Neuropeptide Y-like immunoreactivity in rat cranial parasympathetic neurons: coexistence with vasoactive intestinal peptide and choline acetyltransferase.

Abstract

Neuropeptide Y (NPY) is widely distributed in the sympathetic nervous system, where it is colocalized with norepinephrine. We report here that NPY-immunoreactive neurons are also abundant in three cranial parasympathetic ganglia, the otic, sphenopalatine, and ciliary, in the rat. Neuropeptide Y (NPY) is structurally related to members of the pancreatic polypeptide family but appears to be localized exclusively in central and peripheral neurons (1, 2). In the periphery, NPY is present in sympathetic neurons that innervate the vasculature (3, 4), heart (5, 6), urogenital tract (3, 7), and iris (8). A number of biological actions have been reported for NPY, including a potent vasoconstrictor action on peripheral and cerebral vessels (3, 4, 9) and inhibition of synaptic transmission in the vas deferens, uterus, urinary bladder, and heart (3, 10, 11). NPY may therefore act as a neuromodulator in the sympathetic nervous system. NPY-immunoreactive sympathetic neurons contain the catecholamine-synthetic enzymes tyrosine hydroxylase [TyrOHase; L-tyrosine,tetrahydropteridine:oxygen oxidoreductase (3-hydroxylating), EC 1.14.16.2] and dopamine ,3-hydroxylase [3,4-dihydroxyphenethylamine,ascorbate:oxygen oxidoreductase (l3-hydroxylating), EC 1.14.17.1], indicating that NPY is colocalized with norepinephrine in these neurons (3,(12)(13)(14). In contrast, there is little overlap between populations of sympathetic neurons that contain NPY and those that contain vasoactive intestinal polypeptide (VIP) (12, 14). The minority population of sympathetic neurons that contain VIP has been found to lack catecholamine-synthetic enzymes; as is the case for VIP-containing parasympathetic neurons, there is evidence that at least some of the neurons in this population are cholinergic (12,15,16). The notion has emerged from these studies that coexpression of NPY with norepinephrine, and of VIP with acetylcholine, is an organizational principle in the autonomic nervous system (14).To explore further the relationship between NPY expression and the expression ofother neurotransmitter phenotypes in autonomic neurons, we have examined cranial parasympathetic neurons for the presence of NPY. The present work shows that NPY-immunoreactive neurons are abundant in rat cranial parasympathetic ganglia and examines the colocalization of NPY immunoreactivity with TyrOHase, VIP, and the cholinergic enzyme choline acetyltransferase (ChoAcTase; acetyl-CoA:choline O-acetyltransferase, EC 2.3.1.6) in these neurons.MATERIALS AND METHODS Cytochemistry. The NPY antiserum (Amersham) was raised in rabbit against synthetic porcine NPY. The VIP antiserum, a gift from P. Hogan (Harvard Medical School), was raised in rabbit against a carbodiimide conjugate of synthetic VIP (Boehringer Mannheim) to bovine serum albumin. The TyrOHase antiserum, a gift from J. Thibault, was raised in rabbit against TyrOHase purified from rat pheochromocytoma tumors (17). The ChoAcTase antiserum, a gift from F. Eckenstein, was raised in mouse against ChoAcTase purified from pig ...

Ultrastructural simultaneous localization of vasoactive intestinal polypeptide immunoreactivity and the acetylcholine-like cation in rat endocrine pancreas.

“…Therefore, the present data suggest a neural control of hormonal secretion by ACh and VIP, which are released from nerve endings in contact with endocrine cells. ACh and VIP may act in synergy, as has already been observed in different tissues (LUND-BERG et al, 1980;LEBLANC et al, 1987). However, the precise mechanism of the synergic action is not known.…”

“…Different types of nerve endings, among them cholinergic (WATARI, 1968;SHORR and BLOOM, 1970;FUJITA and KOBAYASHI, 1979) and peptidergic ones (FUJITA and KOBAYASHI, 1979) were characterized by the morphology of the synaptic vesicles they contained. The cholinergic mechanisms are presumed to be modulated by neuropeptides, including VIP (LUNDBERG et al, 1980;LEBLANC et al, 1987).…”

Localization of immunoreactivities for neuropeptides and neurotransmitter-synthesizing enzymes in the pterygopalatine ganglion of the pig

“…The lack of TH-immunoreactivity in these neurons suggests that NPY is involved in non-adrenergic regulation of the peripheral tissues function. In the rat, PPG neurons expressing NPY were found to contain also VIP and/or ChAT immunoreactivity, and did not contain catecholamines and TH (Leblanc et al, 1987).…”

An Immunohistochemical Study of Sensory and Autonomic Innervation of the Dog Tongue with Special Reference to Substance P- and Calcitonin Gene-Related Peptide-Containing Fibers in Blood Vessels and the Intralingual Ganglia.

“…ILG VIP-containing neurons are commonly found in diverse parasympathetic ganglia as well as in local ganglia (SCHULTZBURG and LINDH, 1988;UEMURA et al, 1988) and have been suggested to mediate the vasodilatation and secretion of exocrine glands (SHIMIZU and TAIRA, 1979;LUNDBERG et al, 1980LUNDBERG et al, , 1982LUNDBERG et al, ,1984cEKSTROM et al, 1984;TOBIN et al, 1990). Coexistence of VIP and one or more different neuropeptides such as NPY, SP or CGRP in the parasympathetic ganglionic neurons is known (LEBLANC et al, 1987;DEY et al, 1988;ICHIKAWA et al, 1988;HARDEBO et al, 1992). In the intralaryngeal local ganglia of the dog, we have previously demonstrated a subpopulation of ganglionic cells containing VIP alone, VIP with NPY, VIP with SP, VIP with NPY and SP, and VIP with enkephalin (MASUKO et al, 1991).…”