The intra-adrenal distribution of intrinsic and extrinsic nitrergic nerve fibres in the rat
Abstract
The intra-adrenal distribution of nitric oxide synthase (NOS)-immunoreactive nerve fibres was studied in rats subjected to various denervations. Splanchnic nerve section eliminated the NOS-immunoreactive nerve fibres which innervate adrenal chromaffin and neuronal cells. It did not affect those innervating blood vessels and zona glomerulosa, which instead were affected by adrenal demedullation. Guanethidine, 6-hydroxydopamine (6-OHDA) and capsaicin treatments, however, did not produce any change. These results suggest that nitrergic nerves which innervate adrenal medullary cells are extrinsic (largely preganglionic sympathetic), whilst those innervating the zona glomerulosa and the majority of adrenal vessels are intrinsic, and that they do not belong to nerves sensitive to the sympathetic nerve neurotoxins, guanethidine and 6-OHDA, or the sensory neurotoxin, capsaicin.
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Cited by (15)
Serotonin and the serotonin transporter in the adrenal gland
2024, Vitamins and HormonesThe adrenal glands are key components of the mammalian endocrine system, helping maintain physiological homeostasis and the coordinated response to stress. Each adrenal gland has two morphologically and functionally distinct regions, the outer cortex and inner medulla. The cortex is organized into three concentric zones which secrete steroid hormones, including aldosterone and cortisol. Neural crest-derived chromaffin cells in the medulla are innervated by preganglionic sympathetic neurons and secrete catecholamines (epinephrine, norepinephrine) and neuropeptides into the bloodstream, thereby functioning as the neuroendocrine arm of the sympathetic nervous system. In this article we review serotonin (5-HT) and the serotonin transporter (SERT; SLC6A4) in the adrenal gland. In the adrenal cortex, 5-HT, primarily sourced from resident mast cells, acts as a paracrine signal to stimulate aldosterone and cortisol secretion through 5-HT4/5-HT7 receptors. Medullary chromaffin cells contain a small amount of 5-HT due to SERT-mediated uptake and express 5-HT1A receptors which inhibit secretion. The atypical mechanism of the 5-HT1A receptors and interaction with SERT fine tune this autocrine pathway to control stress-evoked catecholamine secretion. Receptor-independent signaling by SERT/intracellular 5-HT modulates the amount and kinetics of transmitter release from single vesicle fusion events. SERT might also influence stress-evoked upregulation of tyrosine hydroxylase transcription. Transient signaling via 5-HT3 receptors during embryonic development can limit the number of chromaffin cells found in the mature adrenal gland. Together, this emerging evidence suggests that the adrenal medulla is a peripheral hub for serotonergic control of the sympathoadrenal stress response.
Influence of innocuous cervical vertebral movement on the efferent innervation of the adrenal gland in the rat
2006, Autonomic Neuroscience: Basic and ClinicalIn general, in central nervous system intact anesthetized animals, adrenal sympathetic efferent nerve activity and catecholamine secretion increase in response to noxious somatic stimulation, and decrease in response to innocuous somatic stimulation. In anesthetized rats, noxious chemical stimulation of the thoracic and lumbar interspinous tissues is associated with large increases in adrenal sympathetic efferent nerve activity and catecholamine secretion, with a clear segmental organization to the reflex apparent in spinalized animals. However, the adrenal sympathetic nerve responses to mechanical stimulation in the form of pressure applied laterally to the lower thoracic and lower lumbar vertebrae do not display segmental organization, and the depressor response is more characteristic of responses to innocuous somatic stimulation despite the use of large forces (up to 3.0 kg). Therefore, we sought to determine whether innocuous movements of the mechanoreceptor-rich deep tissues of the neck modulate the sympathetic outflow to the adrenal gland. We performed experiments in 14 anaesthetised (Urethane 1 g/kg and Chloralose 0.1 g/kg) adult rats. Rats were intubated and breathed spontaneously. A computer driven small animal manipulator was used to impose ramp and hold rotational displacements (12°/s, hold duration 2 s) of the 2nd cervical vertebra (range 2–30°) while recording multi-unit activity from sympathetic nerves innervating the adrenal gland. While noxious forepaw pinch elicited an increase in sympathetic nerve activity to the adrenal gland, there was no significant change in sympathetic nerve activity with small (2° or 6°) rotations. Significant changes (P < 0.05) in sympathetic activity were observed in only 7% (n = 21) of all trials at larger displacements (12°, 20°, 25°, 30° n = 287 trials). Our data suggest that although noxious stimuli may modulate sympathetic outflow, it is rare for afferents signalling innocuous cervical vertebral movements to modulate sympathetic nerves innervating the adrenal gland.
Re-establishment of neurochemical coding of preganglionic neurons innervating transplanted targets
2003, NeuroscienceWe investigated the effect on neurochemical phenotype of changing the targets innervated by sympathetic preganglionic neurons. In neonatal rats, the adrenal gland was transplanted into the neck, to replace the postganglionic neurons of the superior cervical ganglion. Transplanted adrenal glands survived, and contained noradrenergic and adrenergic chromaffin cells, and adrenal ganglion cells. Retrograde tracing from the transplants showed that they were innervated by preganglionic neurons that would normally have supplied postganglionic neurons of the superior cervical ganglion. The neurochemical phenotypes of preganglionic axons innervating transplanted chromaffin cells were compared with those innervating the normal adrenal medulla or superior cervical ganglion neurons. As in the normal adrenal gland, preganglionic nerve fibres apposing transplanted chromaffin cells were cholinergic. The peptide and calcium-binding protein content of preganglionic fibres was similar in normal and transplanted adrenal glands. In both cases, cholinergic fibres immunoreactive for enkephalin targeted adrenergic chromaffin cells, whilst cholinergic fibres with co-localised calretinin-immunoreactivity innervated noradrenergic chromaffin cells and adrenal ganglion cells. In contrast to the innervation of normal adrenal glands, these axons lacked immunoreactivity to nitric oxide synthase. In a set of control experiments, the superior cervical ganglion was subjected to preganglionic denervation in rat pups the same age as those that received adrenal transplants, and the ganglion was allowed to be re-innervated over the same time course as the adrenal transplants were studied. When the superior cervical ganglion was re-innervated by preganglionic nerve fibres, we observed that all aspects of chemical coding were restored, including cholinergic markers, nitric oxide synthase, enkephalin, calcitonin gene-related peptide and calcium binding proteins in predicted combinations, although the density of nerve fibres was always lower in re-innervated ganglia. These data show that the neurochemical phenotypes expressed by preganglionic neurons re-innervating adrenal chromaffin cells are selective and similar to those seen in the normal adrenal gland. Two explanations are advanced: either that contact of preganglionic axons with novel target cells has induced a switch in their neurochemical phenotypes, or that there has been target-selective reinnervation by pre-existing fibres of appropriate phenotype. Regardless of which of these alternatives is correct, the restoration of normal preganglionic codes to the superior cervical ganglion following denervation supports the idea that the target tissue influences the neurochemistry of innervating preganglionic neurons.
Immunohistochemical localization of nNOS in the head kidney of larval and juvenile rainbow trout, Oncorhynchus mykiss
2001, General and Comparative EndocrinologyThe aim of this investigation was to assess whether in teleosts, as in mammals, nitric oxide (NO) is involved in the regulation of cellular activity in the adrenal homolog. Larval and juvenile stages of the rainbow trout, Oncorhynchus mykiss, were used, in which the adrenal homolog consists of chromaffin adrenergic and interrenal steroidogenic cells localized mainly in the head kidney where there are also ganglion cells and nerve fibres that innervate the gland. In 12-month-old juveniles, the immunohistochemical reaction for neuronal nitric oxide synthase (nNOS), which catalyzes the synthesis of NO, revealed the presence of this enzyme in some nerve fibres and ganglion cells and only rarely in chromaffin cells. The latter are identified by the immunohistochemical reaction for tyrosine hydroxylase (TH) and phenylethanolamine-N-methyltransferase (PNMT). In larvae at 27 days postfertilization, numerous cells dispersed in the head kidney are nNOS positive, whereas the TH and PNMT positive cells are very rare. At hatching (31 days postfertilization), the positivity for nNOS in the cells of the head kidney disappears and reappears at 60 days posthatching in some nerve cells and fibres. These results suggest an involvement of NO in the regulation of adrenal function as in mammals and the nature of nNOS positive cells present in the head kidney of larvae of 27 days is discussed.
Nitric oxide modulates a late step of exocytosis
2000, Journal of Biological ChemistryThe effects of nitric oxide (NO) on the late phase of exocytosis have been studied, by amperometry, on Ba2+-stimulated chromaffin cells. Acute incubation with NO or NO donors (sodium nitroprusside, spermine-NO,S-nitrosoglutathione) produced a drastic slowdown of the granule emptying. Conversely, cell treatment with Nω-nitro-l-arginine methyl ester (a NO synthase inhibitor) or with NO scavengers (methylene blue, 2-(4-carboxyphenyl)-4,4,5,5-tetramethyl-imidazoline-1-oxyl-3-oxide potassium) accelerated the extrusion of catecholamines from chromaffin granules, suggesting the presence of a NO modulatory tone. The incubation with phosphodiesterase inhibitors (3-isobutyl-1-methylxanthine or zaprinast) or with the cell-permeant cGMP analog 8-bromo-cGMP, mimicked the effects of NO, suggesting the involvement of the guanylate cyclase cascade. NO effects were not related to changes in intracellular Ba2+. NO did not modify the duration of feet. Effects were evident even on pre-fusioned granules, observed under hypertonic conditions, suggesting that the fusion pore is not the target for NO, which probably acts by modifying the affinity of catecholamines for the intragranular matrix. NO could modify the synaptic transmitter efficacy through a novel mechanism, which involves the regulation of the emptying of secretory vesicles.
Nitric oxide and fibroblast growth factor in autonomic nervous system: Short- and long-term messengers in autonomic pathway and target-organ control
1997, Progress in NeurobiologyThe freely diffusible messenger nitric oxide (NO), generated by NO synthase (NOS)-containing “nitroxergic” (NO-ergic) neurons, is unique among classical synaptic chemical transmitters because of its “non-specificity”, molecular “NO-receptors” (e.g. guanylyl cyclase, iron complexes, nitrosylated proteins or DNA) in target cells, intracellular targeting, regulated biosynthesis, and growth factor/cytokine-dependence. In the nervous system, expression of NOS is particularly intriguing in central and peripheral autonomic pathways and their targets. Here, anatomical and functional links appear to exist between NOS, its associated catalytic NADPH-diaphorase enzyme activity (NOSaD) and fibroblast growth factor-2 (FGF-2), a pleiotropic cytokine with mitogenic actions, suggesting mutual “short- and long-term” actions. Several recent studies performed in the rat sympathoadrenal system, an anatomically and neurochemically well-defined autonomic pathway with target-specific functional units of sympathetic preganglionic neurons (SPNs) in the spinal cord, provide evidence for this hypothesis. The NO and cytokine signals may interact at the level of gene expression, transcription factors, post-transcriptional control or second messenger cross-talk. Thus, unique biological roles of FGF-2 and the NO system are likely to exist in neuroendocrine actions, vasomotory perfusion control as well as in neurotrophic actions in sympathetic innervation of the adrenal gland. In view of their anatomical co-existence, functional interplay and synchronizing effects on neuronal networks, multiple roles are suggested for both “short- and long-term” signalling molecules in neuroendocrine functions and integrated autonomic target organ control. © 1997 Elsevier Science Ltd. All Rights Reserved.