Separate Mechanisms Regulating Accumbal Taurine Levels During Baseline Conditions and Following Ethanol Exposure in the Rat

Overview

Journal Sci Rep

Specialty Science

Date 2024 Oct 15

PMID 39406746

Authors

Karin Ademar

Lisa Ulenius

Anna Loften

Bo Soderpalm

Louise Adermark

Mia Ericson

Affiliations

Soon will be listed here.

Abstract

Ethanol-induced dopamine release in the nucleus accumbens (nAc) is associated with reward and reinforcement, and for ethanol to elevate nAc dopamine levels, a simultaneous increase in endogenous taurine is required within the same brain region. By employing in vivo microdialysis in male Wistar rats combined with pharmacological, chemogenetic and metabolic approaches, our aim with this study was to identify mechanisms underlying ethanol-induced taurine release. Our results demonstrate that the taurine elevation, elicited by either systemic or local ethanol administration, occurs both in presence and absence of action potential firing or NMDA receptor blockade. Inhibition of volume regulated anion channels did not alter the ethanol-induced taurine levels, while inhibition of the taurine transporter occluded the ethanol-induced taurine increase, putatively due to a ceiling effect. Selective manipulation of nAc astrocytes using G-coupled designer receptors exclusively activated by designer drugs (DREADDs) did not affect ethanol-induced taurine release. However, activation of G-coupled DREADDs, or metabolic inhibition using fluorocitrate, rather enhanced than depressed taurine elevation. Finally, ethanol-induced taurine increase was fully blocked in rats pre-treated with the L-type Ca-channel blocker nicardipine, suggesting that the release is Ca dependent. In conclusion, while astrocytes appear to be important regulators of basal taurine levels in the nAc, they do not appear to be the main cells underlying ethanol-induced taurine release.

References

Morales Mulia M, Moran J, Pasantes-Morales H . Inhibition by dihydropyridines of regulatory volume decrease and osmolyte fluxes in cultured astrocytes is unrelated to extracellular calcium. Neurosci Lett. 1995; 193(3):165-8. DOI: 10.1016/0304-3940(95)11691-o. View

Quertemont E, Devitgh A, de Witte P . Systemic osmotic manipulations modulate ethanol-induced taurine release: a brain microdialysis study. Alcohol. 2003; 29(1):11-9. DOI: 10.1016/s0741-8329(02)00324-5. View

Aschner M, Vitarella D, Allen J, Conklin D, Cowan K . Methylmercury-induced inhibition of regulatory volume decrease in astrocytes: characterization of osmoregulator efflux and its reversal by amiloride. Brain Res. 1998; 811(1-2):133-42. DOI: 10.1016/s0006-8993(98)00629-5. View

Ramirez-Guerrero S, Guardo-Maya S, Medina-Rincon G, Orrego-Gonzalez E, Cabezas-Perez R, Gonzalez-Reyes R . Taurine and Astrocytes: A Homeostatic and Neuroprotective Relationship. Front Mol Neurosci. 2022; 15:937789. PMC: 9294388. DOI: 10.3389/fnmol.2022.937789. View

DAscenzo M, Vairano M, Andreassi C, Navarra P, Azzena G, Grassi C . Electrophysiological and molecular evidence of L-(Cav1), N- (Cav2.2), and R- (Cav2.3) type Ca2+ channels in rat cortical astrocytes. Glia. 2004; 45(4):354-63. DOI: 10.1002/glia.10336. View

Chau P, Lido H, Soderpalm B, Ericson M . Acamprosate's ethanol intake-reducing effect is associated with its ability to increase dopamine. Pharmacol Biochem Behav. 2018; 175:101-107. DOI: 10.1016/j.pbb.2018.09.009. View

Allansson L, Khatibi S, Olsson T, Hansson E . Acute ethanol exposure induces [Ca2+]i transients, cell swelling and transformation of actin cytoskeleton in astroglial primary cultures. J Neurochem. 2001; 76(2):472-9. DOI: 10.1046/j.1471-4159.2001.00097.x. View

McCarty N, ONeil R . Calcium signaling in cell volume regulation. Physiol Rev. 1992; 72(4):1037-61. DOI: 10.1152/physrev.1992.72.4.1037. View

Afzal A, Figueroa E, Kharade S, Bittman K, Matlock B, Flaherty D . The LRRC8 volume-regulated anion channel inhibitor, DCPIB, inhibits mitochondrial respiration independently of the channel. Physiol Rep. 2019; 7(23):e14303. PMC: 6900491. DOI: 10.14814/phy2.14303. View

10.

de Beun R, Schneider R, Klein A, Lohmann A, De Vry J . Effects of nimodipine and other calcium channel antagonists in alcohol-preferring AA rats. Alcohol. 1996; 13(3):263-71. DOI: 10.1016/0741-8329(95)02054-3. View

11.

Ericson M, Chau P, Clarke R, Adermark L, Soderpalm B . Rising taurine and ethanol concentrations in nucleus accumbens interact to produce dopamine release after ethanol administration. Addict Biol. 2010; 16(3):377-85. DOI: 10.1111/j.1369-1600.2010.00245.x. View

12.

Pasantes-Morales H, Morales Mulia S . Influence of calcium on regulatory volume decrease: role of potassium channels. Nephron. 2000; 86(4):414-27. DOI: 10.1159/000045829. View

13.

Bowens N, Dohare P, Kuo Y, Mongin A . DCPIB, the proposed selective blocker of volume-regulated anion channels, inhibits several glutamate transport pathways in glial cells. Mol Pharmacol. 2012; 83(1):22-32. PMC: 3533478. DOI: 10.1124/mol.112.080457. View

14.

Zorec R, Araque A, Carmignoto G, Haydon P, Verkhratsky A, Parpura V . Astroglial excitability and gliotransmission: an appraisal of Ca2+ as a signalling route. ASN Neuro. 2012; 4(2). PMC: 3310306. DOI: 10.1042/AN20110061. View

15.

Adermark L, Clarke R, Olsson T, Hansson E, Soderpalm B, Ericson M . Implications for glycine receptors and astrocytes in ethanol-induced elevation of dopamine levels in the nucleus accumbens. Addict Biol. 2010; 16(1):43-54. DOI: 10.1111/j.1369-1600.2010.00206.x. View

16.

Li G, Liu Y, Olson J . Calcium/calmodulin-modulated chloride and taurine conductances in cultured rat astrocytes. Brain Res. 2002; 925(1):1-8. DOI: 10.1016/s0006-8993(01)03235-8. View

17.

Hussy N, Deleuze C, Desarmenien M, Moos F . Osmotic regulation of neuronal activity: a new role for taurine and glial cells in a hypothalamic neuroendocrine structure. Prog Neurobiol. 2000; 62(2):113-34. DOI: 10.1016/s0301-0082(99)00071-4. View

18.

Agulhon C, Boyt K, Xie A, Friocourt F, Roth B, McCarthy K . Modulation of the autonomic nervous system and behaviour by acute glial cell Gq protein-coupled receptor activation in vivo. J Physiol. 2013; 591(22):5599-609. PMC: 3853498. DOI: 10.1113/jphysiol.2013.261289. View

19.

Liu Y, Harding M, Pittman A, Dore J, Striessnig J, Rajadhyaksha A . Cav1.2 and Cav1.3 L-type calcium channels regulate dopaminergic firing activity in the mouse ventral tegmental area. J Neurophysiol. 2014; 112(5):1119-30. PMC: 4122730. DOI: 10.1152/jn.00757.2013. View

20.

Timmerman W, Cisci G, Nap A, DE VRIES J, Westerink B . Effects of handling on extracellular levels of glutamate and other amino acids in various areas of the brain measured by microdialysis. Brain Res. 1999; 833(2):150-60. DOI: 10.1016/s0006-8993(99)01538-3. View