دورية أكاديمية
أعرض في EDS

NMDA Receptor Activation and Ca 2+ /PKC Signaling in Nicotine-Induced GABA Transport Shift in Embryonic Chick Retina.

التفاصيل البيبلوغرافية
العنوان: NMDA Receptor Activation and Ca 2+ /PKC Signaling in Nicotine-Induced GABA Transport Shift in Embryonic Chick Retina.
المؤلفون: Souto AC; Laboratório de Neurofarmacologia, Departamento de Fisiologia e Farmacologia, Universidade Federal Fluminense, Inst Biomédico - Rua São João Batista, 187, Sala 416, Centro, Niterói, CEPRJ, 24020-005, Brazil., Tempone MH; Laboratório de Neuroquímica. IBCCF, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil., Gonçalves LAC; Laboratório de Neurofarmacologia, Departamento de Fisiologia e Farmacologia, Universidade Federal Fluminense, Inst Biomédico - Rua São João Batista, 187, Sala 416, Centro, Niterói, CEPRJ, 24020-005, Brazil., Borges-Martins VPP; Laboratório de Neurofarmacologia, Departamento de Fisiologia e Farmacologia, Universidade Federal Fluminense, Inst Biomédico - Rua São João Batista, 187, Sala 416, Centro, Niterói, CEPRJ, 24020-005, Brazil., Peixoto-Rodrigues MC; Laboratório de Neuroplasticidade, Departamento de Neurobiologia, Instituto de Biologia, Universidade Federal Fluminense, Niterói, RJ, Brazil., Damascena ACO; Laboratório de Neurofarmacologia, Departamento de Fisiologia e Farmacologia, Universidade Federal Fluminense, Inst Biomédico - Rua São João Batista, 187, Sala 416, Centro, Niterói, CEPRJ, 24020-005, Brazil., Ferraz G; Laboratório de Farmacologia Molecular, ICB, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil., Manhães AC; Laboratório de Neurofisiologia, IBRAG, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil., Castro NG; Laboratório de Farmacologia Molecular, ICB, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil., de Melo Reis RA; Laboratório de Neuroquímica. IBCCF, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil., Ventura ALM; Laboratório de Neuroquímica, Departamento de Neurobiologia, Universidade Federal Fluminense, Rio de Janeiro, RJ, Brazil., Kubrusly RCC; Laboratório de Neurofarmacologia, Departamento de Fisiologia e Farmacologia, Universidade Federal Fluminense, Inst Biomédico - Rua São João Batista, 187, Sala 416, Centro, Niterói, CEPRJ, 24020-005, Brazil. reginakubrusly@id.uff.br.
المصدر: Neurochemical research [Neurochem Res] 2023 Jul; Vol. 48 (7), pp. 2104-2115. Date of Electronic Publication: 2023 Feb 15.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Kluwer Academic/Plenum Publishers Country of Publication: United States NLM ID: 7613461 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-6903 (Electronic) Linking ISSN: 03643190 NLM ISO Abbreviation: Neurochem Res Subsets: MEDLINE
أسماء مطبوعة: Publication: 1999- : New York, NY : Kluwer Academic/Plenum Publishers
Original Publication: New York, Plenum Press
مواضيع طبية MeSH: Nicotine*/pharmacology , Receptors, Nicotinic*/metabolism, Animals ; Receptors, N-Methyl-D-Aspartate/metabolism ; Calcium/metabolism ; gamma-Aminobutyric Acid/metabolism ; Excitatory Amino Acid Antagonists/pharmacology ; Retina
مستخلص: Nicotinic receptors are present in the retina of different vertebrates, and in the chick retina, it is present during early development throughout to post-hatching. These receptors are activated by nicotine, an alkaloid with addictive and neurotransmitter release modulation properties, such as GABA signaling. Here we evaluated the mechanisms of nicotine signaling in the avian retina during the development of neuron-glia cells at a stage where synapses are peaking. Nicotine almost halved [ 3 H]-GABA uptake, reducing it by 45% whilst increasing more than two-fold [ 3 H]-GABA release in E12 embryonic chick retinas. Additionally, nicotine mediated a 33% increase in [ 3 H]-D-aspartate release. MK-801 50 μM blocked 66% of nicotine-induced [ 3 H]-GABA release and Gö 6983 100 nM prevented the nicotine-induced reduction in [ 3 H]-GABA uptake by rescuing 40% of this neurotransmitter uptake, implicating NMDAR and PKC (respectively) in the nicotinic responses. In addition, NO-711 prevented [ 3 H]-GABA uptake and release induced by nicotine. Furthermore, the relevance of calcium influx for PKC activation was evidenced through fura-2 imaging. We conclude that the shift of GABA transport mediated by nicotine promotes GABA release by inducing transporter reversal via nicotine-induced EAA release through EAATs, or by a direct effect of nicotine in activating nicotinic receptors permeable to calcium and promoting PKC pathway activation and shifting GAT-1 activity, both prompting calcium influx, and activation of the PKC pathway and shifting GAT-1 activity.
(© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.)
References: Israel MR, Morgan M, Tay B, Deuis JR (2018) Toxins as tools: fingerprinting neuronal pharmacology. Neurosci Lett 679:4–14. https://doi.org/10.1016/j.neulet.2018.02.001. (PMID: 10.1016/j.neulet.2018.02.00129425731)
Ávila-Ruiz T, Carranza V, Gustavo LL et al (2014) Chronic administration of nicotine enhances NMDA-activated currents in the prefrontal cortex and core part of the nucleus accumbens of rats. Synapse 68:248–256. https://doi.org/10.1002/SYN.21726. (PMID: 10.1002/SYN.2172624549882)
Fowler CD, Turner JR, Imad Damaj M (2020) Molecular mechanisms associated with nicotine pharmacology and dependence. Handb Exp Pharmacol 258:373–393. https://doi.org/10.1007/164_2019_252. (PMID: 10.1007/164_2019_25231267166)
Neal MJ, Cunningham JR, Matthews KL (2001) Activation of nicotinic receptors on GABAergic amacrine cells in the rabbit retina indirectly stimulates dopamine release. Vis Neurosci 18:55–64. https://doi.org/10.1017/S0952523801181058. (PMID: 10.1017/S095252380118105811347816)
Wonnacott S (1997) Presynaptic nicotinic ACh receptors. Trends Neurosci 20:92–98. https://doi.org/10.1016/S0166-2236(96)10073-4. (PMID: 10.1016/S0166-2236(96)10073-49023878)
Reid MS, Fox L, Ho LB, Berger SP (2000) Nicotine stimulation of extracellular glutamate levels in the nucleus accumbens: neuropharmacological characterization. Synapse 35:129–136. https://doi.org/10.1002/(SICI)1098-2396(200002)35:2%3c129::AID-SYN5%3e3.0.CO;2-D. (PMID: 10.1002/(SICI)1098-2396(200002)35:2<129::AID-SYN5>3.0.CO;2-D10611638)
Sears SMS, Hewett SJ (2021) Influence of glutamate and GABA transport on brain excitatory/inhibitory balance. Exp Biol Med 246:1069–1083. https://doi.org/10.1177/1535370221989263. (PMID: 10.1177/1535370221989263)
Popova E (2015) GABAergic neurotransmission and retinal ganglion cell function. J Comp Physiol A 201(3):261–283. https://doi.org/10.1007/S00359-015-0981-Z. (PMID: 10.1007/S00359-015-0981-Z)
Wang L, Shen X, Wu Y, Zhang D (2016) Coffee and caffeine consumption and depression: a meta-analysis of observational studies. Aust N Z J Psychiatry 50:228–242. https://doi.org/10.1177/0004867415603131. (PMID: 10.1177/000486741560313126339067)
da Calaza K, C, Gardino PF, (2010) Neurochemical phenotype and birthdating of specific cell populations in the chick retina. An Acad Bras Cienc 82:595–608. https://doi.org/10.1590/S0001-37652010000300007. (PMID: 10.1590/S0001-3765201000030000721562688)
Thangaraj G, Greif A, Bachmann G, Layer PG (2012) Intricate paths of cells and networks becoming “Cholinergic” in the embryonic chicken retina. J Comp Neurol 520:3181–3193. https://doi.org/10.1002/CNE.23083. (PMID: 10.1002/CNE.2308322886733)
Ferreira DDPDP, Stutz B, de Mello FGG et al (2014) Caffeine potentiates the release of GABA mediated by NMDA receptor activation: Involvement of A1 adenosine receptors. Neuroscience 281:208–215. https://doi.org/10.1016/j.neuroscience.2014.09.060. (PMID: 10.1016/j.neuroscience.2014.09.06025286387)
Sorimachi M, Rhee JS, Shimura M, Akaike N (1997) Mechanisms of GABA- and glycine-induced increases of cytosolic Ca2+ concentrations in chick embryo ciliary ganglion cells. J Neurochem 69:797–805. https://doi.org/10.1046/J.1471-4159.1997.69020797.X. (PMID: 10.1046/J.1471-4159.1997.69020797.X9231741)
Govindpani K, Calvo-Flores Guzman B, Vinnakota C et al (2017) Towards a better understanding of GABAergic remodeling in Alzheimer’s disease. Int J Mol Sci. https://doi.org/10.3390/ijms18081813. (PMID: 10.3390/ijms18081813288256835578199)
Borges-Martins VPP, Ferreira DDP, Souto AC et al (2019) Caffeine regulates GABA transport via A1R blockade and cAMP signaling. Neurochem Int. https://doi.org/10.1016/j.neuint.2019.104550. (PMID: 10.1016/j.neuint.2019.10455031563462)
Eskandari S, Willford SL, Anderson CM (2017) Revised ion/substrate coupling stoichiometry of GABA transporters. Adv Neurobiol 16:85–116. https://doi.org/10.1007/978-3-319-55769-4&#95;5. (PMID: 10.1007/978-3-319-55769-4_528828607)
Bernath S, Zigmond MJ (1988) Characterization of [ 3 H] GABA release from striatal slices: evidence for a calcium-independent process via the GABA uptake system. Neuroscience 27:563–570. https://doi.org/10.1016/0306-4522(88)90289-8. (PMID: 10.1016/0306-4522(88)90289-83217004)
Calaza KC, Gardino PF, de Mello FG (2006) Transporter mediated GABA release in the retina: role of excitatory amino acids and dopamine. Neurochem Int 49:769–777. https://doi.org/10.1016/J.NEUINT.2006.07.003. (PMID: 10.1016/J.NEUINT.2006.07.00316956697)
do Nascimento JL, Ventura AL, Paes de Carvalho R, (1998) Veratridine- and glutamate-induced release of [3H]-GABA from cultured chick retina cells: possible involvement of a GAT-1-like subtype of GABA transporter. Brain Res 798:217–222. (PMID: 10.1016/S0006-8993(98)00417-X9666133)
Whitworth TL, Quick MW (2001) Substrate-induced regulation of γ-aminobutyric acid transporter trafficking requires tyrosine phosphorylation. J Biol Chem 276:42932–42937. https://doi.org/10.1074/jbc.M107638200. (PMID: 10.1074/jbc.M10763820011555659)
Law RM, Stafford A, Quick MW (2000) Functional regulation of γ-aminobutyric acid transporters by direct tyrosine phosphorylation. J Biol Chem 275:23986–23991. https://doi.org/10.1074/jbc.M910283199. (PMID: 10.1074/jbc.M91028319910816599)
Beckman ML, Bernstein EM, Quick MW (1999) Multiple G protein-coupled receptors initiate protein kinase C redistribution of GABA transporters in hippocampal neurons. J Neurosci. https://doi.org/10.1523/JNEUROSCI.19-11-J0006.1999. (PMID: 10.1523/JNEUROSCI.19-11-J0006.1999103412706782603)
Wang D, Quick MW (2005) Trafficking of the plasma membrane gamma-aminobutyric acid transporter GAT1. Size and rates of an acutely recycling pool. J Biol Chem 280:18703–18709. https://doi.org/10.1074/jbc.M500381200. (PMID: 10.1074/jbc.M50038120015778221)
Yang XL (2004) Characterization of receptors for glutamate and GABA in retinal neurons. Prog Neurobiol 73:127–150. https://doi.org/10.1016/J.PNEUROBIO.2004.04.002. (PMID: 10.1016/J.PNEUROBIO.2004.04.00215201037)
Hamassaki-Britto DE, Brzozowska-Prechtl A, Karten HJ et al (1991) GABA-like immunoreactive cells containing nicotinic acetylcholine receptors in the chick retina. J Comp Neurol 313:394–408. https://doi.org/10.1002/CNE.903130213. (PMID: 10.1002/CNE.9031302131765586)
Dmitrieva NA, Lindstrom JM, Keyser KT (2001) The relationship between GABA-containing cells and the cholinergic circuitry in the rabbit retina. Vis Neurosci 18:93–100. https://doi.org/10.1017/S0952523801181083. (PMID: 10.1017/S095252380118108311347820)
Masland RH (2012) The neuronal organization of the retina. Neuron 76:266–280. https://doi.org/10.1016/j.neuron.2012.10.002. (PMID: 10.1016/j.neuron.2012.10.002230837313714606)
Kubrusly RCC, de Mello MCF, de Mello FG (1998) Aspartate as a selective NMDA receptor agonist in cultured cells from the avian retina. Neurochem Int 32:47–52. https://doi.org/10.1016/S0197-0186(97)00051-X. (PMID: 10.1016/S0197-0186(97)00051-X9460701)
Kubrusly RCC, Günter A, Sampaio L et al (2018) Neuro-glial cannabinoid receptors modulate signaling in the embryonic avian retina. Neurochem Int 112:27–37. https://doi.org/10.1016/j.neuint.2017.10.016. (PMID: 10.1016/j.neuint.2017.10.01629108864)
Loureiro-dos-Santos NE, Prado MAM, De Melo Reis RA et al (2002) Regulation of vesicular acetylcholine transporter by the activation of excitatory amino acid receptors in the avian retina. Cell Mol Neurobiol 22:727–740. https://doi.org/10.1023/A:1021809124814. (PMID: 10.1023/A:102180912481412585691)
Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. Dev Dyn 195:231–272. https://doi.org/10.1002/aja.1001950404. (PMID: 10.1002/aja.10019504041304821)
de Freitas APAP, Ferreira DDPDDP, Fernandes A et al (2016) Caffeine alters glutamate–aspartate transporter function and expression in rat retina. Neuroscience 337:285–294. https://doi.org/10.1016/j.neuroscience.2016.09.028. (PMID: 10.1016/j.neuroscience.2016.09.02827663541)
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3. (PMID: 10.1016/0003-2697(76)90527-3942051)
de Melo Reis RA, Freitas HR, de Mello FG (2020) Cell calcium imaging as a reliable method to study neuron-glial circuits. Front Neurosci 14:975. https://doi.org/10.3389/FNINS.2020.569361/BIBTEX. (PMID: 10.3389/FNINS.2020.569361/BIBTEX)
Freitas HR, Ferraz G, Ferreira GC et al (2016) Glutathione-induced calcium shifts in chick retinal glial cells. PLoS One 11:e0153677. https://doi.org/10.1371/JOURNAL.PONE.0153677. (PMID: 10.1371/JOURNAL.PONE.0153677270788784831842)
Castillo-Rolón D, Ramírez-Sánchez E, Arenas-López G et al (2021) Nicotine increases spontaneous glutamate release in the rostromedial tegmental nucleus. Front Neurosci 14:1323. https://doi.org/10.3389/FNINS.2020.604583/BIBTEX. (PMID: 10.3389/FNINS.2020.604583/BIBTEX)
Martins RS, de Freitas IG, Sathler MF et al (2018) Beta-adrenergic receptor activation increases GABA uptake in adolescent mice frontal cortex: modulation by cannabinoid receptor agonist WIN55,212–2. Neurochem Int 120:182–190. https://doi.org/10.1016/j.neuint.2018.08.011. (PMID: 10.1016/j.neuint.2018.08.01130170018)
Scimemi A (2014) Plasticity of GABA transporters: an unconventional route to shape inhibitory synaptic transmission. Front Cell Neurosci 8:128. https://doi.org/10.3389/fncel.2014.00128. (PMID: 10.3389/fncel.2014.00128248604304026733)
Sathler MF, Stutz B, Martins RS et al (2016) Single exposure to cocaine impairs aspartate uptake in the pre-frontal cortex via dopamine D1-receptor dependent mechanisms. Neuroscience 329:326–336. https://doi.org/10.1016/j.neuroscience.2016.05.022. (PMID: 10.1016/j.neuroscience.2016.05.02227208619)
Loring RH, Zigmond RE (1990) Pharmacological and biochemical properties of nicotinic receptors from chick retina. Eur J Neurosci 2:863–872. https://doi.org/10.1111/J.1460-9568.1990.TB00397.X. (PMID: 10.1111/J.1460-9568.1990.TB00397.X12106093)
Ryu IS, Kim J, Seo SY et al (2017) Behavioral changes after nicotine challenge are associated with α7 nicotinic acetylcholine receptor-stimulated glutamate release in the rat dorsal striatum. Sci Rep 7:1–14. https://doi.org/10.1038/s41598-017-15161-7. (PMID: 10.1038/s41598-017-15161-7)
Damborsky JC, Griffith WH, Winzer-Serhan UH (2015) Neonatal nicotine exposure increases excitatory synaptic transmission and attenuates nicotine-stimulated GABA release in the adult rat hippocampus. Neuropharmacology 88:187–198. https://doi.org/10.1016/j.neuropharm.2014.06.010. (PMID: 10.1016/j.neuropharm.2014.06.01024950455)
Lambe EK, Picciotto MR, Aghajanian GK (2003) Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology 28(2):216–225. https://doi.org/10.1038/sj.npp.1300032. (PMID: 10.1038/sj.npp.130003212589374)
Lenoir M, Kiyatkin EA (2013) Intravenous nicotine injection induces rapid, experience-dependent sensitization of glutamate release in the ventral tegmental area and nucleus accumbens. J Neurochem 127:541. https://doi.org/10.1111/JNC.12450. (PMID: 10.1111/JNC.12450240327184529058)
Alasmari F, Al-Rejaie SS, AlSharari SD, Sari Y (2016) Targeting glutamate homeostasis for potential treatment of nicotine dependence. Brain Res Bull 121:1. https://doi.org/10.1016/J.BRAINRESBULL.2015.11.010. (PMID: 10.1016/J.BRAINRESBULL.2015.11.01026589642)
Briggs CA, McKenna DG (1996) Effect of MK-801 at the human α7 nicotinic acetylcholine receptor. Neuropharmacology 35:407–414. https://doi.org/10.1016/0028-3908(96)00006-8. (PMID: 10.1016/0028-3908(96)00006-88793902)
Bennett ER, Kanner BI (1997) The membrane topology of GAT-1, a (Na+ + Cl-)-coupled γ-aminobutyric acid transporter from rat brain. J Biol Chem 272:1203–1210. https://doi.org/10.1074/jbc.272.2.1203. (PMID: 10.1074/jbc.272.2.12038995422)
Zafar S, Jabeen I (2018) Structure, function, and modulation of γ-aminobutyric acid transporter 1 (GAT1) in neurological disorders: a pharmacoinformatic prospective. Front Chem 6:397. https://doi.org/10.3389/fchem.2018.00397. (PMID: 10.3389/fchem.2018.00397302550126141625)
Lee JS, Kim HJ, Ahn CH, Jeon CJ (2017) Expression of nicotinic acetylcholine receptor α4 and β2 subunits on direction-selective retinal ganglion cells in the rabbit. Acta Histochem Cytochem 50:29–37. https://doi.org/10.1267/AHC.16024. (PMID: 10.1267/AHC.16024283861485374101)
Stutz B, Yamasaki EN, De Mello MCF, De Mello FG (2011) Exchange of extracellular l-glutamate by intracellular d-aspartate: the main mechanism of d-aspartate release in the avian retina. Neurochem Int 58:767–775. https://doi.org/10.1016/J.NEUINT.2011.03.001. (PMID: 10.1016/J.NEUINT.2011.03.00121396420)
Blankenship AG, Ford KJ, Johnson J et al (2009) Synaptic and extrasynaptic factors governing glutamatergic retinal waves. Neuron 62:230–241. https://doi.org/10.1016/J.NEURON.2009.03.015. (PMID: 10.1016/J.NEURON.2009.03.015194092682807181)
Stone TW (2021) Relationships and interactions between ionotropic glutamate receptors and nicotinic receptors in the CNS. Neuroscience 468:321–365. https://doi.org/10.1016/J.NEUROSCIENCE.2021.06.007. (PMID: 10.1016/J.NEUROSCIENCE.2021.06.00734111447)
Zhou X, Zong Y, Zhang R et al (2017) Differential modulation of GABAA and NMDA receptors by an α7-nicotinic acetylcholine receptor agonist in chronic glaucoma. Front Mol Neurosci 10:422. https://doi.org/10.3389/FNMOL.2017.00422/BIBTEX. (PMID: 10.3389/FNMOL.2017.00422/BIBTEX293265495741651)
فهرسة مساهمة: Keywords: Acetylcholine; GABA; GABA transport; Glutamate; Nicotine; Nicotinic receptors
المشرفين على المادة: 6M3C89ZY6R (Nicotine)
0 (Receptors, N-Methyl-D-Aspartate)
SY7Q814VUP (Calcium)
56-12-2 (gamma-Aminobutyric Acid)
0 (Excitatory Amino Acid Antagonists)
0 (Receptors, Nicotinic)
تواريخ الأحداث: Date Created: 20230215 Date Completed: 20230515 Latest Revision: 20230515
رمز التحديث: 20230515
DOI: 10.1007/s11064-023-03870-7
PMID: 36792758
قاعدة البيانات: MEDLINE
الوصف
تدمد:1573-6903
DOI:10.1007/s11064-023-03870-7