Glutamatergic and gabaergic metabolism in mouse brain under chronic nicotine exposure: Implications for addiction

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Shameem, Mohammad ^a,b   Patel, Anant Bahadur ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ACETIC ACID; AMINO ACID; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; NICOTINE;

AMINO ACID BRAIN LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN METABOLISM; BRAIN NERVE CELL; BRAIN TISSUE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL ACTIVITY; CELL FUNCTION; CEREBELLUM; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; GLUCOSE OXIDATION; INHIBITORY POSTSYNAPTIC POTENTIAL; ISOTOPE LABELING; LONG TERM EXPOSURE; MALE; METABOLIC PARAMETERS; MOUSE; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NEUROTRANSMISSION; NONHUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; SMOKING; SUBCORTEX; TOBACCO DEPENDENCE;

ACETATES; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; GAMMA-AMINOBUTYRIC ACID; GLUCOSE; GLUTAMIC ACID; MALE; MICE; MICE, INBRED C57BL; NICOTINE; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION; SUBSTANCE-RELATED DISORDERS;

MUS;

EID: 84864367031     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041824     Document Type: Article

References (63)

1. Benowitz NL, (2009) Pharmacology of nicotine: addiction, smoking-induced disease, and therapeutics. Annu Rev Pharmacol Toxicol 49: 57-71.
2. Paterson NE, Semenova S, Gasparini F, Markou A, (2003) The mGluR5 antagonist MPEP decreased nicotine self-administration in rats and mice. Psychopharmacology (Berl) 167: 257-264.
3. Kalivas PW, Volkow ND, (2005) The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162: 1403-1413.
4. Benowitz NL, (1996) Pharmacology of nicotine: addiction and therapeutics. Annu Rev Pharmacol Toxicol 36: 597-613.
5. MacDermott AB, Role LW, Siegelbaum SA, (1999) Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 22: 443-485.
6. Mansvelder HD, Keath JR, McGehee DS, (2002) Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33: 905-919.
7. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW, (1995) Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269: 1692-1696.
8. Hyder F, Patel AB, Gjedde A, Rothman DL, Behar KL, et al. (2006) Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J Cereb Blood Flow Metab 26: 865-877.
9. Ottersen OP, Storm-Mathisen J, (1986) Excitatory amino acid pathways in the brain. Adv Exp Med Biol 203: 263-284.
10. Schmidt WJ, Bubser M, Hauber W, (1992) Behavioural pharmacology of glutamate in the basal ganglia. J Neural Transm pp. 65-89.
11. Shulman RG, Rothman DL, Behar KL, Hyder F, (2004) Energetic basis of brain activity: implications for neuroimaging. Trends Neurosci 27: 489-495.
12. Sibson NR, Dhankhar A, Mason GF, Behar KL, Rothman DL, et al. (1997) In vivo 13C NMR measurements of cerebral glutamine synthesis as evidence for glutamate-glutamine cycling. Proc Natl Acad Sci U S A 94: 2699-2704.
13. de Graaf RA, Brown PB, Mason GF, Rothman DL, Behar KL, (2003) Detection of [1,6-13C2]-glucose metabolism in rat brain by in vivo 1H-[13C]-NMR spectroscopy. Magn Reson Med 49: 37-46.
14. 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.
15. Patel AB, de Graaf RA, Mason GF, Rothman DL, Shulman RG, et al. (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.
16. Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, et al. (1998) Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci U S A 95: 316-321.
17. Patel AB, de Graaf RA, Mason GF, Kanamatsu T, Rothman DL, et al. (2004) Glutamatergic neurotransmission and neuronal glucose oxidation are coupled during intense neuronal activation. J Cereb Blood Flow Metab 24: 972-985.
18. Greenamyre JT, Maragos WF, (1993) Neurotransmitter receptors in Alzheimer disease. Cerebrovasc Brain Metab Rev 5: 61-94.
19. Heath PR, Shaw PJ, (2002) Update on the glutamatergic neurotransmitter system and the role of excitotoxicity in amyotrophic lateral sclerosis. Muscle Nerve 26: 438-458.
20. Pearl PL, Gibson KM, (2004) Clinical aspects of the disorders of GABA metabolism in children. Curr Opin Neurol 17: 107-113.
21. Sanacora G, Rothman DL, Mason G, Krystal JH, (2003) Clinical studies implementing glutamate neurotransmission in mood disorders. Ann N Y Acad Sci 1003: 292-308.
22. Domino EF, Minoshima S, Guthrie SK, Ohl L, Ni L, et al. (2000) Effects of nicotine on regional cerebral glucose metabolism in awake resting tobacco smokers. Neuroscience 101: 277-282.
23. Domino EF, Minoshima S, Guthrie S, Ohl L, Ni L, et al. (2000) Nicotine effects on regional cerebral blood flow in awake, resting tobacco smokers. Synapse 38: 313-321.
24. Marenco T, Bernstein S, Cumming P, Clarke PB, (2000) Effects of nicotine and chlorisondamine on cerebral glucose utilization in immobilized and freely-moving rats. Br J Pharmacol 129: 147-155.
25. Hyder F, Kennan RP, Kida I, Mason GF, Behar KL, et al. (2000) Dependence of oxygen delivery on blood flow in rat brain: a 7 tesla nuclear magnetic resonance study. J Cereb Blood Flow Metab 20: 485-498.
26. Turegano L, Martinez-Rodriguez R, Alvarez MI, Gragera RR, Gomez de Segura A, et al. (2001) Histochemical study of acute and chronic intraperitoneal nicotine effects on several glycolytic and Krebs cycle dehydrogenase activities in the frontoparietal cortex and subcortical nuclei of the rat brain. J Neurosci Res 64: 626-635.
27. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW, (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89: 73-120.
28. Fagen ZM, Mansvelder HD, Keath JR, McGehee DS, (2003) Short- and long-term modulation of synaptic inputs to brain reward areas by nicotine. Ann N Y Acad Sci 1003: 185-195.
29. Zhang TA, Tang J, Pidoplichko VI, Dani JA, (2010) Addictive nicotine alters local circuit inhibition during the induction of in vivo hippocampal synaptic potentiation. J Neurosci 30: 6443-6453.
30. Mansvelder HD, McGehee DS, (2000) Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27: 349-357.
31. Patel AB, Shameem M, (2010) NMR investigations of neuronal and astroglial metabolism in nicotine addiction. Proc Intl Soc Magn Reson Med 18: 3356.
32. Grabus SD, Martin BR, Batman AM, Tyndale RF, Sellers E, et al. (2005) Nicotine physical dependence and tolerance in the mouse following chronic oral administration. Psychopharmacology (Berl) 178: 183-192.
33. Jackson KJ, Walters CL, Miles MF, Martin BR, Damaj MI, (2009) Characterization of pharmacological and behavioral differences to nicotine in C57Bl/6 and DBA/2 mice. Neuropharmacology 57: 347-355.
34. London ED, Connolly RJ, Szikszay M, Wamsley JK, Dam M, (1988) Effects of nicotine on local cerebral glucose utilization in the rat. J Neurosci 8: 3920-3928.
35. Marks MJ, Meinerz NM, Brown RW, Collins AC, (2010) 86Rb+ efflux mediated by alpha4beta2*-nicotinic acetylcholine receptors with high and low-sensitivity to stimulation by acetylcholine display similar agonist-induced desensitization. Biochem Pharmacol 80: 1238-1251.
36. Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, et al. (2007) Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190: 269-319.
37. Bagga P, Patel AB, (2012) Regional cerebral metabolism in mouse under chronic manganese exposure: Implications for Manganism. Neurochem Int 60: 177-185.
38. Fitzpatrick SM, Hetherington HP, Behar KL, Shulman RG, (1990) The flux from glucose to glutamate in the rat brain in vivo as determined by 1H-observed, 13C-edited NMR spectroscopy. J Cereb Blood Flow Metab 10: 170-179.
39. Tiwari V, Patel AB, (2012) Impaired Glutamatergic and GABAergic Function at Early Age in AbetaPPswe-PS1dE9 Mice: Implications for Alzheimer's Disease. J Alzheimers Dis 28: 765-769.
40. 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.
41. Waniewski RA, Martin DL, (1998) Preferential utilization of acetate by astrocytes is attributable to transport. J Neurosci 18: 5225-5233.
42. Zwingmann C, Leibfritz D, Hazell AS, (2003) Energy metabolism in astrocytes and neurons treated with manganese: relation among cell-specific energy failure, glucose metabolism, and intercellular trafficking using multinuclear NMR-spectroscopic analysis. J Cereb Blood Flow Metab 23: 756-771.
43. Badar-Goffer RS, Bachelard HS, Morris PG, (1990) Cerebral metabolism of acetate and glucose studied by 13C NMR spectroscopy. A technique for investigating metabolic compartmentation in the brain. Biochem J 266: 133-139.
44. Zubieta J, Lombardi U, Minoshima S, Guthrie S, Ni L, et al. (2001) Regional cerebral blood flow effects of nicotine in overnight abstinent smokers. Biol Psychiatry 49: 906-913.
45. Wang J, Jiang L, Jiang Y, Ma X, Chowdhury GM, et al. (2010) Regional metabolite levels and turnover in the awake rat brain under the influence of nicotine. J Neurochem 113: 1447-1458.
46. Mao D, McGehee DS, (2010) Nicotine and behavioral sensitization. J Mol Neurosci 40: 154-163.
47. Gruetter R, Novotny EJ, Boulware SD, Mason GF, Rothman DL, et al. (1994) Localized 13C NMR spectroscopy in the human brain of amino acid labeling from D-[1-13C]glucose. J Neurochem 63: 1377-1385.
48. 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 1H-[13C]-NMR. J Cereb Blood Flow Metab 30: 1200-1213.
49. 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.
50. Lebon V, Petersen KF, Cline GW, Shen J, Mason GF, et al. (2002) Astroglial contribution to brain energy metabolism in humans revealed by 13C nuclear magnetic resonance spectroscopy: elucidation of the dominant pathway for neurotransmitter glutamate repletion and measurement of astrocytic oxidative metabolism. J Neurosci 22: 1523-1531.
51. Shen J, Petersen KF, Behar KL, Brown P, Nixon TW, et al. (1999) Determination of the rate of the glutamate/glutamine cycle in the human brain by in vivo 13C NMR. Proc Natl Acad Sci U S A 96: 8235-8240.
52. Ortells MO, Barrantes GE, (2010) Tobacco addiction: a biochemical model of nicotine dependence. Med Hypotheses 74: 884-894.
53. Kuryatov A, Luo J, Cooper J, Lindstrom J, (2005) Nicotine acts as a pharmacological chaperone to up-regulate human alpha4beta2 acetylcholine receptors. Mol Pharmacol 68: 1839-1851.
54. Sallette J, Pons S, Devillers-Thiery A, Soudant M, Prado de Carvalho L, et al. (2005) Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 46: 595-607.
55. Giniatullin R, Nistri A, Yakel JL, (2005) Desensitization of nicotinic ACh receptors: shaping cholinergic signaling. Trends Neurosci 28: 371-378.
56. Laviolette SR, van der Kooy D, (2004) The neurobiology of nicotine addiction: bridging the gap from molecules to behaviour. Nat Rev Neurosci 5: 55-65.
57. Rahman S, Zhang J, Engleman EA, Corrigall WA, (2004) Neuroadaptive changes in the mesoaccumbens dopamine system after chronic nicotine self-administration: a microdialysis study. Neuroscience 129: 415-424.
58. Nisell M, Nomikos GG, Svensson TH, (1994) Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 16: 36-44.
59. Marchi M, Risso F, Viola C, Cavazzani P, Raiteri M, (2002) Direct evidence that release-stimulating alpha7* nicotinic cholinergic receptors are localized on human and rat brain glutamatergic axon terminals. J Neurochem 80: 1071-1078.
60. Schilstrom B, Fagerquist MV, Zhang X, Hertel P, Panagis G, et al. (2000) Putative role of presynaptic alpha7* nicotinic receptors in nicotine stimulated increases of extracellular levels of glutamate and aspartate in the ventral tegmental area. Synapse 38: 375-383.
61. Sharma G, Grybko M, Vijayaraghavan S, (2008) Action potential-independent and nicotinic receptor-mediated concerted release of multiple quanta at hippocampal CA3-mossy fiber synapses. J Neurosci 28: 2563-2575.
62. Chowdhury GM, Behar KL, Cho W, Thomas MA, Rothman DL, et al. (2012) (1)H-[(13)C]-Nuclear Magnetic Resonance Spectroscopy Measures of Ketamine's Effect on Amino Acid Neurotransmitter Metabolism. Biol Psychiatry 71: 1022-1025.
63. Meisingset TW, Risa O, Brenner M, Messing A, Sonnewald U, (2010) Alteration of glial-neuronal metabolic interactions in a mouse model of Alexander disease. Glia 58: 1228-1234.