Differences in vulnerability to nicotine-induced kindling between female and male periadolescent rats

Psychopharmacology

Volumn 225, Issue 1, 2013, Pages 115-126

  Gomes, Patrícia Xavier L ^a   De Oliveira, Gersilene V ^a   De Araújo, Fernanda Yvelize R ^a   De Barros Viana, Glauce Socorro ^a   De Sousa, Francisca Cléa F ^a   Hyphantis, Thomas N ^b   Grunberg, Neil E ^c   Carvalho, André F ^a   MacÊdo, Danielle S ^a  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^b UNIVERSITY OF IOANNINA   (Greece)

^c Uniformed Services University of the Health Sciences   (United States)

Author keywords

Antioxidant; Hippocampus; Kindling; Nicotine; Oxidative stress; Prefrontal cortex; Seizure; Striatum

Indexed keywords

ALPHA TOCOPHEROL; ESTRADIOL; GLUTATHIONE; MALONALDEHYDE; NICOTINE; SUPEROXIDE DISMUTASE; TESTOSTERONE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; FEMALE; HIPPOCAMPUS; KINDLING; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SEIZURE; SEX DIFFERENCE; TREATMENT OUTCOME;

ANIMALS; ANTIOXIDANTS; CORPUS STRIATUM; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GLUTATHIONE; HIPPOCAMPUS; KINDLING, NEUROLOGIC; LIPID PEROXIDATION; MALE; NICOTINE; NICOTINIC AGONISTS; OXIDATIVE STRESS; PREFRONTAL CORTEX; RATS; RATS, WISTAR; SEX FACTORS; SUPEROXIDE DISMUTASE; TIME FACTORS; VITAMIN E;

EID: 84872356754     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-012-2799-5     Document Type: Article

References (96)

1. Adams JD, Wang B (1994) Vitamin E uptake into the brain and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine toxicity. J Cereb Blood Flow Metab 14:362-363
2. Agarwal NB, Jain S, Agarwal NK, Mediratta PK, Sharma KK (2011) Modulation of pentylenetetrazole-induced kindling and oxidative stress by curcumin in mice. Phytomedicine 18:756-759
3. Alkondon M, Pereira EFR, Almeida LEF, Randall WR, Albuquerque EX (2000) Nicotine at concentrations found in cigarette smokers activates and desensitizes nicotinic acetylcholine receptors in CA1 interneurons of rat hippocampus. Neuropharmacology 39:2726-2739
4. Andersen SL, Rutstein M, Benzo JM, Hostetter JC, Teicher MH (1997) Sex differences in dopamine receptor overproduction and elimination. Neuroreport 8:1495-1498
5. Andersen SL, Thompson AT, Rutstein M, Hostetter JC, Teicher MH (2000) Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37:167-169
6. Andersen SL, Thompson AP, Krenzel E, Teicher MH (2002) Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction. Psychoneuroendocrinology 27:683-691
7. Bastlund JF, Berry D, Watson WP (2005) Pharmacological and histological characterisation of nicotine-kindled seizures in mice. Neuropharmacology 48:975-983
8. Becker JB, Robinson TE, Lorenz KA (1982) Sex differences and estrous cycle variations in amphetamine-elicited rotational behavior. Eur J Pharmacol 80:65-72
9. Bell IR, Rossi J, Gilbert ME, Kobal G, Morrow LA, Newlin DB, Sorg BA, Wood RW (1997) Testing the neural sensitization and kindling hypothesis for illness from low levels of environmental chemicals. Environ Health Perspect 105:539-547
10. Bob P, Glaslova K, Susta M, Jasova D, Raboch J (2006) Traumatic dissociation, epileptic-like phenomena, and schizophrenia. Neuroendocrinol Lett 27:321-326
11. Booze RM, Welch MA, Wood ML, Billings KA, Apple SR, Mactutus CF (1999) Behavioral sensitization following repeated intravenous nicotine administration: gender differences and gonadal hormones. Pharmacol Biochem Behav 64:827-839
12. 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
13. Buchmann AF, Blomeyer D, Jennen-Steinmetz C, Schmidt MH, Esser G, Banaschewski T, Laucht M (2011) Early smoking onset may promise initial pleasurable sensations and later addiction. Addict Biol. doi: 10.1111/j.1369-1600.2011.00377.x
14. Burton GW, Traber MG (1990) Vitamin E: antioxidant activity, biokinetics, and bioavailability. Annu Rev Nutr 10:357-382
15. Castle L, Perkins MJ (1986) Inhibition-kinetics of chain-breaking phenolic antioxidants in SDS micelles - evidence that intermicellar diffusion rates may be rate-limiting for hydrophobic inhibitors such as alpha-tocopherol. J Am Chem Soc 108:6381-6382
16. Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, Lena C, Clementi F, Moretti M, Rossi FM, Le Novere N, McIntosh JM, Gardier AM, Changeux JP (2003) Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J Neurosci 23:7820-7829
17. Chen TY, Zhang D, Dragomir A, Akay Y, Akay M (2011) The effects of nicotine exposure and PFC transection on the time-frequency distribution of VTA DA neurons' firing activities. Med Biol Eng Comput 49:605-612
18. Clarke PB, Kumar R (1983) The effects of nicotine on locomotor activity in non-tolerant and tolerant rats. Br J Pharmacol 78:329-337
19. Collins SL, Wade D, Ledon J, Izenwasser S (2004) Neurochemical alterations produced by daily nicotine exposure in periadolescent vs. adult male rats. Eur J Pharmacol 502:75-85
20. Damaj MI, Glassco W, Dukat M, Martin BR (1999) Pharmacological characterization of nicotine-induced seizures in mice. J Pharmacol Exp Ther 291:1284-1291
21. Delfino RJ, Jamner LD, Whalen CK (2001) Temporal analysis of the relationship of smoking behavior and urges to mood states in men versus women. Nicotine Tob Res 3:235-248
22. Doura MB, Gold AB, Keller AB, Perry DC (2008) Adult and periadolescent rats differ in expression of nicotinic cholinergic receptor subtypes and in the response of these subtypes to chronic nicotine exposure. Brain Res 1215:40-52
23. Dringen R, Hirrlinger J (2003) Glutathione pathways in the brain. Biol Chem 384:505-516
24. Duchen MR (2000) Mitochondria and calcium: from cell signalling to cell death. J Physiol Lond 529:57-68
25. Edwards HE, Burnham WM, MacLusky NJ (1999) Testosterone and its metabolites affect afterdischarge thresholds and the development of amygdala kindled seizures. Brain Res 838:151-157
26. El-Abhar Hanan S, El Gawad Hanan MA (2003) Modulation of cortical nitric oxide synthase, glutamate, and redox state by nifedipine and taurine in PTZ-kindled mice. Epilepsia 44:276-281
27. Erakovic V, Zupan G, Varljen J, Simonic A (2003) Pentylenetetrazol- induced seizures and kindling: changes in free fatty acids, superoxide dismutase, and glutathione peroxidase activity. Neurochem Int 42:173-178
28. Frantseva MV, Velazquez JLP, Tsoraklidis G, Mendonca AJ, Adamchik Y, Mills LR, Carlen PL, Burnham MW (2000) Oxidative stress is involved in seizure-induced neurodegeneration in the kindling model of epilepsy. Neuroscience 97:431-435
29. Freitas RM, Vasconcelos SMM, Souza FCF, Viana GSB, Fonteles MMF (2005) Oxidative stress in the hippocampus after pilocarpine-induced status epilepticus in Wistar rats. FEBS J 272:1307-1312
30. Frye CA, Reed TA (1998) Androgenic neurosteroids: anti-seizure effects in an animal model of epilepsy. Psychoneuroendocrinology 23:385-399
31. Gluck MR, Jayatilleke E, Shaw S, Rowan AJ, Haroutunian V (2000) CNS oxidative stress associated with the kainic acid rodent model of experimental epilepsy. Epilepsy Res 39:63-71
32. Goddard GV (1969) Analysis of avoidance conditioning following cholinergic stimulation of amygdala in rats. J Comp Physiol Psychol 68:1-18
33. Grunberg NE, Winders SE, Wewers ME (1991) Gender differences in tobacco use. Health Psychol 10:143-153
34. Grunberg NE, Berger SS, Starosciak A (2011) Tobacco use: Psychology, neurobiology, and clinical implications. In: Baum A, Revenson T, Singer JE (eds) Handbook of health psychology. Psychology Press, New York
35. Gumustekin K, Altinkaynak K, Timur H, Taysi S, Oztasan N, Polat MF, Akcay F, Suleyman H, Dane S, Gul M (2003) Vitamin E but not Hippophea rhamnoides L. prevented nicotine-induced oxidative stress in rat brain. Hum Exp Toxicol 22:425-431
36. Gusakov I, Sharonov B, Oparina T, Kambarova D (1995) Effect of superoxide dismutase on convulsive seizures in rat models of epilepsy. Bull Exp Biol Med 120:665-667
37. Hamed SA, Abdellah MM, El-Melegy N (2004) Blood levels of trace elements, electrolytes, and oxidative stress/antioxidant systems in epileptic patients. J Pharmacol Sci 96:465-473
38. Harrod SB, Mactutus CF, Bennett K, Hasselrot U, Wu G, Welch M, Booze RM (2004) Sex differences and repeated intravenous nicotine: behavioral sensitization and dopamine receptors. Pharmacol Biochem Behav 78:581-592
39. Huong NT, Matsumoto K, Watanabe H (1998) The antistress effect of majonoside-R2, a major saponin component of Vietnamese ginseng: neuronal mechanisms of action. Methods Find Exp Clin Pharmacol 20:65-76
40. Ilhan A, Aladag MA, Kocer A, Boluk A, Gurel A, Armutcu F (2005) Erdosteine ameliorates PTZ-induced oxidative stress in mice seizure model. Brain Res Bull 65:495-499
41. Ishige K, Schubert D, Sagara Y (2001) Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms. Free Radic Biol Med 30:433-446
42. Itzhak Y (1996) Attenuation of cocaine kindling by 7-nitroindazole, an inhibitor of brain nitric oxide synthase. Neuropharmacology 35:1065-1073
43. 3H] dopamine release by glutathione in mouse striatal slices. Neurochem Res 32:1357-1364
44. Kovacic P, Cooksy A (2005) Iminium metabolite mechanism for nicotine toxicity and addiction: oxidative stress and electron transfer. Med Hypotheses 64:104-111
45. Kumar P, Kale RK, McLean P, Baquer NZ (2011) Protective effects of 17 beta estradiol on altered age related neuronal parameters in female rat brain. Neurosci Lett 502:56-60
46. Levin ED, Rezvani AH, Montoya D, Rose JE, Swartzwelder HS (2003) Adolescent-onset nicotine self-administration modeled in female rats. Psychopharmacology (Berl) 169:141-149
47. Levin ED, Slade S, Wells C, Cauley M, Petro A, Vendittelli A, Johnson M, Williams P, Horton K, Rezvani AH (2011) Threshold of adulthood for the onset of nicotine self-administration in male and female rats. Behav Brain Res 225:473-481
48. Lin YT, Han YX, Xu JJ, Cao LL, Gao J, Xie NC, Zhao XH, Jiang H, Chi ZF (2010) Mitochondrial DNA damage and the involvement of antioxidant defense and repair system in hippocampi of rats with chronic seizures. Cell Mol Neurobiol 30:947-954
49. McClernon FJ, Hiott FB, Westman EC, Rose JE, Levin ED (2006) Transdermal nicotine attenuates depression symptoms in nonsmokers: a double-blind, placebo-controlled trial. Psychopharmacology 189:125-133
50. Meredith M (1998) Vomeronasal, olfactory, hormonal convergence in the brain. Cooperation or coincidence? Ann N Y Acad Sci 855:349-361
51. Minozzi S, Amato L, Davoli M, Farrell M, Lima R, Pani PP, Silva DM, Soares B, Vecchi S (2008) Anticonvulsants for cocaine dependence. Cochrane Database Syst Rev 35:CD:006754
52. Mula M, Marotta AE, Monaco F (2010) Epilepsy and bipolar disorders. Expert Rev Neurother 10:13-23
53. Nordberg A (1993) In-vivo detection of neurotransmitter changes in alzheimers disease. In: Nitsch RM et al (eds) Alzheimers disease: amyloid precusor proteins, signal transduction, and neuronal transplantation, vol 695. New York Acad Sciences, New York, pp 27-33
54. Okamoto M, Kita T, Okuda H, Nakashima T (1992) Tolerance to the convulsions induced by daily nicotine treatment in rats. Jpn J Pharmacol 59:449-455
55. Olfert ED, Cross BM, McWilliam AA (1993) Guide to the care and use of experimental animals. Canadian Council on Animal Care, Ontario Canada
56. Ortiz GG, Sanchez-Ruiz MY, Tan DX, Reiter RJ, Benitez-King G, Beas-Zarate C (2001) Melatonin, vitamin E, and estrogen reduce damage induced by kainic acid in the hippocampus: potassium-stimulated GABA release. J Pineal Res 31:62-67
57. Pappert EJ, Tangney CC, Goetz CG, Ling ZD, Lipton JW, Stebbins GT, Carvey PM (1996) Alpha-tocopherol in the ventricular cerebrospinal fluid of Parkinson's disease patients: dose-response study and correlations with plasma levels. Neurology 47:1037-1042
58. Parameshwaran K, Buabeid MA, Karuppagounder SS, Uthayathas S, Thiruchelvam K, Shonesy B, Dityatev A, Escobar MC, Dhanasekaran M, Suppiramaniam V (2012) Developmental nicotine exposure induced alterations in behavior and glutamate receptor function in hippocampus. Cell Mol Life Sci 69:829-841
59. Pauly JR (2008) Gender differences in tobacco smoking dynamics and the neuropharmacological actions of nicotine. Front Biosci 13:505-516
60. Perkins KA (1999) Nicotine discrimination in men and women. Pharmacol Biochem Behav 64:295-299
61. Pontieri FE, Tanda G, Orzi F, Di Chiara G (1996) Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 382:255-257
62. Post RM (2004) Neurobiology of seizures and behavioral abnormalities. Epilepsia 45:5-14
63. Post RM (2007) Kindling and sensitization as models for affective episode recurrence, cyclicity, and tolerance phenomena. Neurosci Biobehav Rev 31:858-873
64. Post RM, Weiss SRB (1992) Endogenous biochemical-abnormalities in affective-illness - therapeutic versus pathogenic. Biol Psychiatry 32:469-484
65. Post RM, Weiss SRB, Smith M, Li H, McCann U (1997) Kindling versus quenching - implications for the evolution and treatment of posttraumatic stress disorder. In: Yehuda R, McFarlane AC (eds) Psychobiology of posttraumatic stress disorder, vol 821. New York Academy of Sciences, New York, pp 285-295
66. Racine RJ, Gartner JG, Burnham WM (1972) Epileptiform activity and neural plasticity in limbic structures. Brain Res 47:262-268
67. Rasheed N, Ahmad A, Al-Sheeha M, Alghasham A, Palit G (2011) Neuroprotective and anti-stress effect of A68930 in acute and chronic unpredictable stress model in rats. Neurosci Lett 504:151-155
68. Rauca C, Wiswedel I, Zerbe R, Keilhoff G, Krug M (2004) The role of superoxide dismutase and alpha-tocopherol in the development of seizures and kindling induced by pentylenetetrazol - influence of the radical scavenger alpha-phenyl-N-tert-butyl nitrone. Brain Res 1009:203-212
69. Reddy DS, Jian K (2010) The testosterone-derived neurosteroid androstanediol is a positive allosteric modulator of GABAA receptors. J Pharmacol Exp Ther 334:1031-1041
70. Reichert VC, Seltzer V, Efferen LS, Kohn N (2009) Women and tobacco dependence. Obstet Gynecol Clin North Am 36:877-890, xi
71. Riljak V, Milotova M, Jandova K, Pokorny J, Langmeier M (2007) Morphological changes in the hippocampus following nicotine and kainic acid administration. Physiol Res 56:641-649
72. Rosse RB, Mastropaolo J, Novitzki MR, Deutsch SI (1990) Depot testosterone attenuates the anticonvulsant effect of flurazepam in mice. Psychoneuroendocrinology 15:83-85
73. Rubboli F, Court JA, Sala C, Morris C, Perry E, Clementi F (1994) Distribution of neuronal nicotinic receptor subunits in human brain. Neurochem Int 25:69-71
74. Sashindranath M, McLean KJ, Trounce IA, Cotton RGH, Cook MJ (2010) Early hippocampal oxidative stress is a direct consequence of seizures in the rapid electrical amygdala kindling model. Epilepsy Res 90:285-294
75. Sechi G, Rosati G, Deiana GA, Petruzzi V, Deriu F, Correddu P, De Riu PL (1997) Co-variation of free amino acids in brain interstitial fluid during pentylenetetrazole-induced convulsive status epilepticus. Brain Res 764:230-236
76. Sedlak J, Hanus L (1982) Changes of glutathione and protein bound SH-groups concentration in rat adrenals under acute and repeated stress. Endocrinol Exp 16:103-109
77. Sejima H, Ito M, Kishi K, Tsuda H, Shiraishi H (1997) Regional excitatory and inhibitory amino acid concentrations in pentylenetetrazol kindling and kindled rat brain. Brain Dev 19:171-175
78. Shandra AA, Mazarati AM, Godlevsky LS, Vastyanov RS (1996) Chemical kindling: implications for antiepileptic drugs - sensitive and resistant epilepsy models. Epilepsia 37:269-274
79. Shin EJ, Jeong JH, Chung YH, Kim WK, Ko KH, Bach JH, Hong JS, Yoneda Y, Kim HC (2011) Role of oxidative stress in epileptic seizures. Neurochem Int 59:122-137
80. Silverstein B, Feld S, Kozlowski LT (1980) The availability of low-nicotine cigarettes as a cause of cigarette-smoking among teenage females. J Health Soc Behav 21:383-388
81. Singh R, Pathak DN (1990) Lipid-peroxidation and glutathione-peroxidase, glutathione-reductase, seperoxide-dismutase, catalase and glucose-6-phosphate- dehydrogenase activities in FeCl3-induced epileptogenic foci in the rat brain. Epilepsia 31:15-26
82. Sleven H, Gibbs JE, Heales S, Thom M, Cock HR (2006) Depletion of reduced glutathione precedes inactivation of mitochondrial enzymes following limbic status epilepticus in the rat hippocampus. Neurochem Int 48:75-82
83. Slotkin TA, Cousins MM, Seidler FJ (2004) Administration of nicotine to adolescent rats evokes regionally selective upregulation of CNS alpha 7 nicotinic acetylcholine receptors. Brain Res 1030:159-163
84. Smith RF (2003) Animal models of periadolescent substance abuse. Neurotoxicol Teratol 25:291-301
85. Sood N, Sahai AK, Medhi B, Chakrabarti A (2008) Dose-finding study with nicotine as a proconvulsant agent in PTZ-induced seizure model in mice. J Biomed Sci 15:755-765
86. Sun Y, Colburn NH, Oberley LW (1993) Decreased expression of manganese superoxide dismutase mRNA and protein after immortalization and transformation of mouse liver cells. Oncol Res 5:127-132
87. Tchekalarova J, Sotiriou E, Angelatou F (2004) Down-regulation of dopamine D1 and D2 receptors in the basal ganglia of PTZ kindling model of epilepsy: effects of angiotensin IV. Brain Res 1024:159-166
88. Tizabi Y, Hauser SR, Tyler KY, Getachew B, Madani R, Sharma Y, Manaye KF (2010) Effects of nicotine on depressive-like behavior and hippocampal volume of female WKY rats. Prog Neuropsychopharmacol Biol Psychiatry 34:62-69
89. Trauth JA, Seidler FJ, Slotkin TA (2000) Persistent and delayed behavioral changes after nicotine treatment in adolescent rats. Brain Res 880:167-172
90. USHHS (1988) The health consequences of smoking: nicotine addiction: a report of the Surgeon General: Center for Health Promotion and Education. Office on Smoking and Health
91. Waldbaum S, Liang LP, Patel M (2010) Persistent impairment of mitochondrial and tissue redox status during lithium-pilocarpine-induced epileptogenesis. J Neurochem 115:1172-1182
92. Walker QD, Rooney MB, Wightman RM, Kuhn CM (2000) Dopamine release and uptake are greater in female than male rat striatum as measured by fast cyclic voltammetry. Neuroscience 95:1061-1070
93. Wallace TL, Porter RH (2011) Targeting the nicotinic alpha7 acetylcholine receptor to enhance cognition in disease. Biochem Pharmacol 82:891-903
94. Wang X-J, Zhang S, Yan Z-Q, Zhao Y-X, Zhou H-Y, Wang Y, Lu G-Q, Zhang J-D (2011) Impaired CD200-CD200R-mediated microglia silencing enhances midbrain dopaminergic neurodegeneration: roles of aging, superoxide, NADPH oxidase, and p38 MAPK. Free Radic Biol Med 50:1094-1106
95. Wonnacott S, Soliakov L, Wilkie G, Redfern P, Marshall D (1996) Presynaptic nicotinic acetylcholine receptors in the brain. Drug Dev Res 38:149-159
96. Yang JL, Tadokoro T, Keijzers G, Mattson MP, Bohr VA (2010) Neurons efficiently repair glutamate-induced oxidative DNA damage by a process involving CREB-mediated up-regulation of apurinic endonuclease 1. J Biol Chem 285:28191-28199