Caste1 et al, 1990;Reppert et al, 1987;Van den Pol, 1986;Van den Pol and Tsujimoto, 1985), vasoactive intestinal polypeptide (VIP; Albers et al, 1990;Card et al, 1981;Gozes et al, 1989;Stopa et al, 1988), gastrin releasing peptide (GRP; Okamura et al, 1986;Van den Pol, 1986;Wada et al, 19901, and GABA (Van den Pol, 1986;Van den Pol and Gorcs, 1986). It appears that, within the SCN, a subset of neurons synthesizing VIP also synthesize GRP (Albers et al, 1991;Okamura et al, 1986;Zoeller et al, 1992).…”

Section: Introductionmentioning

confidence: 98%

Characterization of the suprachiasmatic nucleus in organotypic slice explant cultures

Wray

Castel

Gainer

1993

Microscopy Res & Technique

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Suprachiasmatic nuclei (SCN) from hypothalami of postnatal rats were maintained for 18-39 days in vitro as organotypic slice explants. Neuronal subtypes containing vasopressin (VP), vasoactive intestinal polypeptide (VIP), gastrin releasing hormone (GRP), and GABA were immunocytochemically identifiable in these cultures. In situ hybridization histochemistry was compatible with these SCN slice explant cultures, and mRNA encoding for VP was detected bilaterally within these nuclei. After 18 days in vitro, both VP mRNA and VP immunoreactivity increased from levels present on postnatal days 4 (the earliest age from which the explanted tissue was derived) to levels typical of adult SCNs. In contrast, the GRP expression remained low, characteristic of early postnatal animals and far lower than adult levels. This suggests that the developmental cues or programs necessary for enhanced VP expression are maintained in these cultures, while those affecting GRP expression are absent or inhibited. VIP-containing neurons were numerous in the cultures. Culture slices appeared healthy, and similar numbers and distributions of identifiable neurons within the SCN were observed, whether or not the slices were grown in the presence of serum. EM analysis revealed that the SCN in vitro is composed of tightly packed neurons, processes, and abundant synapses containing both clear and dense core vesicles, closely resembling the SCN in vivo. Vasopressinergic neuronal somata contained extensive Golgi systems and labeled secretory granules, the latter organelle being present also within processes and synaptic terminals. GABA-immunopositive processes and synaptic profiles were abundant, with labeling occurring particularly over secretory vesicles and mitochondria. This slice culture system effectively maintained much of the intrinsic organization and cellular components of the SCN for long periods in vitro and should be an excellent model system for studying the intrinsic molecular mechanisms and extrinsic cues which regulate neuronal phenotype in this circadian pacemaker.

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Localization of vasoactive intestinal peptide and peptide histidine isoleucine immunoreactivity and mRNA within the rat suprachiasmatic nucleus

Cited by 51 publications

References 19 publications

Sex Differences in the Daily Rhythm of Vasoactive Intestinal Polypeptide But Not Arginine Vasopressin Messenger Ribonucleic Acid in the Suprachiasmatic Nuclei¹

Sex Differences in the Daily Rhythm of Vasoactive Intestinal Polypeptide But Not Arginine Vasopressin Messenger Ribonucleic Acid in the Suprachiasmatic Nuclei¹

Neurons that express the AMPA receptor GluR2/3 subunits in suprachiasmatic nuclei of Syrian hamsters colocalize either vasoactive intestinal peptide, peptide histidine isoleucine or gastrin-releasing peptide

Characterization of the suprachiasmatic nucleus in organotypic slice explant cultures

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Localization of vasoactive intestinal peptide and peptide histidine isoleucine immunoreactivity and mRNA within the rat suprachiasmatic nucleus

Cited by 51 publications

References 19 publications

Sex Differences in the Daily Rhythm of Vasoactive Intestinal Polypeptide But Not Arginine Vasopressin Messenger Ribonucleic Acid in the Suprachiasmatic Nuclei1

Sex Differences in the Daily Rhythm of Vasoactive Intestinal Polypeptide But Not Arginine Vasopressin Messenger Ribonucleic Acid in the Suprachiasmatic Nuclei1

Neurons that express the AMPA receptor GluR2/3 subunits in suprachiasmatic nuclei of Syrian hamsters colocalize either vasoactive intestinal peptide, peptide histidine isoleucine or gastrin-releasing peptide

Characterization of the suprachiasmatic nucleus in organotypic slice explant cultures

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Sex Differences in the Daily Rhythm of Vasoactive Intestinal Polypeptide But Not Arginine Vasopressin Messenger Ribonucleic Acid in the Suprachiasmatic Nuclei¹

Sex Differences in the Daily Rhythm of Vasoactive Intestinal Polypeptide But Not Arginine Vasopressin Messenger Ribonucleic Acid in the Suprachiasmatic Nuclei¹