Biochemical, autoradiographic and functional studies on a unique glutamate binding site in adrenal gland

doi:10.1016/0165-1838(92)90227-8

Journal of the Autonomic Nervous System

Volume 40, Issue 1, August 1992, Pages 71-85

Journal of the Auton...

https://doi.org/10.1016/0165-1838(92)90227-8 Get rights and content

Abstract

l-Glutamate is known to function as a major excitatory neurotransmitter in the mammalian central nervous system, and recent reports suggest the existence of receptors for glutamate in several peripheral tissues. In the present study, the characteristics of the binding of [³H]l-glutamate to sections of bovine adrenal gland were studied, and the localisation of this binding was investigated in adrenal glands from cow, dog, rat and guinea pig. In addition, the effects of glutamate on catecholamine release from the perfused isolated bovine adrenal gland were investigated. Binding of [³H]l-glutamate to slide-mounted sections of bovine adrenal gland was of high affinity (K_d 0.4 μM), rapid, saturable, reversible, stereospecific and to a single population of sites. The pharmacological profile of this binding site appeared to be unique, and did not correspond to any of the central receptor subtypes for glutamate so far identified. In the adrenal gland of the cow, rat and guinea pig, the binding density of [³H]l-glutamate was higher in cortex than medulla, while this pattern was reversed in the canine adrenal gland. Glutamate had no effect on the basal secretion of noradrenaline or adrenaline from the perfused isolated bovine adrenal gland, and neither glutamate nor the glutamate receptor antagonist kynurenate altered the nicotine-stimulated release of these catecholamines. These results suggest the existence of a novel peripheral binding site for glutamate in the adrenal gland. The differential autoradiographic localisation of this binding site in the adrenal glands of the various species studied may reflect different functional properties of glutamate in these species, and suggests possible roles for glutamate in the modulation of adrenal function.

References (56)

P. Aas et al.
Stimulation of peripheral nerves by glutamate indicates a new peripheral glutamate receptor
Eur. J. Pharmacol.
(1989)
P. Boksa
Dopamine release from bovine adrenal medullary cells in culture
J. Auton. Nerv. Syst.
(1990)
S.J. Bunn et al.
The distribution of opioid binding subtypes in the bovine adrenal medulla
Neuroscience
(1988)
M. Cincotta et al.
Biochemical characterization of an autoradiographic method for studying excitatory amino acid receptors using l-[³H]glutamate
Anal. Biochem.
(1989)
G.E. Fagg et al.
Chloride and calcium ions separate l-glutamate receptor populations in synaptic membranes
Eur. J. Pharmacol.
(1983)
A.C. Foster et al.
Acidic amino acid binding sites in mammalian neuronal membranes: Their characteristics and relationship to synaptic receptors
Brain Res. Rev.
(1984)
P.D. Marley et al.
Localization of angiotensin II binding sites in the bovine adrenal medulla using a labelled specific antagonist
Neuroscience
(1989)
R. Maurer et al.
Distribution and coregulation of three peptide receptors in adrenals
Eur. J. Pharmacol.
(1986)
M.L. Mayer et al.
The physiology of excitatory amino acids in the vertebrate central nervous system
Progr. Neurobiol.
(1987)
E.E. Mena et al.
Chloride ions enhance l-glutamate binding to rat brain synaptic membranes
Brain Res.
(1982)

I. Moeller et al.

Actions of somatostatin on perfused bovine adrenal glands and cultured bovine adrenal medullary cells

Brain Res.

(1989)

F. Moroni et al.

The presence of $N- methyl - d - aspartate - type$ receptors for glutamic acid in the guinea pig myenteric plexus

Neurosci. Lett.

(1986)

F. Moroni et al.

Glycine and kynurenate modulate the glutamate receptors in the myenteric plexus and in cortical membranes

Eur. J. Pharmacol.

(1989)

H. Nakamuta et al.

Characterization of [³H]glutamate binding sites on frozen sections from rat adrenal

Neurochem. Int.

(1987)

T. Nishikawa et al.

Stimulation of catecholamine release from isolated adrenal glands by some amino acids

Jpn. J. Pharmacol.

(1982)

A. Nistri et al.

Pharmacological characterization of different types of GABA and glutamate receptors in vertebrates and invertebrates

Prog. Neurobiol.

(1979)

E. Palmer et al.

Trans-ACPD, a selective agonist of the phosphoinositide-coupled excitatory amino acid receptor

Eur. J. Pharmacol.

(1989)

A. Reggiani et al.

Effect of 7-chlorokynurenic acid on glycine modulation of the $N- methyl - d - aspartate$ response in guinea-pig myenteric plexus

Eur. J. Pharmacol.

(1989)

M.B. Robinson et al.

Quisqualate selectively inhibits a brain peptidase which cleaves $N- acetyl - l - aspartyl - l - glutamate$ in vitro

Eur. J. Pharmacol.

(1986)

M.B. Robinson et al.

Exposure of hippocampal slices to quisqualate sensitizes synaptic responses to phosphonate-containing analogues of glutamate

Brain Res.

(1986)

M.B. Robinson et al.

Hydrolysis of the brain dipeptide $N- acetyl - l - aspartyl - l - gluamate$ : identification and characterization of a novel N-acylated α-linked acidic dipeptidase activity from rat brain

J. Biol. Chem.

(1987)

Y. Yoneda et al.

Localization of [³H]glutamate binding sites in rat adrenal medulla

Brain Res.

(1986)

Y. Yoneda et al.

[³H]glutamate binding sites in the rat pituitary

Neurosci. Res.

(1986)

Y. Yoneda et al.

Enhancement of [³H]glutamate binding by $N- methyl - d - aspartic$ acid in rat adrenal

Brain Res.

(1987)

Y. Yoneda et al.

Characterization of quisqualate-sensitive [³H]glutamate binding activity solubilized from rat adrenal

Neurochem. Int.

(1989)

Y. Yoneda et al.

Solubilization of stereospecific and quisqualate-sensitive activity of [³H]glutamate binding in the pituitary of the rat

Neuropharmacology

(1989)

A.B. Young et al.

EAA pharmacology: Excitatory amino acid receptors in the brain: membrane binding and receptor autoradiographic approaches

Trends Pharmacol. Sci.

(1990)

R. Zaczek et al.

Characteristics of chloride-dependent incorporation of glutamate into brain membranes argue against a receptor binding site

Neuropharmacology

(1987)

Cited by (11)

Molecular mechanisms of glutamate release by bovine chromaffin cells in primary culture
2003, Neuroscience
Previous work indicated that glutamate could be involved in the regulation of catecholamine secretion in bovine chromaffin cells. Thus, the question arises on the source of this putative regulatory glutamate. In this work we have examined the possibility that glutamate could be released from chromaffin cells. Data from this study indicate that chromaffin cells are able to release glutamate when they are stimulated by different depolarising agents such as 60 mM KCl, 1 mM 4-aminopyridine or 50 μM veratridine. The amount of glutamate released by these compounds was 0.32 nmol/10⁶ cells (9.24% of cellular glutamate content), 0.275 (7.86%) and 0.158 (4.52%) for KCl, 4-AP and veratridine stimulation, respectively. All these catecholamine-secretagogues induced glutamate secretion by two mechanisms: 1) a Ca²⁺-dependent, probably exocytotic, mechanism and 2) a Ca²⁺-independent mechanism mediated by reversion of the electrogenic glutamate transporter. Analysis of Ca²⁺-dependent and independent releases for different compounds carried out by several experimental approaches, indicate that Ca²⁺-dependent release was the predominant mechanism for release induced by 4-aminopyridine (84% of total release) and high KCl (63%) whilst Ca²⁺-independent release was predominant for veratridine (67%). The Ca²⁺-dependent glutamate release evoked by depolarisation of chromaffin cells with high KCl and 4-AP could be split into both a fast and a slow kinetic component, which might correspond to the release of docked and mobilised chromaffin granules, respectively. On the other hand, depolarisation of cells with veratridine result in glutamate release with only the fast kinetic component. In the case of 60 mM KCl-evoked glutamate release, the fast component exhibited a decay time of <1 s and accounted for 0.63 nmol glu/6×10⁶ cells (70% of total exocytotic release), whereas the slow component, which exhibited a decay time of 231 s, accounted for the release of 0.27 nmol glu/6×10⁶ cells (30% of total exocytotic release). By contrast in the case of 4-aminopyridine the fast component of exocytosis only represents a 19% of total secretion and the slow a 81% with a decay time of 94 s. These data are very similar to those found in neurones and support the possible intracellular origin of glutamate having a role in the regulation of catecholamine secretion from chromaffin cells. In support of this, we have found that glutamate secretion could be evoked by stimulation of the nicotinic cholinergic receptors.
Limbic seizures induce neuropeptide and chromogranin mRNA expression in rat adrenal medulla
1997, Molecular Brain Research
Rats treated with kainic acid develop limbic seizures and have elevated levels of circulating catecholamines resulting from an extensive stimulation of the adrenal gland. We investigated the levels of several constituents of chromaffin granules in rat adrenal medulla after injection of kainic acid. This treatment increased mRNA steady-state levels of enkephalin, neuropeptide Y and chromogranin B 2–6-fold. Elevated levels of these constituents were found as early as 2 h after treatment and lasted up to 24 h. Chromogranin A and secretogranin II mRNA levels, on the other hand, remained unchanged. Adrenal catecholamine concentrations were reduced by 80%. Pre-treatment of rats with thiopental prior to kainic acid prevented seizures, the decline in catecholamines and the elevation of enkephalin and neuropeptide Y mRNAs but not that of chromogranin B. On the other hand, the peripherally acting ganglionic blocker chlorisondamine did not protect from the kainic acid-induced up-regulation of chromogranin B mRNA, suggesting that chromogranin B mRNA may be regulated by a direct effect of kainic acid on chromaffin cells. The pattern of changes in mRNA expression differed from that seen after insulin hypoglycemia or reserpine treatment. Thus, stimulation of the splanchnic innervation in vivo by various means leads to an individual and independent regulation of granule constituents by quite different mechanisms.
Differential expression of AMPA glutamate receptor mRNAs in the rat adrenal gland
1993, FEBS Letters
Localisation of mRNA encoding the four AMPA glutamate receptor subunits in the rat adrenal gland was investigated using in situ hybridisation. GluR1 is found in the zona glomerulosa of the cortex, GluR3 in the remaining parts of the cortex, GluR2 in adrenal medullary cells and GluR4 at a very low level in the zona glomerulosa. All four receptor mRNAs are found in medullary ganglion cells. The flip form of GluR2 and GluR3 dominate and the GluR2 mRNA is present in the arginine encoding form. Different cell populations of the adrenal gland may express homomeric forms of different receptor subtypes.
Immunocytochemical localization of metabotrophic (mGluR2/3 and mGluR4a) and ionotropic (GluR2/3) glutamate receptors in adrenal medullary ganglion cells
2006, Histology and Histopathology
Glutamate receptors in endocrine tissues
2005, Glutamate Receptors in Peripheral Tissue: Excitatory Transmission Outside the CNS
Adrenal glutamate receptors: A role in stress and drug addiction?
2005, Glutamate Receptors in Peripheral Tissue: Excitatory Transmission Outside the CNS

View all citing articles on Scopus

View full text

Research paperBiochemical, autoradiographic and functional studies on a unique glutamate binding site in adrenal gland

Abstract

Eur. J. Pharmacol.

J. Auton. Nerv. Syst.

Neuroscience

Anal. Biochem.

Eur. J. Pharmacol.

Brain Res. Rev.

Neuroscience

Eur. J. Pharmacol.

Progr. Neurobiol.

Brain Res.

Brain Res.

Neurosci. Lett.

Eur. J. Pharmacol.

Neurochem. Int.

Jpn. J. Pharmacol.

Prog. Neurobiol.

Eur. J. Pharmacol.

Eur. J. Pharmacol.

Eur. J. Pharmacol.

Brain Res.

J. Biol. Chem.

Brain Res.

Neurosci. Res.

Brain Res.

Neurochem. Int.

Neuropharmacology

Trends Pharmacol. Sci.

Neuropharmacology

Research paper
Biochemical, autoradiographic and functional studies on a unique glutamate binding site in adrenal gland