Cocaine causes memory and learning impairments in rats: Involvement of nuclear factor kappa B and oxidative stress, and prevention by topiramate

Journal of Neurochemistry

Volumn 114, Issue 3, 2010, Pages 675-684

  Muriach, María ^a   López Pedrajas, Rosa ^a   Barcia, Jorge M ^a   Sanchez Villarejo, María V ^a   Almansa, Inmaculada ^a   Romero, Francisco J ^a  

^a UNIVERSIDAD CEU CARDENAL HERRERA   (Spain)

Author keywords

cocaine; learning and memory; nuclear factor kappa B; oxidative stress; rat; topiramate

Indexed keywords

CASPASE 3; COCAINE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; TOPIRAMATE; DOPAMINE UPTAKE INHIBITOR; FRUCTOSE; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; FRONTAL CORTEX; HISTOCHEMISTRY; LEARNING; MALE; MAZE TEST; MEMORY; NEUROPROTECTION; NICK END LABELING; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; ANALOGS AND DERIVATIVES; ANIMAL; CHEMICALLY INDUCED; COCAINE DEPENDENCE; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; FRONTAL LOBE; LEARNING DISORDERS; MEMORY DISORDERS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TOXICITY; WISTAR RAT;

RATTUS;

ANIMALS; COCAINE; COCAINE-RELATED DISORDERS; DISEASE MODELS, ANIMAL; DOPAMINE UPTAKE INHIBITORS; FRONTAL LOBE; FRUCTOSE; LEARNING DISORDERS; MALE; MEMORY DISORDERS; NEUROPROTECTIVE AGENTS; NF-KAPPA B; OXIDATIVE STRESS; RATS; RATS, WISTAR;

EID: 77954338704     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06794.x     Document Type: Article

References (59)

1. Bashkatova V., Meunier J., Vanin A. Maurice T. (2006) Nitric oxide and oxidative stress in the brain of rats exposed in utero to cocaine. Ann. N Y Acad. Sci. 1074, 632 642.
2. Calcagnetti D. J., Keck B. J., Quatrella L. A. Schechter M. D. (1995) Blockade of cocaine-induced conditioned place preference: relevance to cocaine abuse therapeutics. Br. J. Pharmacol. 144, 926 932.
3. Collins S. L. Kantak K. M. (2002) Neuronal nitric oxide synthase inhibition decreases cocaine self-administration behavior in rats. Psychopharmacology (Berl.) 159, 361 369.
4. Collinson N., Kuenzi F. M., Jarolimek W., et al 2002) Enhanced learning and memory and altered GABAergic synaptic transmission in mice lacking the alpha 5 subunit of the GABAA receptor. J. Neurosci. 22, 5572 5580.
5. Dawson T. M., Bredt D. S., Fotuhi M., Hwang P. M. Snyder S. H. (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl Acad. Sci. USA 88, 7797 7801.
6. Dietrich J. B., Mangeol A., Revel M. O., Burgun C., Aunis D. Zwiller J. (2005) Acute or repeated cocaine adminsitration generates reactive oxygen species and induces antioxidant enzime activity in dopaminergic rat brain structures. Neuropharmacology 48, 965 974.
7. Farook J. M., Morrell D. J., Lewis B., Littleton J. M. Barron S. (2007) Topiramate (Topamax) reduces conditioned abstinence behaviours and handling-induced convulsions (HIC) after chronic administration of alcohol in Swiss-Webster mice. Alcohol Alcohol. 42, 296 300.
8. Gasior M., Kaminski R. Witkin J. M. (2004) Pharmacological modulation of GABA(B) receptor affects cocaine-induced seizures in mice. Psychopharmacology (Berl.) 174, 211 219.
9. Gass J. T. Olive M. F. (2008) Glutamatergic substrates of drug addiction and alcoholism. Biochem. Pharmacol. 75, 218 265.
10. Gordey M., DeLorey T. M. Olsen R. W. (2000) Differential sensitivity of recombinant GABA(A) receptors expressed in Xenopus oocytes to modulation by topiramate. Epilepsia 41, S25 S29.
11. Gramsbergen J. B., Sandberg M., Møller-Dall A., Kornblit B. Zimmer J. (2002) Glutathione depletion in nigrostriatal slice cultures: GABA loss, dopamine resistance and protection by the tetrahydrobiopterin precursor sepiapterin. Brain Res. 935, 47 58.
12. Hastings T. G. (1995) Enzymatic oxidation of dopamine: the role of prostaglandin H synthase. J. Neurochem. 64, 919 924.
13. Herrera D. G., Yague A. G., Johnsen-Soriano S., Bosch-Morell F., Collado-Morente L., Muriach M., Romero F. J. García-Verdugo J. M. (2003) Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc. Natl Acad. Sci. USA 100, 7919 7924.
14. Hnasko T. S., Sotak N. B. Palmiter R. D. (2007) Cocaine-conditioned place preference by dopamine-deficient mice is mediated by serotonin. J. Neurosci. 27, 12484 12488.
15. Hope B. T., Michael G. J., Nigge K. M. Vincent S. R. (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl Acad. Sci. USA 88, 2811 2814.
16. Huang C. C., Lin H. J. Hsu K. S. (2007) Repeated cocaine administration prometes long-term potentiation induction in rat medial prefrontal cortex. Cereb. Cortex 17, 1877 1888.
17. Ishikawa M., Mu P., Moyer J. T., Wolf J. A., Quock R. M., Davies N. M., Hu X. T., Schlüter O. M. Dong Y. (2009) Homeostatic synapse-driven membrane plasticity in nucleus accumbens neurons. J. Neurosci. 29, 5820 5831.
18. Itzhak Y. Anderson K. L. (2007) Memory reconsolidation of cocaine-associated context requires nitric oxide signaling. Synapse 61, 1002 1005.
19. Itzhak Y., Ali S. F., Martin J. L., Black M. D. Huang P. L. (1998) Resistance of neuronal nitric oxide synthase-deficient mice to cocaine-induced locomotor sensitization. Psychopharmacology (Berl.) 140, 378 386. (Pubitemid 28562458)
20. Kaltschmidt C., Kaltschmidt B. Baeuerle P. A. (1995) Stimulation of ionotropic glutamate receptors activates transcription NF-Kappa B in primary neurons. Proc. Natl Acad. Sci. USA 92, 9618 9622.
21. Kampman K. M., Pettinati H., Lynch K. G., Dackis C., Sparkman T., Weigley C. O′Brien C. P. (2004) A pilot trial of topiramate for the treatment of cocaine dependence. Drug Alcohol Depend. 75, 233 240.
22. Kandel E. R. (2001) The molecular biology of memory storage: a dialog betwen genes and synapses. Biosci. Rep. 21, 565 611.
23. Kelleher R. J., Govidarajan A. Tonegawa S. (2004) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44, 59 73.
24. Kirchner L., Weitzdoerfer R., Hoeger H., Url A., Schmidt P., Engelmann M., Villar S. R., Fountoulakis M., Lubec G. Lubec B. (2004) Impaired cognitive performance in neuronal nitric oxide synthase knock-out mice is associated with hippocampal protein derangements. Nitric Oxide 11, 316 330.
25. Lawrence R. A., Parkhill L. K. Burk R. F. (1978) Hepatic cytosolic non-selenium dependent glutathione peroxidase activity: its nature and the effect of selenium deficiency. J. Nutr. 108, 981 987.
26. Lowry O. H., Rosebrough N. J., Farr A. L. Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265 275.
27. Lyng G. D. Seegal R. F. (2008) Polychlorinated biphenyl-induced oxidative stress in organotypic co-cultures: experimental dopamine depletion prevents reductions in GABA. Neurotoxicology 29, 301 308.
28. Macêdo D. S., deVasconcelos S. M., dosSantos R. S., Aguillar L. M., Lima V. T., Viana G. S. deSousa F. C. (2005) Cocaine alters catalase activity in prefrontal cortex and striatum of mice. Neurosci. Lett. 387, 53 56.
29. Marr D. (1971) Simple memory: a theory for archicortex. Phil. Trans. R Soc. Biol. Sci. 262, 23 81.
30. Mattson M. P. Camandola S. (2001) NF-kappaB in neuronal plasticity and neurodegenerative disorders. J. Clin. Invest. 107, 247 254.
31. McClelland J. L., McNaughton B. L. O′Reilly R. C. (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102, 419 457.
32. Meffert M. K., Chang J. M., Wiltgen B. J., Fanselow M. S. Baltimore D. (2003) NF-kappaB functions in synaptic signaling and behavior. Nat. Neurosci. 6, 1072 1078.
33. Merlo E., Freudenthal R., Maldonado H. Romano A. (2005) Activation of the transcription factor NF-kappaB by retrieval is required for long-term memory reconsolidation. Learn Mem. 12, 23 29. (Pubitemid 40205084)
34. Morris R. G., Garrud P., Rawlins J. N. O′Keefe J. (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297, 681 683.
35. 2+ATPase activity, and EEG records in pentylentetrazol-induced seizures in rats. J. Membr. Biol. 225, 39 49.
36. Numa R., Kohen R., Poltyrev T. Yaka R. (2008) Tempol diminishes cocaine-induced oxidative damage and attenuates the development and expression of behavioral sensitization. Neuroscience 155, 649 658.
37. O′Mahoney A., Raber J., Montano J. M., Foehr E., Ham V., Lu S. M., Kwon H., Lefevour A., Chakraborty-Sett S. Greene W. C. (2006) NF-kappa B/Rel regulated inhibitory and excitatory neuronal function and synaptic plasticity. Mol. Cell. Biol. 26, 7283 7298.
38. O′Neill L. A. Kaltschmidt C. (1997) NF-kappaB: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci. 20, 252 258.
39. delOlmo N., Higuera-Matas A., Miguéns M., García-Lecumberri C., Borcel E., Solis J. M. Ambrosio E. (2006) Hippocampal synaptic plasticity and water maze learning in cocaine self-administered rats. Ann. N Y Acad. Sci. 1074, 427 437.
40. delOlmo N., Higuera-Matas A., Miguéns M., García-Lecumberri C. Ambrosio E. (2007) Cocaine self-administration improves performance in a highly demanding water maze task. Psychopharmacology (Berl.) 195, 19 25.
41. Pavone A. Cardile V. (2003) An in vitro study of new antiepileptic drugs and astrocytes. Epilepsia 44, 34 39.
42. Przewlocka B., Lason W., Machelska H. Przewlocki R. (1994) The effects of cocaine-induced seizures on the proenkephalin mRNA level in the mouse hippocampus: a possible involvement of the nitric oxide pathway. Neurosci. Lett. 168, 81 84.
43. Rawls S. M., Rodriguez T., Baron D. A. Raffa R. B. (2006) A nitric oxide synthase inhibitor (L-NAME) attenuates abstinence-induced withdrawal from both cocaine and a cannabinoid agonist (WIN 55212-2) in Planaria. Brain Res. 1099, 82 87.
44. Reed D. J., Babson J. R., Beatty P. W., Brodie A. E., Ellis W. W. Potter D. W. (1980) High-performance liquid chromatography analysis of nanomole levels of glutathione, glutathione disulfide, and related disulfides. Anal. Biochem. 106, 55 62.
45. Rigoulot M. A., Boehrer A. Nehlig A. (2003) Effects of topiramate in two models of genetically determined generalized epilepsy, the GAERS and the Audiogenic Wistar AS. Epilepsia 44, 14 19. (Pubitemid 36733615)
46. Saha G. B., MacIntyre W. J. Go R. T. (1994) Radiopharmaceuticals for brain imaging. Semin. Nucl. Med. 24, 324 349.
47. Schmidt H. H., Pollock J. S., Nakane M., Gorsky L. D., Förstermann U. Murad F. (1991) Purification of a soluble isoform of guanylyl cyclase-activating-factor synthase. Proc. Natl. Acad. Sci. USA 88, 365 369.
48. Schreck R., Albertmann K. Bauerle P. A. (1992) Nuclear factor kappa B: an oxidative stress-response transcription factor of eukaryotic cells. Free Rad. Res. Commun. 17, 221 237.
49. Schroeder J. A., McCafferty M. R. Unterwald E. M. (2009) Regulation of dynamin 2 and G protein-coupled receptor kinase 2 in rat nucleus accumbens during acute and repeated cocaine administration. Synapse 63, 863 870.
50. Stuehr D. J. Ikeda-Saito M. (1992) Spectral characterization of brain and macrophage nitric oxide synthases. Cytochrome P-450-like hemeproteins that contain a flavin semiquinone radical. J. Biol. Chem. 267, 20547 20550.
51. Takehara K., Kawahara S. Kirino Y. (2003) Time-dependent reorganization of the brain components underlying memory retention in trace abling conditioning. J. Neurosci. 23, 9897 9905.
52. Tzschentke T. M. Schmidt W. J. (2000) Differential effects of discrete subarea-specific lesions of the rat medial prefrontal cortex on amphetamine- and cocaine-induced behavioural sensitization. Cereb. Cortex 10, 488 498.
53. Volkow N. D. Fowler J. S. (2000) Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb. Cortex 10, 318 325.
54. Volkow N. D., Fowler J. S., Wang G. J. Swanson J. M. (2004) Dopamine in drug abuse and addiction: results from imaging studies and treatment implications. Mol. Psychiatry 9, 557 569.
55. Volz T. J. Schenk J. O. (2004) L-arginine increases dopamine transporter activity in rat striatum via a nitric oxide synthase-dependent mechanism. Synapse 54, 173 182.
56. West A. E., Griffith E. C. Greenberg M. E. (2002) Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3, 921 929.
57. Wilson S. J., Sayette M. A. Fiez J. A. (2004) Prefrontal responses to drug cues: a neurocognitive analysis. Nat. Neurosci. 7, 211 214.
58. Wood S. C., Fay J., Sage J. R. Anagnostaras S. G. (2007) Cocaine and Pavlovian fear conditioning: dose-effect analysis. Behav. Brain Res. 176, 244 250.
59. Zhang S., Chen J. Wang S. (1998) Spatial learning and memory induce up-regulation of nitric oxide-producing neurons in rat brain. Brain Res. 801, 101 106.