Functional expression and tissue distribution of a novel receptor for vasoactive intestinal polypeptide

First identified by Said and Mutt some 30 years ago, the vasoactive intestinal peptide (VIP) was originally isolated as a vasodilator peptide. Subsequently, its biochemistry was elucidated, and within the 1st decade, their signature features as a neuropeptide became consolidated. It did not take long for these insights to permeate the field of immunology, out of which surprising new attributes for VIP were found in the last years. VIP is rapidly transforming into something more than a mere hormone. In evolving scientifically from a hormone to a novel agent for modifying immune function and possibly a cytokine-like molecule, VIP research has engaged many physiologists, molecular biologists, biochemists, endocrinologists, and pharmacologists and it is a paradigm to explore mutual interactions between neural and neuroendocrine links in health and disease. The aim of this review is firstly to update our knowledge of the cellular and molecular events relevant to VIP function on the immune system and secondly to gather together recent data that support its role as a type 2 cytokine. Recognition of the central functions VIP plays in cellular processes is focusing our attention on this "very important peptide" as exciting new candidates for therapeutic intervention and drug development.

The Significance of Vasoactive Intestinal Peptide in Immunomodulation

The suprachiasmatic nucleus of the hypothalamus (SCN) is the master circadian pacemaker or clock in the mammalian brain. Canonical theory holds that the output from this single, dominant clock is responsible for driving most daily rhythms in physiology and behaviour. However, important recent findings challenge this uniclock model and reveal clock-like activities in many neural and non-neural tissues. Thus, in addition to the SCN, a number of areas of the mammalian brain including the olfactory bulb, amygdala, lateral habenula and a variety of nuclei in the hypothalamus, express circadian rhythms in core clock gene expression, hormone output and electrical activity. This review examines the evidence for extra-SCN circadian oscillators in the mammalian brain and highlights some of the essential properties and key differences between brain oscillators. The demonstration of neural pacemakers outside the SCN has wide-ranging implications for models of the circadian system at a whole-organism level.

Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain?

The suprachiasmatic nucleus and the circadian time-keeping system revisited

https://pure.knaw.nl/ws/files/488368/19218.pdf

Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release.

Messenger RNAs (mRNA) coding for vasoactive intestinal polypeptide (VIP), peptide histidine isoleucine (PHI), somatostatin and vasopressin were localized in the suprachiasmatic nucleus (SCN) of the rat hypothalamus using in situ hybridization histochemistry. Specific mRNA coding for each of these peptides was distributed in areas coextensive with the immunohistochemical localization of the appropriate peptide. The autoradiographic signal produced with probes to VIP and PHI created dense concentrations of silver grains over neuronal perikarya in the ventrolateral SCN, and the coextensive distribution of both VIP- and PHI-mRNAs suggests that both peptides are synthesized within the same neurons. The distribution of somatostatin-mRNA was distinct from the of VIP and PHI. Labeled neurons are observed at the interface of the two SCN subdivisions and the distribution of these neurons is identical to those shown to contain somatostatin immunoreactivity. Vasopressin-mRNA is also differentially concentrated within neurons in the dorsomedial subdivision of the SCN in an area that is coextensive with vasopressin-immunoreactive perikarya. The discrete pattern of hybridization for each of these mRNAs indicates that each of these peptides are synthesized in SCN neurons and reaffirms the differential distribution of each of these chemically defined cell populations within cytoarchitecturally distinct subdivisions of the nucleus.

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

Messenger RNA (mRNA) coding for vasoactive intestinal polypeptide (VIP) and peptide histidine isoleucine (PHI-27) were localized in cortical and thalamic neurons with synthetic DNA probes complementary to the PHI-27 and VIP exon coding sequence of the rat VIP precursor gene. Hybridization signal with these probes was found widely distributed in the thalamus, neocortex, and pyriform cortex, and the distribution of hybridization signal for each probe was identical. Furthermore, the distribution of each message was correlated closely with peptide distribution demonstrated immunohistochemically. Labeling of individual neurons with in situ hybridization histochemistry was characterized by a dense accumulation of silver grains in the cytoplasm of these cells with little or no label in the nucleus. Labeled neurons in the thalamus were observed in the ventrolateral, ventromedial, ventrobasal, and lateral reticular nuclei. In the neocortex, the distribution of labeled neurons was concentrated in layers II and III with scattered cells also apparent in deeper cortical layers. Hybridization signal was limited to nonpyramidal neurons in both the neo- and pyriform cortex. The coextensive distribution of immunoreactivity and mRNA coding regions for VIP and PHI-27 establishes that these peptides are synthesized from the same precursor mRNA in the same thalamic and cortical cell groups. Although the physiological role of these peptides in thalamocortical function remains unknown, these data provide an anatomical substrate which suggests that VIP and PHI-27 may be cotransmitters in thalamic and cortical neurons.

Localization of VIP and PHI-27 messenger RNA in rat thalamic and cortical neurons.

The distribution of neuronal perikarya containing somatostatin mRNA in the developing rat brain was investigated with in situ hybridization histochemistry. This study describes the expression of somatostatin mRNA during selected perinatal stages and demonstrates regional changes in somatostatin mRNA expression at the single cell level. The mRNA expression closely parallels previously reported developmental localization of the peptide. As early as embryonic day 13 (E13), somatostatin mRNA was observed in discrete spinal cord and brainstem regions. At birth, densely hybridized somata could be seen primarily in ventral and caudal brain areas with small scattered neurons in the hippocampus and dorsal neocortex. After birth, somatostatin mRNA increased in forebrain regions, such as the hippocampus, dorsal neocortex, and caudate. By postnatal day 14 (P14), the distribution in the telencephalic and diencephalic regions approached that of the adult brain. Several brain regions manifested large changes in the density of somatostatin mRNA hybridization during development. For example, the cerebellar vermis and brainstem contained somatostatin mRNA perikarya during early postnatal development but decreased in these regions in the adult. During perinatal development, increases in somatostatin mRNA content were the results of increases in both the number of neurons containing somatostatin mRNA as well as in themore » amount of this mRNA expressed in each cell. As the brain differentiates, the apparent numbers of somatostatin mRNA containing neurons in certain brain regions are reduced. These data provide evidence for transient somatostatinergic neurons during early development in discrete areas of the occipital cortex, pyriform cortex, cerebellum, and brainstem and suggest that this peptide may play a role in the development of these regions.« less

Ontogeny of somatostatin mRNA-containing perikarya in the rat central nervous system.

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

Localization of VIP and PHI-27 messenger RNA in rat thalamic and cortical neurons.

Ontogeny of somatostatin mRNA-containing perikarya in the rat central nervous system.