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Erschienen in: Acta Neurologica Belgica 3/2020

21.08.2018 | Original Article

Involvement of glutamate receptors of the paragigantocellularis lateralis nucleus in the pain modulatory effect of 17β-estradiol in male rats

verfasst von: Roghaieh Khakpay, Maryam Azaddar, Fatemeh Khakpai

Erschienen in: Acta Neurologica Belgica | Ausgabe 3/2020

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Abstract

The pain modulatory role of the paragigantocellularis lateralis nucleus (LPGi) and the 17β-estradiol has thoroughly been probed. This study investigates the contribution of ionotropic glutamate receptors in pain modulatory effect of intra-LPGi injection of 17β-estradiol. For this purpose, the LPGi nucleus cannulation was performed and drugs were injected into this nucleus, 15 min prior to the formalin test. The duration of formalin-induced flexing and licking behaviors was recorded for 60 min immediately after formalin injection. The results showed that the flexing behavior is significantly decreased by intra-LPGi injection of 0.8 µmol 17β-estradiol duringboth phases of formalin test (P < 0.001). However, 17β-estradiol attenuated the licking duration only in the second phase (P < 0.001). Interestingly, NMDA and AMPA/kainate receptor antagonists (AP5 and CNQX, respectively) significantly counteracted the analgesic effect of intra-LPGi injection of 17β-estradiol in both phases of the formalin test (P < 0.001). Consequently, the revealing results showed that the analgesic effect of intra-LPGi injection of 17β-estradiol on acute inflammatory pain might be mediated via the activation of ionotropic glutamate receptors.
Literatur
1.
Zurück zum Zitat Millan M (1997) The role of descending noradrenergic and serotoninergic pathways in the modulation of nociception: focus on receptor multiplicity. In: Dickenson A, Besson JM (eds) The pharmacology of pain, vol 130. Springer. Berlin, Heidelberg, pp 385–446CrossRef Millan M (1997) The role of descending noradrenergic and serotoninergic pathways in the modulation of nociception: focus on receptor multiplicity. In: Dickenson A, Besson JM (eds) The pharmacology of pain, vol 130. Springer. Berlin, Heidelberg, pp 385–446CrossRef
2.
Zurück zum Zitat Sajedianfard J, Nazarian Z (2011) The role of left and right Locus Coeruleus in formalin test in rats. Physiol Pharmacol 15(2):277–287 Sajedianfard J, Nazarian Z (2011) The role of left and right Locus Coeruleus in formalin test in rats. Physiol Pharmacol 15(2):277–287
3.
Zurück zum Zitat Singewald N, Philippu A (1998) Release of neurotransmitters in the locus coeruleus. Prog Neurobiol 56(2):237–267PubMedCrossRef Singewald N, Philippu A (1998) Release of neurotransmitters in the locus coeruleus. Prog Neurobiol 56(2):237–267PubMedCrossRef
4.
Zurück zum Zitat Aston-Jones G, Chiang C, Alexinsky T (1991) Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog Brain Res 88:501–520PubMedCrossRef Aston-Jones G, Chiang C, Alexinsky T (1991) Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog Brain Res 88:501–520PubMedCrossRef
5.
Zurück zum Zitat Van Bockstaele E, Akaoka H, Aston-Jones G (1993) Brainstem afferents to the rostral (juxtafacial) nucleus paragigantocellularis: integration of exteroceptive and interoceptive sensory inputs in the ventral tegmentum. Brain Res 603(1):1–18PubMedCrossRef Van Bockstaele E, Akaoka H, Aston-Jones G (1993) Brainstem afferents to the rostral (juxtafacial) nucleus paragigantocellularis: integration of exteroceptive and interoceptive sensory inputs in the ventral tegmentum. Brain Res 603(1):1–18PubMedCrossRef
6.
Zurück zum Zitat Arita H, Kogo N, Ichikawa K (1988) Locations of medullary neurons with non-phasic discharges excited by stimulation of central and/or peripheral chemoreceptors and by activation of nociceptors in cat. Brain Res 442(1):1–10PubMedCrossRef Arita H, Kogo N, Ichikawa K (1988) Locations of medullary neurons with non-phasic discharges excited by stimulation of central and/or peripheral chemoreceptors and by activation of nociceptors in cat. Brain Res 442(1):1–10PubMedCrossRef
7.
Zurück zum Zitat Fathi-Moghaddam H, Kesmati M, Mohammad Pour Kargar H (2006) The effect of paragigantocellularis lateralis lesion on conditioned place preference (CPP) in presence or absence of a 2 adrenergic agonist (clonidine) in male rats. Acta Physiol Hung 93(1):33–40PubMedCrossRef Fathi-Moghaddam H, Kesmati M, Mohammad Pour Kargar H (2006) The effect of paragigantocellularis lateralis lesion on conditioned place preference (CPP) in presence or absence of a 2 adrenergic agonist (clonidine) in male rats. Acta Physiol Hung 93(1):33–40PubMedCrossRef
9.
Zurück zum Zitat Khakpay R, Semnanian S, Javan M, Janahmadi M (2010) The effect of intra-locus coeruleus injection of 17β-estradiol on inflammatory pain modulation in male rat. Behav Brain Res 214(2):409–416PubMedCrossRef Khakpay R, Semnanian S, Javan M, Janahmadi M (2010) The effect of intra-locus coeruleus injection of 17β-estradiol on inflammatory pain modulation in male rat. Behav Brain Res 214(2):409–416PubMedCrossRef
10.
Zurück zum Zitat Zarmehri HA, Semnanian S, Fathollahi Y, Erami E, Khakpay R, Azizi H, Rohampour K (2011) Intra-periaqueductal gray matter microinjection of orexin-A decreases formalin-induced nociceptive behaviors in adult male rats. J Pain 12(2):280–287CrossRef Zarmehri HA, Semnanian S, Fathollahi Y, Erami E, Khakpay R, Azizi H, Rohampour K (2011) Intra-periaqueductal gray matter microinjection of orexin-A decreases formalin-induced nociceptive behaviors in adult male rats. J Pain 12(2):280–287CrossRef
11.
Zurück zum Zitat Semnanian S, Fathollahi Y (2008) Comparing the analgesic effects of periaqueductal gray matter injection of orexin A and morphine on formalin-induced nociceptive behaviors. Physiol Pharmacol 12(3):188–193 Semnanian S, Fathollahi Y (2008) Comparing the analgesic effects of periaqueductal gray matter injection of orexin A and morphine on formalin-induced nociceptive behaviors. Physiol Pharmacol 12(3):188–193
12.
Zurück zum Zitat Khakpay R, Azaddar M, Khakpai F (2016) The antinociceptive effect of 17β-estradiol in the nucleus paragigantocellularis lateralis of male rats may be mediated by the NMDA receptors. Physiol Pharmacol 20(2):122–129 Khakpay R, Azaddar M, Khakpai F (2016) The antinociceptive effect of 17β-estradiol in the nucleus paragigantocellularis lateralis of male rats may be mediated by the NMDA receptors. Physiol Pharmacol 20(2):122–129
13.
Zurück zum Zitat Yukhananov R, Guan J, Crosby G (2002) Antisense oligonucleotides to N-methyl-d-aspartate receptor subunits attenuate formalin-induced nociception in the rat. Brain Res 930(1–2):163–169PubMedCrossRef Yukhananov R, Guan J, Crosby G (2002) Antisense oligonucleotides to N-methyl-d-aspartate receptor subunits attenuate formalin-induced nociception in the rat. Brain Res 930(1–2):163–169PubMedCrossRef
14.
Zurück zum Zitat Yashpal K, Fisher K, Chabot JG, Coderre TJ (2001) Differential effects of NMDA and group I mGluR antagonists on both nociception and spinal cord protein kinase C translocation in the formalin test and a model of neuropathic pain in rats. Pain 94(1):17–29PubMedCrossRef Yashpal K, Fisher K, Chabot JG, Coderre TJ (2001) Differential effects of NMDA and group I mGluR antagonists on both nociception and spinal cord protein kinase C translocation in the formalin test and a model of neuropathic pain in rats. Pain 94(1):17–29PubMedCrossRef
15.
Zurück zum Zitat Kandel ER, Schwartz JH, Jessell TM, SA S, AJ H (2012) Principles of neural science, 15th edn. Academic Press, NewYork Kandel ER, Schwartz JH, Jessell TM, SA S, AJ H (2012) Principles of neural science, 15th edn. Academic Press, NewYork
20.
Zurück zum Zitat Khakpay R, Azaddar M, Khakpai F, Hatami Nemati H (2015) The role of GABAA receptors in the analgesic effect of intra-paragigantocellularis lateralis injection of 17β-estradiol in male rat. Physiol Pharmacol 19(2):99–106CrossRef Khakpay R, Azaddar M, Khakpai F, Hatami Nemati H (2015) The role of GABAA receptors in the analgesic effect of intra-paragigantocellularis lateralis injection of 17β-estradiol in male rat. Physiol Pharmacol 19(2):99–106CrossRef
22.
Zurück zum Zitat Khakpay R, Ansari S, Khakpai F (2017) The antinociceptive effect of 17β-estradiol in the paragigantocellularis lateralis nucleus of ovariectomized female rats mediated by estrogen receptors. Arak Med Univ J 20(125):29–38 Khakpay R, Ansari S, Khakpai F (2017) The antinociceptive effect of 17β-estradiol in the paragigantocellularis lateralis nucleus of ovariectomized female rats mediated by estrogen receptors. Arak Med Univ J 20(125):29–38
25.
Zurück zum Zitat Tanaka M, Sokabe M (2013) Bidirectional modulatory effect of 17β-estradiol on NMDA receptors via ERα and ERβ in the dentate gyrus of juvenile male rats. Neuropharmacology 75:262–273PubMedCrossRef Tanaka M, Sokabe M (2013) Bidirectional modulatory effect of 17β-estradiol on NMDA receptors via ERα and ERβ in the dentate gyrus of juvenile male rats. Neuropharmacology 75:262–273PubMedCrossRef
26.
Zurück zum Zitat Wong M, Moss RL (1992) Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J Neurosc 12(8):3217–3225CrossRef Wong M, Moss RL (1992) Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J Neurosc 12(8):3217–3225CrossRef
28.
Zurück zum Zitat Khakpay R, Azaddar M, Khakpay F, Hatami Nemati H (2017) Analgesic effect of 17β-estradiol on nucleus paragigantocellularis lateralis of male rats mediated via GABAA receptors. Basic Clin Neurosci 8(1):51–60PubMedPubMedCentral Khakpay R, Azaddar M, Khakpay F, Hatami Nemati H (2017) Analgesic effect of 17β-estradiol on nucleus paragigantocellularis lateralis of male rats mediated via GABAA receptors. Basic Clin Neurosci 8(1):51–60PubMedPubMedCentral
31.
Zurück zum Zitat Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th ed. Academic Press, London Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th ed. Academic Press, London
32.
33.
Zurück zum Zitat Aloisi AM, Ceccarelli I, Lupo C (1998) Behavioural and hormonal effects of restraint stress and formalin test in male and female rats. Brain Res Bull 47(1):57–62PubMedCrossRef Aloisi AM, Ceccarelli I, Lupo C (1998) Behavioural and hormonal effects of restraint stress and formalin test in male and female rats. Brain Res Bull 47(1):57–62PubMedCrossRef
34.
Zurück zum Zitat Mahmoudi M, Zarrindast MR (2002) Effect of intracerebroventricular injection of GABA receptor agents on morphine-induced antinociception in the formalin test. J Psychopharmacol 16(1):85–91PubMedCrossRef Mahmoudi M, Zarrindast MR (2002) Effect of intracerebroventricular injection of GABA receptor agents on morphine-induced antinociception in the formalin test. J Psychopharmacol 16(1):85–91PubMedCrossRef
35.
Zurück zum Zitat Stening KD, Eriksson O, Henriksson KG, Brynhildsen J, Lindh-Astrand L, Berg G, Hammar M, Amandusson A, Blomqvist A (2011) Hormonal replacement therapy does not affect self-estimated pain or experimental pain responses in post-menopausal women suffering from fibromyalgia: a double-blind, randomized, placebo-controlled trial. Rheumatology 50(3):544–551. https://doi.org/10.1093/rheumatology/keq348 PubMedCrossRef Stening KD, Eriksson O, Henriksson KG, Brynhildsen J, Lindh-Astrand L, Berg G, Hammar M, Amandusson A, Blomqvist A (2011) Hormonal replacement therapy does not affect self-estimated pain or experimental pain responses in post-menopausal women suffering from fibromyalgia: a double-blind, randomized, placebo-controlled trial. Rheumatology 50(3):544–551. https://​doi.​org/​10.​1093/​rheumatology/​keq348 PubMedCrossRef
43.
Zurück zum Zitat Moura PJ, Petersen SL (2010) Estradiol acts through nuclear- and membrane-initiated mechanisms to maintain a balance between GABAergic and glutamatergic signaling in the brain: implications for hormone replacement therapy. Rev Neurosci 21(5):363–380PubMedCrossRef Moura PJ, Petersen SL (2010) Estradiol acts through nuclear- and membrane-initiated mechanisms to maintain a balance between GABAergic and glutamatergic signaling in the brain: implications for hormone replacement therapy. Rev Neurosci 21(5):363–380PubMedCrossRef
44.
Zurück zum Zitat Azhdari-Zarmehri H, Semnanian S, Fathollahi Y, Pakdel FG (2014) Tail flick modification of orexin-a induced changes of electrophysiological parameters in the rostral ventromedial medulla. Cell J 16(2):131–140PubMedPubMedCentral Azhdari-Zarmehri H, Semnanian S, Fathollahi Y, Pakdel FG (2014) Tail flick modification of orexin-a induced changes of electrophysiological parameters in the rostral ventromedial medulla. Cell J 16(2):131–140PubMedPubMedCentral
45.
Zurück zum Zitat Azhdari-Zarmehri H, Semnanian S, Fathollahi Y (2015) Orexin-a modulates firing of rat rostral ventromedial medulla neurons: an in vitro study. Cell J 17(1):163–170PubMedPubMedCentral Azhdari-Zarmehri H, Semnanian S, Fathollahi Y (2015) Orexin-a modulates firing of rat rostral ventromedial medulla neurons: an in vitro study. Cell J 17(1):163–170PubMedPubMedCentral
46.
Zurück zum Zitat Shamsizadeh A, Soliemani N, Mohammad-Zadeh M, Azhdari-Zarmehri H (2014) Permanent lesion in rostral ventromedial medulla potentiates swim stress-induced analgesia in formalin test. Iran J Basic Med Sci 17(3):209–215PubMedPubMedCentral Shamsizadeh A, Soliemani N, Mohammad-Zadeh M, Azhdari-Zarmehri H (2014) Permanent lesion in rostral ventromedial medulla potentiates swim stress-induced analgesia in formalin test. Iran J Basic Med Sci 17(3):209–215PubMedPubMedCentral
49.
Zurück zum Zitat Coderre TJ, Van Empel I (1994) The utility of excitatory amino acid (EAA) antagonists as analgesic agents. I. Comparison of the antinociceptive activity of various classes of EAA antagonists in mechanical, thermal and chemical nociceptive tests. Pain 59(3):345–352PubMedCrossRef Coderre TJ, Van Empel I (1994) The utility of excitatory amino acid (EAA) antagonists as analgesic agents. I. Comparison of the antinociceptive activity of various classes of EAA antagonists in mechanical, thermal and chemical nociceptive tests. Pain 59(3):345–352PubMedCrossRef
Metadaten
Titel
Involvement of glutamate receptors of the paragigantocellularis lateralis nucleus in the pain modulatory effect of 17β-estradiol in male rats
verfasst von
Roghaieh Khakpay
Maryam Azaddar
Fatemeh Khakpai
Publikationsdatum
21.08.2018
Verlag
Springer International Publishing
Erschienen in
Acta Neurologica Belgica / Ausgabe 3/2020
Print ISSN: 0300-9009
Elektronische ISSN: 2240-2993
DOI
https://doi.org/10.1007/s13760-018-0998-5

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