Increase in galanin and neuropeptide Y mRNA in locus coeruleus following acute reserpine treatment

doi:10.1016/0014-2999(90)90677-X

European Journal of Pharmacology

Volume 184, Issue 1, 2 August 1990, Pages 163-167

https://doi.org/10.1016/0014-2999(90)90677-X Get rights and content

Abstract

Galanin and neuropeptide Y are known to coexist with noradrenaline in neurons of the locus coeruleus. Furthermore, reserpine depletes noradrenaline from, and increases the synthesis and activity of the catecholamine- synthesizing enzyme tyrosine hydroxylase in, this nucleus. We have found by in situ hybridization of specific ³⁵S-labelled oligonucleotide probes that a single dose of reserpine (10 mg/kg) induced a significant (70–145%) and long-lasting (up to at least 3 days) increase in the amount of galanin and neuropeptide Y mRNA in the locus coeruleus (along with the characteristic increase in tyrosine hydroxylase mRNA). These results suggest a similar reserpine-sensitive mechanism of galanin, neuropeptide Y and tyrosine hydroxylase gene regulation.

References (10)

H. Higuchi et al.
Rat neuropeptide Y precursor gene expression: mRNA structure, tissue distribution and regulation by glucocorticoids, cyclic AMP, and phorbol ester
J. Biol. Chem.
(1988)
V.R. Holets et al.
Locus coeruleus neurons in the rat containing neuropeptide Y, tyrosine hydroxylase or galanin and their efferent projections to the spinal cord, cerebral cortex and hypothalamus
Neuroscience
(1988)
F. Schon et al.
The effect of 6-hydroxydopamine, reserpine and cold stress on the neuropeptide Y content of the rat central nervous system
Neuroscience
(1986)
N. Faucon Biguet et al.
Time course of the changes of TH mRNA in rat brain and adrenal medulla after a single injection of reserpine
EMBO J.
(1986)
Gundlach, A.L., W. Wisden, B.J. Morris and S.P. Hunt, Localization of preprogalanin mRNA in rat brain: in situ...

There are more references available in the full text version of this article.

Cited by (28)

Expression of galanin and galanin receptor-1 in normal bone and during fracture repair in the rat
2003, Bone
The neuropeptide galanin (GAL) has recognized physiological actions in the nervous system and other tissues, but there is no documented evidence of GAL influencing normal or pathological bone metabolism. GAL expression, however, is upregulated in central and peripheral nerves following axotomy and is known to influence neural regeneration. Thus, severance of skeletal-associated nerves during fracture could similarly increase local GAL concentrations and thereby influence fracture healing. The initial aim of this study was therefore to identify the presence of GAL in normal bone and/or fracture callus by assessing the concentration and cellular localization of GAL in intact and/or fractured rat rib, using radioimmunoassay and immunohistochemistry, respectively. Groups of Sprague–Dawley rats (13 weeks old) had their left sixth ribs surgically fractured or underwent sham surgery and then calluses and nonfractured rib samples were analyzed at 1 and 2 weeks postsurgery (n = 5–6 per group). Low (basal) concentrations of GAL were detected in control ribs, whereas at 1 and 2 weeks postfracture, callus samples contained markedly increased levels of peptide (∼32- and 18-fold increase, respectively, relative to controls; P < 0.01), revealing a strong upregulation during bone healing. Plasma GAL concentrations were also increased at 2 weeks postfracture (P < 0.005). In normal (nonfractured) rib, minimal levels of GAL-like immunoreactivity (LI) were present in cortical bone, periosteum, endosteum, and surrounding skeletal muscle. In costal cartilage plates, intense GAL-LI was present in all chondrocytes of the hypertrophic zone and in a population of chondrocytes in the reserve zone. GAL-LI was not present, however, in chondrocytes in the proliferative zone of costal cartilage or skeletal muscle fibers. In fracture callus, levels of GAL-LI were moderate to intense in osteoprogenitor cells and osteoblasts, in some chondrocytes, and in cartilaginous, osseous, and periosteal matrices. Subsequent studies revealed the presence of galanin receptor-1-like immunoreactivity (GALR1-LI) in most cell types shown to contain GAL-LI, although the distribution of GALR1-LI was more extensive in reserve zone chondrocytes than that of GAL-LI; and GALR1-LI also appeared in late proliferative zone chondrocytes of costal cartilage. In summary, GAL concentrations were significantly increased in fracture callus and plasma of rats that underwent rib fracture. In addition, GAL- and GALR1-LI was also detected in specific cells and structures within costal cartilage, bone, and fracture callus. These results strongly implicate GAL in aspects of cartilage growth plate physiology and fracture repair, possibly acting in an autocrine/paracrine fashion via GALR1.
Catecholamine secretory vesicle stimulus-transcription coupling in vivo. Demonstration by a novel transgenic promoter/photoprotein reporter and inhibition of secretion and transcription by the chromogranin A fragment catestatin
2003, Journal of Biological Chemistry
Citation Excerpt :
Thus, catestatin in vivo seems to exert nicotinic cholinergic antagonist activity on both secretory and transcriptional processes in the sympathoadrenal system. Depletion of neurotransmitter storage by reserpine also increases gene expression of enzymes involved in neurotransmitter synthesis, such as tyrosine hydroxylase (37), as well as neurotransmitter transporters, such as the serotonin transporter (38), and neuropeptides including preproenkephalin (39), preprotachykinin (39), galanin, vasopressin (40), neuropeptide Y (41), chromogranin B, and secretogranin II (40). In the present study, transmitter depletion caused time- and dose-dependent increments of transgene expression in the brain, with ∼3.3-fold stimulation at 5 mg of reserpine/kg (Fig. 8C).
Stimulation of chromaffin cell secretion in vitro triggers not only secretion but also resynthesis of just released catecholamines and chromogranin A, the precursor of the catecholamine release-inhibitory, nicotinic cholinergic antagonist peptide catestatin. Does stimulus-transcription coupling occur in vivo? And does catestatin antagonize secretion and transcription in vivo? To answer these questions, we employed a novel mouse strain harboring a chromogranin A promoter/firefly luciferase reporter transgene. Tissue-specific expression of the reporter was established by both luminescence and reverse transcription-PCR. Secretion and transcription in vivo were triggered by either direct nicotinic stimulation or vesicular transmitter depletion. Nicotinic blockade in vivo was attempted with either the classical antagonist chlorisondamine or the novel antagonist catestatin. Luciferase reporter expression was exquisitely sensitive over a large dynamic range, was specific for the transgenic animals, and paralleled typical neuroendocrine distribution of endogenous chromogranin A. Adrenal ontogeny revealed a rise of embryonic transgene expression until embryonal day 18, with an abrupt postnatal decline. Direct nicotinic stimulation of chromaffin cells caused catecholamine release and transgene transcription, each of which was nearly completely blocked by chlorisondamine. Similar adrenal results were obtained during vesicular catecholamine depletion. Both secretion and transcription were substantially blocked in the adrenal gland by catestatin. In brain and sympathetic nerve, stimulation of transcription was more modest, and reserpine responses were only incompletely blocked by chlorisondamine or catestatin, perhaps because of limited blood-brain barrier penetration by these cationic antagonists. Thus, nicotinic cholinergic stimulus-transcription coupling occurs in vivo and can be provoked either directly or indirectly (by vesicular transmitter depletion). Such coupling triggers the biosynthesis of chromogranin A, the precursor of catestatin. Catestatin itself blocks stimulation of both secretion and transcription in vivo. Thus, chromogranin A and its catestatin fragment may lie at the nexus of nicotinic cholinergic signaling in vivo.
Effect of 6-hydroxydopamine on neuropeptide Y and corticotropin-releasing factor expression in rat amygdala
1999, Neuroscience
The influence of dopaminergic denervation on neuropeptide Y and corticotropin-releasing factor-containing neurons in the amygdala was investigated in rats by examining the effects of a selective, unilateral 6-hydroxydopamine lesion of mesencephalic dopaminergic neurons in both the substantia nigra and the ventral tegmental area on these peptides and their messenger RNA expression, observed eight to 10 days after the lesion. The studies were conducted by immunocytochemical and in situ hybridization methods. Neuropeptide Y or corticotropin-releasing factor-immunoreactive neurons were counted in sections of the amygdala under a microscope, and the messenger RNA expression was measured as optical density units in autoradiograms. A significant increase in both neuropeptide Y and corticotropin-releasing factor messenger RNA expression was found in the amygdala on the lesioned side in comparison with the contralateral one, as well as with the ipsilateral side of vehicle-injected controls. Immunohistochemical studies showed that the number of neuropeptide Y-immunoreactive neurons increased in the whole amygdala on the lesioned side. At the same time, the number of corticotropin-releasing factor-immunoreactive neurons grouped in the central amygdaloid nucleus declined, and so did the staining intensity.
The obtained results indicate that dopaminergic denervation stimulates the synthesis of neuropeptide Y and corticotropin-releasing factor in rat amygdala, but the peptide levels are differently regulated, which points to a diverse release of these peptides.
Acute methamphetamine administration increases tyrosine hydroxylase mRNA levels in the rat locus coeruleus
1997, Molecular Brain Research
Tyrosine hydroxylase (TH) mRNA levels in the rat substantia nigra (SN), ventral tegmental area (VTA) and locus coeruleus (LC) were measured by in situ hybridization histochemistry 1, 4, 6 and 24 h after a single injection of methamphetamine (MAP, 4 mg/kg, i.p.) or an equivalent volume of saline. TH mRNA levels in LC were transiently increased (130% of control saline group, P<0.05) at 1 h after MAP injection, and returned to basal levels within 4 h. In contrast, acute MAP administration did not significantly affect TH mRNA levels in SN and VTA. These findings are the first to demonstrate TH mRNA expression in the different responses of catecholaminergic neurons to acute MAP administration.
Localization of preprogalanin messenger RNA in rat brain: Identification of transcripts in a subpopulation of cerebellar Purkinje cells
1996, Neuroscience
Galanin, a 29 amino acid peptide, is widely distributed throughout both the peripheral and central nervous systems and is thought to be involved in multiple physiological functions including smooth muscle relaxation, stimulation of feeding, blood pressure regulation, control of hormone secretion and modulation of nociception. Galanin has been shown to co-exist with several neurotransmitters throughout the neuroaxis and in some cases to modify their presynaptic and postsynaptic actions. In the present study, the anatomical distribution of preprogalanin messenger RNA in rat brain was examined by in situ hybridization histochemistry using specific ³⁵S-labelled oligonucleotide probes. Neurons expressing preprogalanin messenger RNA were found throughout the brain and were particularly abundant in the hypothalamus. High densities of preprogalanin messenger RNA-positive neurons were found in the anteroventral preoptic, supraoptic, paraventricular and dorsomedial nuclei of the hypothalamus, in the locus coeruleus and in the nucleus of the solitary tract. Moderate densities of preprogalanin messenger RNA-positive cells were apparent in the periventricular and arcuate nuclei of the hypothalamus, in the dorsal raphe and dorsal cochlear nuclei. Low densities of preprogalanin messenger RNA-expressing neurons were observed in the piriform cortex, medial septum and the retrochiasmatic area. These findings are consistent with results of previous in situ localization studies of preprogalanin messenger RNA and also with studies reporting the distribution of galanin-like immunoreactivity in rat brain. A novel finding, however, was the detection of preprogalanin messenger RNA in Purkinje cells in the caudal cerebellar vermis (lobules 6 to 10) and the flocculus and paraflocculus of the lateral hemispheres of the cerebellum. Galanin is presumably co-localized in these cells with GABA, which is normally present in Purkinje cells and possibly with tyrosine hydroxylase, which has recently been detected in a similar subpopulation of cerebellar Purkinje cells in both rat and mouse.
Thus, the present study reveals a previously unreported site of galanin gene expression in the cerebellum which represents a novel, putative site of action for galanin to add to its already varied physiological roles.
Noradrenergic regulation of immediate early gene expression in rat forebrain: differential effects of α<inf>l</inf>- and α<inf>2</inf>-adrenoceptor drugs
1995, Molecular Brain Research
Noradrenergic (NAergic) transmission in the rat cerebral cortex has recently been shown to be involved in the regulation of the basal expression of NGFI-A, an immediate early gene (IEG) which encodes a zinc-finger transcription factor. The present study further investigated the role of the NAergic system in mediating cortical IEG expression and possible topographical changes in expression of NGFI-A mRNA in rat forebrain after α₁ and α₂-adrenoceptor (AR) agonist and antagonist treatment. Expression of c-fos and c-jun, which encode leucine-zipper class transcription factors, was also studied. Male Sprague-Dawley rats were injected intraperitoneally with either an α₁-AR agonist (methoxamine, 5 or 10 mg/kg); an α₁-AR antagonist (prazosin, 5 mg/kg); an α₂-AR agonist (clonidine, 0.5 mg/kg); or an α₂-AR antagonist (methoxyidazoxan, 5 mg/kg) and killed after I h. IEG mRNA levels were detected by quantitative in situ hybridization histochemistry using ³⁵S-labelled oligonucleotides. High basal levels of NGFI-A mRNA were present in cortical layers IV and VI, hippocampul CAI, piriform cortex, amygdala and caudate putamen. α₁-AR agonist and antagonist treatment had essentially no effect on IEG mRNA, despite producing characteristic behavioral and peripheral effects at the doses used. Methoxyidazoxan significantly increased (mean%) NGFI-A mRNA in: cerebral cortex (44); caudate putamen (82); amygdala (92); and CA1 of hippocampus (48), while clonidine significantly decreased NGFI-A mRNA in the various cortical layers to a similar extent (27–37%). Basal c-fos mRNA expression was lower than that for NGFI-A in forebrain areas including cortex, caudate putamen and hippocampus. Methoxyidazoxan increased c-fos mRNA in cortex (30%), with no marked effect in other areas. Clonidine had no significant effect on c fos mRNA. In contrast, c-jun mRNA was not altered by any of the α-AR drugs used, although high basal c-jun mRNA levels were present in cortex, CA2–3, dentate gyrus and thalamus. These results suggest that α₂-ARs normally mediate a strong inhibitory influence on NGFI-A expression in rat forebrain and that induction of the cellular transcription factor genes, NGFI-A and c-fos, mediate influences of the NAergic innervation on cortical and subcortical neuron activity.

View all citing articles on Scopus

View full text

Short communicationIncrease in galanin and neuropeptide Y mRNA in locus coeruleus following acute reserpine treatment

Abstract

J. Biol. Chem.

Neuroscience

Neuroscience

Time course of the changes of TH mRNA in rat brain and adrenal medulla after a single injection of reserpine

EMBO J.

Short communication
Increase in galanin and neuropeptide Y mRNA in locus coeruleus following acute reserpine treatment