Organizational principles in the peripheral sympathetic nervous system: Subdivision by coexisting peptides (somatostatin-, avian pancreatic polypeptide-, and vasoactive intestinal polypeptide-like immunoreactive materials

Abstract

Sympathetic ganglia and some peripheral tissues of adult guinea pig and cat were analyzed by the indirect immunofluorescence technique with antisera to catecholamine-synthesizing enzymes and some peptides. In the guinea pig, noradrenergic neurons could be subdivided into three populations containing respectively (i) somatostatin-like immunoreactive material, (ii) avian pancreatic polypeptide (APP)-like immunoreactive material, and (iii) apparently only noradrenaline (NA; norepinephrine). A fourth population of sympathetic neurons was nonadrenergic and contained vasoactive intestinal polypeptide (VIP)-immunoreactive material. In the cat many noradrenergic neurons with APP and some without this peptide were seen, but no somatostatin-immunoreactive neurons were observed. Also a population of non-adrenergic, presumably cholinergic, neurons containing a VIP-like peptide was observed. These neuron, populations seemed to innervate different tissues with some target specificity.For example, in the nasal mucosa ofthe cat, nerves containing NA/ APP-like immunoreactive material (called NA/APP nerves) were found around small arteries and arterioles, whereas venules and sinusoids were surrounded by nerves containing only NA (called NA nerves). Also in the submandibular salivary gland of the cat, the NA/APP nerves surrounded arteries and drterioles, whereas NA nerves were seen in relation to acini and ducts. The sympathetic (cholinergic) VIP-containing neurons innervated blood vessels and exocrine tissue in the cat sweat glands. In the coeliac-superior mesenteric ganglion complex of the guinea pig and cat, a dense network of VIP-immunoreactive fibers was seen preferentially around noradrenergic ganglionic cell bodies lacking APP-immunoreactive material. Thus, adult peripheral sympathetic neurons can be subdivided into several categories on the basis of specific peptides. These subdivisions may innervate specific targets and may receive peptide-specific neuronal inputs.Classically the peripheral autonomic nervous system can be subdivided into the sympathetic and the parasympathetic portions (1, 2). The enteric nerves have been considered to represent a separate division (3). The principal transmitter in the sympathetic division is noradrenaline (NA), as discovered by von Euler (4). However, a small population of sympathetic nerves supply sweat glands (5, 6) and skeletal muscle vessels and are cholinergic (7).During recent years, an extensive distribution ofpeptides in peripheral neurons has been identified (8-10). Further analysis has revealed-that some of these peptides coexist with classical transmitters in sympathetic neurons. Thus, some peripheral noradrenergic cell bodies in sympathetic ganglia of the guinea pig, particularly prevertebral ganglia, contain a somatostatinlike peptide (11). An avian pancreatic polypeptide (APP)-like peptide has been demonstrated in a population of peripheral noradrenaline neurons (12). Finally, the acetylcholine (AcCho) esterase-rich, presumably cholinergic, neurons in sympathetic g...

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

“…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.…”

“…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).…”

Stimulation of somatostatin expression in developing ciliary ganglion neurons by cells of the choroid layer

“…Within the PNS, the pattern of neuropeptide expression appears to be tightly correlated with target innervation (Lundberg et al, 1982;Leblanc and Landis, 1988;Macrae et al, 1986). This correlation has led to the speculation that the target cells specify the type of neuropeptide expressed by the innervating neuron.…”

Localization of peptide YY (PYY) in gastrointestinal endocrine cells and effects on intestinal blood flow and motility.

“…The present study was approved by the ethical committee at the Karolinska Hospital (81:204). After rinsing in ice-cold saline for 15 min, tissues were fixed by immersion in a mixture of 0.25% parabenzoquinone (Sigma) and 5% formalin at 4°C in phosphate buffer (9). After rinsing in sucrose and cryostat sectioning, the tissues were processed as described (9).…”

“…After rinsing in ice-cold saline for 15 min, tissues were fixed by immersion in a mixture of 0.25% parabenzoquinone (Sigma) and 5% formalin at 4°C in phosphate buffer (9). After rinsing in sucrose and cryostat sectioning, the tissues were processed as described (9). Briefly, the sections were incubated in a humid atmosphere at 4°C for [14][15][16][17][18][19][20] In vivo experiments were performed in six cats anesthetized with chloralose (50 mg/kg) and urethane (100 mg/kg).…”