Differential Effects of Chronic Ethanol Use on Mouse Neuronal and Astroglial Metabolic Activity.
13C NMR spectroscopy
Alcohol abuse
Astrocytes
Brain metabolism
GABA
Glutamate
Monocarboxylic acid transporters
Neurons
Journal
Neurochemical research
ISSN: 1573-6903
Titre abrégé: Neurochem Res
Pays: United States
ID NLM: 7613461
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
received:
29
11
2022
accepted:
24
03
2023
revised:
20
03
2023
medline:
15
6
2023
pubmed:
18
4
2023
entrez:
17
4
2023
Statut:
ppublish
Résumé
Chronic alcohol use disorder, a major risk factor for the development of neuropsychiatric disorders including addiction to other substances, is associated with several neuropathology including perturbed neuronal and glial activities in the brain. It affects carbon metabolism in specific brain regions, and perturbs neuro-metabolite homeostasis in neuronal and glial cells. Alcohol induced changes in the brain neurochemical profile accompany the negative emotional state associated with dysregulated reward and sensitized stress response to withdrawal. However, the underlying alterations in neuro-astroglial activities and neurochemical dysregulations in brain regions after chronic alcohol use are poorly understood. This study evaluates the impact of chronic ethanol use on the regional neuro-astroglial metabolic activity using
Identifiants
pubmed: 37069415
doi: 10.1007/s11064-023-03922-y
pii: 10.1007/s11064-023-03922-y
doi:
Substances chimiques
Acetates
0
Ethanol
3K9958V90M
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2580-2594Subventions
Organisme : Department of Biotechnology, Ministry of Science and Technology, India
ID : BT/PR27426/MED/122/140/2018
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Nutt DJ, King LA, Phillips LD (2010) Drug harms in the UK: a multicriteria decision analysis. The Lancet 376:1558–1565
Koob GF (2015) The dark side of emotion: the addiction perspective. Eur J Pharmacol 753:73–87
pubmed: 25583178
pmcid: 4380644
Koob GF (2017) The Dark Side of Addiction: The Horsley Gantt to Joseph Brady Connection. J Nerv Ment Dis 205:270–272
pubmed: 27356121
pmcid: 6135258
Wise RA, Koob GF (2014) The development and maintenance of drug addiction. Neuropsychopharmacology 39:254–262
pubmed: 24121188
Fama R, Le Berre AP, Hardcastle C, Sassoon SA, Pfefferbaum A, Sullivan EV, Zahr NM (2019) Neurological, nutritional and alcohol consumption factors underlie cognitive and motor deficits in chronic alcoholism. Addict Biol 24:290–302
pubmed: 29243370
Bruijnen CJ, Dijkstra BA, Walvoort SJ, Markus W, VanDerNagel JE, Kessels RP, De Jong CA (2019) Prevalence of cognitive impairment in patients with substance use disorder. Drug Alcohol Rev 38:435–442
pubmed: 30916448
pmcid: 6593747
Le Berre AP, Fama R, Sullivan EV (2017) Executive functions, memory, and social cognitive deficits and recovery in chronic alcoholism: a critical review to inform future research. Alcohol Clin Exp Res 41:1432–1443
pubmed: 28618018
pmcid: 5531758
White AM, Matthews DB, Best PJ (2000) Ethanol, memory, and hippocampal function: a review of recent findings. Hippocampus 10:88–93
pubmed: 10706220
Gilpin NW, Herman MA, Roberto M (2015) The central amygdala as an integrative hub for anxiety and alcohol use disorders. Biol Psychiatry 77:859–869
pubmed: 25433901
Koob GF, Buck CL, Cohen A, Edwards S, Park PE, Schlosburg JE, Schmeichel B, Vendruscolo LF, Wade CL, Whitfield TW Jr (2014) Addiction as a stress surfeit disorder. Neuropharmacology 76:370–382
pubmed: 23747571
Wang J, Du H, Jiang L, Ma X, de Graaf RA, Behar KL, Mason GF (2013) Oxidation of ethanol in the rat brain and effects associated with chronic ethanol exposure. Proc Natl Acad Sci U S A 110:14444–14449
pubmed: 23940368
pmcid: 3761635
Yang W, Singla R, Maheshwari O, Fontaine CJ, Gil-Mohapel J (2022) Alcohol use disorder: neurobiology and therapeutics. Biomedicines 10:1192
pubmed: 35625928
pmcid: 9139063
Chastain G (2006) Alcohol, neurotransmitter systems, and behavior. J Gen Psychol 133:329–335
pubmed: 17128954
Valenzuela CF (1997) Alcohol and neurotransmitter interactions. Alcohol Health Res World 21:144
pubmed: 15704351
pmcid: 6826822
Jagannathan NR, Desai NG, Raghunathan P (1996) Brain metabolite changes in alcoholism: an in vivo proton magnetic resonance spectroscopy (MRS) study. Magn Reson Imaging 14:553–557
pubmed: 8843367
Enculescu C, Kerr ED, Yeo KYB, Schenk G, Fortes MRS, Schulz BL (2019) Proteomics reveals profound metabolic changes in the alcohol use disorder brain. ACS Chem Neurosci 10:2364–2373
pubmed: 30807102
Tiwari V, Veeraiah P, Subramaniam V, Patel AB (2014) Differential effects of ethanol on regional glutamatergic and GABAergic neurotransmitter pathways in mouse brain. J Neurochem 128:628–640
pubmed: 24164397
Hyder F, Patel AB, Gjedde A, Rothman DL, Behar KL, Shulman RG (2006) Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J Cereb Blood Flow Metab 26:865–877
pubmed: 16407855
Patel AB, de Graaf RA, Mason GF, Kanamatsu T, Rothman DL, Shulman RG, Behar KL (2004) Glutamatergic neurotransmission and neuronal glucose oxidation are coupled during intense neuronal activation. J Cereb Blood Flow Metab 24:972–985
pubmed: 15356418
Gruetter R, Seaquist ER, Ugurbil K (2001) A mathematical model of compartmentalized neurotransmitter metabolism in the human brain. Am J Physiol Endocrinol Metab 281:E100-112
pubmed: 11404227
Lebon V, Petersen KF, Cline GW, Shen J, Mason GF, Dufour S, Behar KL, Shulman GI, Rothman DL (2002) Astroglial contribution to brain energy metabolism in humans revealed by
pubmed: 11880482
pmcid: 2995528
Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1:848–858
pubmed: 17406317
pmcid: 2895266
Karisetty BC, Maitra S, Wahul AB, Musalamadugu A, Khandelwal N, Guntupalli S, Garikapati R, Jhansyrani T, Kumar A, Chakravarty S (2017) Differential effect of chronic stress on mouse hippocampal memory and affective behavior: Role of major ovarian hormones. Behav Brain Res 318:36–44
pubmed: 27780721
Khandelwal N, Dey SK, Chakravarty S, Kumar A (2019) miR-30 family miRNAs mediate the effect of chronic social defeat stress on hippocampal neurogenesis in mouse depression model. Front Mol Neurosci 12:188
pubmed: 31440139
pmcid: 6694739
Amalakanti S, Bhat UA, Mylavarapu MB, Khandelwal N, Sundarachary NV, Chakravarty S, Kumar A (2021) Gene expression analysis identifies cholesterol metabolism dysregulation in hippocampus of phenytoin-resistant pentylenetetrazol-kindled epileptic mice. Neuromolecular Med 23:485–490
pubmed: 33604751
Duarte JM, Gruetter R (2013) Glutamatergic and GABAergic energy metabolism measured in the rat brain by (13) C NMR spectroscopy at 14.1 T. J Neurochem 126:579–590
pubmed: 23745684
Lanz B, Xin L, Millet P, Gruetter R (2014) In vivo quantification of neuro-glial metabolism and glial glutamate concentration using 1H-[13C] MRS at 14.1T. J Neurochem 128:125–139
pubmed: 24117599
Mishra PK, Kumar A, Behar KL, Patel AB (2018) Subanesthetic ketamine reverses neuronal and astroglial metabolic activity deficits in a social defeat model of depression. J Neurochem 146:722–734
pubmed: 29964293
Tiwari V, Ambadipudi S, Patel AB (2013) Glutamatergic and GABAergic TCA cycle and neurotransmitter cycling fluxes in different regions of mouse brain. J Cereb Blood Flow Metab 33:1523–1531
pubmed: 23838829
pmcid: 3790929
Soni ND, Ramesh A, Roy D, Patel AB (2021) Brain energy metabolism in intracerebroventricularly administered streptozotocin mouse model of Alzheimer’s disease: A
pubmed: 33657898
pmcid: 8393290
Patel AB, Rothman DL, Cline GW, Behar KL (2001) Glutamine is the major precursor for GABA synthesis in rat neocortex in vivo following acute GABA-transaminase inhibition. Brain Res 919:207–220
pubmed: 11701133
Bagga P, Chugani AN, Varadarajan KS, Patel AB (2013) In vivo NMR studies of regional cerebral energetics in MPTP model of Parkinson’s disease: recovery of cerebral metabolism with acute levodopa treatment. J Neurochem 127:365–377
pubmed: 23957451
de Graaf RA, Brown PB, Mason GF, Rothman DL, Behar KL (2003) Detection of [1,6–
pubmed: 12509818
Patel AB, de Graaf RA, Mason GF, Rothman DL, Shulman RG, Behar KL (2005) The contribution of GABA to glutamate/glutamine cycling and energy metabolism in the rat cortex in vivo. Proc Natl Acad Sci U S A 102:5588–5593
pubmed: 15809416
pmcid: 556230
Rae C, Fekete AD, Kashem MA, Nasrallah FA, Bröer S (2012) Metabolism, compartmentation, transport and production of acetate in the cortical brain tissue slice. Neurochem Res 37:2541–2553
pubmed: 22851350
Patel AB, de Graaf RA, Rothman DL, Behar KL, Mason GF (2010) Evaluation of cerebral acetate transport and metabolic rates in the rat brain in vivo using
pubmed: 20125180
pmcid: 2879471
Waniewski RA, Martin DL (1998) Preferential utilization of acetate by astrocytes is attributable to transport. J Neurosci 18:5225–5233
pubmed: 9651205
pmcid: 6793490
Xin L, Mlynarik V, Lanz B, Frenkel H, Gruetter R (2010) 1H-[13C] NMR spectroscopy of the rat brain during infusion of [2-13C] acetate at 14.1 T. Magn Reson Med 64:334–340
pubmed: 20535808
Bendszus M, Weijers HG, Wiesbeck G, Warmuth-Metz M, Bartsch AJ, Engels S, Boning J, Solymosi L (2001) Sequential MR imaging and proton MR spectroscopy in patients who underwent recent detoxification for chronic alcoholism: correlation with clinical and neuropsychological data. AJNR Am J Neuroradiol 22:1926–1932
pubmed: 11733327
pmcid: 7973857
Zahr NM, Carr RA, Rohlfing T, Mayer D, Sullivan EV, Colrain IM, Pfefferbaum A (2016) Brain metabolite levels in recently sober individuals with alcohol use disorder: Relation to drinking variables and relapse. Psychiat Res Neuroim 250:42–49
Lee DW, Kim SY, Lee T, Nam YK, Ju A, Woo DC, You SJ, Han JS, Lee SH, Choi CB, Kim SS, Shin HC, Kim HY, Kim DJ, Rhim HS, Choe BY (2012) Ex vivo detection for chronic ethanol consumption-induced neurochemical changes in rats. Brain Res 1429:134–144
pubmed: 22079322
Durazzo TC, Gazdzinski S, Rothlind JC, Banys P, Meyerhoff DJ (2006) Brain metabolite concentrations and neurocognition during short-term recovery from alcohol dependence: preliminary evidence of the effects of concurrent chronic cigarette smoking. Alcohol Clin Exp Res 30:539–551
pubmed: 16499496
Mason GF, Petrakis IL, de Graaf RA, Gueorguieva R, Guidone E, Coric V, Epperson CN, Rothman DL, Krystal JH (2006) Cortical gamma-aminobutyric acid levels and the recovery from ethanol dependence: preliminary evidence of modification by cigarette smoking. Biol Psychiatry 59:85–93
pubmed: 16289397
Thoma R, Mullins P, Ruhl D, Monnig M, Yeo RA, Caprihan A, Bogenschutz M, Lysne P, Tonigan S, Kalyanam R, Gasparovic C (2011) Perturbation of the glutamate-glutamine system in alcohol dependence and remission. Neuropsychopharmacology 36:1359–1365
pubmed: 21389979
pmcid: 3096805
Prisciandaro JJ, Schacht JP, Prescot AP, Renshaw PF, Brown TR, Anton RF (2016) Associations between recent heavy drinking and dorsal anterior cingulate N-acetylaspartate and glutamate concentrations in non-treatment-seeking individuals with alcohol dependence. Alcohol Clin Exp Res 40:491–496
pubmed: 26853538
pmcid: 4775399
Howarth C, Gleeson P, Attwell D (2012) Updated energy budgets for neural computation in the neocortex and cerebellum. J Cereb Blood Flow Metab 32:1222–1232
pubmed: 22434069
pmcid: 3390818
Angelova PR, Abramov AY (2018) Role of mitochondrial ROS in the brain: from physiology to neurodegeneration. FEBS Lett 592:692–702
pubmed: 29292494
Jung ME, Metzger DB (2010) Alcohol withdrawal and brain injuries: beyond classical mechanisms. Molecules 15:4984–5011
pubmed: 20657404
pmcid: 6257660
Gardner S, Sohrabi S, Shen K, Rainey-Smith S, Weinborn M, Bates K, Shah T, Foster J, Lenzo N, Salvado O (2016) Cerebral glucose metabolism is associated with verbal not visual performance in community-dwelling older adults. J Alzheimers Dis 10:x–x
Mosconi L, De Santi S, Li J, Tsui WH, Li Y, Boppana M, Laska E, Rusinek H, de Leon MJ (2008) Hippocampal hypometabolism predicts cognitive decline from normal aging. Neurobiol Aging 29:676–692
pubmed: 17222480
Mosconi L, Tsui W-H, De Santi S, Li J, Rusinek H, Convit A, Li Y, Boppana M, De Leon M (2005) Reduced hippocampal metabolism in MCI and AD: automated FDG-PET image analysis. Neurology 64:1860–1867
pubmed: 15955934
Patel AB, Tiwari V, Veeraiah P, Saba K (2018) Increased astroglial activity and reduced neuronal function across brain in AβPP-PS1 mouse model of Alzheimer’s disease. J Cereb Blood Flow Metab 38:1213–1226
pubmed: 28585882
Tiwari V, Patel AB (2012) Impaired glutamatergic and GABAergic function at early age in APPswe-PS1dE9 mice: implications for preclinical diagnosis of Alzheimer’s disease 1. J Alzheimers Dis 20(10):3233
Schallier A, Smolders I, Van Dam D, Loyens E, De Deyn PP, Michotte A, Michotte Y, Massie A (2011) Region- and age-specific changes in glutamate transport in the AbetaPP23 mouse model for Alzheimer’s disease. J Alzheimers Dis 24:287–300
pubmed: 21297271
Chen KH, Reese EA, Kim HW, Rapoport SI, Rao JS (2011) Disturbed neurotransmitter transporter expression in Alzheimer’s disease brain. J Alzheimers Dis 26:755–766
pubmed: 21743130
pmcid: 3188700
Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG (1998) Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci U S A 95:316–321
pubmed: 9419373
pmcid: 18211
Jiang L, Gulanski BI, De Feyter HM, Weinzimer SA, Pittman B, Guidone E, Koretski J, Harman S, Petrakis IL, Krystal JH, Mason GF (2013) Increased brain uptake and oxidation of acetate in heavy drinkers. J Clin Invest 123:1605–1614
pubmed: 23478412
pmcid: 3613911
Pierre K, Pellerin L (2005) Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J Neurochem 94:1–14
pubmed: 15953344
Pellerin L, Halestrap AP, Pierre K (2005) Cellular and subcellular distribution of monocarboxylate transporters in cultured brain cells and in the adult brain. J Neurosci Res 79:55–64
pubmed: 15573400
Bergersen LH, Magistretti PJ, Pellerin L (2005) Selective postsynaptic co-localization of MCT2 with AMPA receptor GluR2/3 subunits at excitatory synapses exhibiting AMPA receptor trafficking. Cereb Cortex 15:361–370
pubmed: 15749979
Pierre K, Magistretti PJ, Pellerin L (2002) MCT2 is a major neuronal monocarboxylate transporter in the adult mouse brain. J Cereb Blood Flow Metab 22:586–595
pubmed: 11973431
Flores-Bastias O, Karahanian E (2018) Neuroinflammation produced by heavy alcohol intake is due to loops of interactions between Toll-like 4 and TNF receptors, peroxisome proliferator-activated receptors and the central melanocortin system: a novel hypothesis and new therapeutic avenues. Neuropharmacology 128:401–407
pubmed: 29113896
Nam M-H, Ko HY, Lee S, Park YM, Hyeon SJ, Won W, Kim SY, Jo HH, Chung J-I, Han Y-E; Lee G-H, Ju Y, Stein TD, Kong M, Lee L, Lee SE, Oh S-J, Chun J-H, Park KD, Ryu H, Yun M, Lee CJ (2021) Visualization of reactive astrocytes in living brain of Alzheimer’s disease patient. https://doi.org/10.1101/2021.04.13.439744
Jurga AM, Paleczna M, Kadluczka J, Kuter KZ (2021) Beyond the GFAP-astrocyte protein markers in the brain. Biomolecules 11:1361
pubmed: 34572572
pmcid: 8468264
Li T, Chen X, Zhang C, Zhang Y, Yao W (2019) An update on reactive astrocytes in chronic pain. J Neuroinflammation 16:1–13
Li K, Li J, Zheng J, Qin S (2019) Reactive astrocytes in neurodegenerative diseases. Aging Dis 10:664
pubmed: 31165009
pmcid: 6538217
Fowler A-K, Thompson J, Chen L, Dagda M, Dertien J, Dossou KSS, Moaddel R, Bergeson SE, Kruman II (2014) Differential sensitivity of prefrontal cortex and hippocampus to alcohol-induced toxicity. PLoS ONE 9:e106945
pubmed: 25188266
pmcid: 4154772
de Graaf RA, Mason GF, Patel AB, Rothman DL, Behar KL (2004) Regional glucose metabolism and glutamatergic neurotransmission in rat brain in vivo. Proc Natl Acad Sci U S A 101:12700–12705
pubmed: 15310848
pmcid: 515118
Lai M, Gruetter R, Lanz B (2017) Progress towards in vivo brain
pubmed: 28119064
McNair LM, Mason GF, Chowdhury GM, Jiang L, Ma X, Rothman DL, Waagepetersen HS, Behar KL (2022) Rates of pyruvate carboxylase, glutamate and GABA neurotransmitter cycling, and glucose oxidation in multiple brain regions of the awake rat using a combination of [2-
pubmed: 35048735
pmcid: 9274856
Sonnay S, Poirot J, Just N, Clerc AC, Gruetter R, Rainer G, Duarte JMN (2018) Astrocytic and neuronal oxidative metabolism are coupled to the rate of glutamate-glutamine cycle in the tree shrew visual cortex. Glia 66:477–491
pubmed: 29120073
Jensen NJ, Wodschow HZ, Nilsson M, Rungby J (2020) Effects of ketone bodies on brain metabolism and function in neurodegenerative diseases. Int J Mol Sci 21(22):8767
Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill GF Jr (1967) Brain metabolism during fasting. J Clin Invest 46:1589–1595
pubmed: 6061736
pmcid: 292907
Yudkoff M, Daikhin Y, Lin ZP, Nissim I, Stern J, Pleasure D, Nissim I (1994) Interrelationships of leucine and glutamate metabolism in cultured astrocytes. J Neurochem 62:1192–1202
pubmed: 7906717
Bagga P, Behar KL, Mason GF, De Feyter HM, Rothman DL, Patel AB (2014) Characterization of cerebral glutamine uptake from blood in the mouse brain: implications for metabolic modeling of
pubmed: 25074745
pmcid: 4269725