A sex difference in oxidative stress and behavioral suppression induced by ethanol withdrawal in rats

Behavioural Brain Research

Volumn 314, Issue , 2016, Pages 199-214

  Jung, Marianna E ^a   Metzger, Daniel B ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

17 Estradiol; Antioxidant; Cerebellum; Cytochrome c oxidase; Ethanol withdrawal; Hippocampus

Indexed keywords

ALPHA TOCOPHEROL; CYTOCHROME C OXIDASE; ESTRADIOL; MALONALDEHYDE; OXYGEN RADICAL; PROTEIN CARBONYL; PROTEIN DERIVATIVE; UBIDECARENONE; UNCLASSIFIED DRUG; ALCOHOL; ANTIOXIDANT; REACTIVE OXYGEN METABOLITE;

ADULT; ALCOHOL WITHDRAWAL; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CEREBELLUM; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HIPPOCAMPUS; MALE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MORRIS WATER MAZE TEST; NONHUMAN; OVARIECTOMY; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; ROTAROD TEST; SEX DIFFERENCE; ANIMAL; DRUG EFFECTS; METABOLISM; MITOCHONDRION; MOUSE; SEXUAL CHARACTERISTICS; SPRAGUE DAWLEY RAT; WITHDRAWAL SYNDROME;

ANIMALS; ANTIOXIDANTS; ESTRADIOL; ETHANOL; FEMALE; MALE; MICE; MITOCHONDRIA; OXIDATIVE STRESS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SEX CHARACTERISTICS; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 84981170543     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2016.07.054     Document Type: Article

References (70)

1. [1] Gonzaga, N.A., Mecawi, A.S., Antunes-Rodrigues, J., De Martinis, B.S., Padovan, C.M., Tirapelli, C.R., Ethanol withdrawal increases oxidative stress and reduces nitric oxide bioavailability in the vasculature of rats. Alcohol 49 (2015), 47–56.
2. [2] Tsai, G.E., Ragan, P., Chang, R., Chen, S., Linnoila, V.M., Coyle, J.T., Increased glutamatergic neurotransmission and oxidative stress after alcohol withdrawal. Am. J. Psychiatry 155 (1998), 726–732.
3. [3] Huang, M.C., Chen, C.H., Peng, F.C., Tang, S.H., Chen, C.C., Alterations in oxidative stress status during early alcohol withdrawal in alcoholic patients. J. Formos. Med. Assoc. 108 (2009), 560–569.
4. [4] Lecomte, E., Herbeth, B., Pirollet, P., Chancerelle, Y., Arnaud, J., Musse, N., Paille, F., Siest, G., Artur, Y., Effect of alcohol consumption on blood antioxidant nutrients and oxidative stress indicators. Am. J. Clin. Nutr. 60 (1994), 255–261.
5. [5] Peng, F.C., Tang, S.H., Huang, M.C., Chen, C.C., Kuo, T.L., Yin, S.J., Oxidative status in patients with alcohol dependence: a clinical study in Taiwan. J. Toxicol. Environ. Health A 68 (2005), 1497–1509.
6. [6] SAMHSA Administration, National Survey on Drug Use and Health (NSDUH). 2014 http://www.samhsa.gov/data/sites/default/files/NSDUH-DetTabs2014/NSDUH-DetTabs2014.htm#tab5-8a.
7. [7] Wojnar, M., Wasilewski, D., Matsumoto, H., Cedro, A., Differences in the course of alcohol withdrawal in women and men: a Polish sample. Alcohol Clin. Exp. Res. 21 (1997), 1351–1355.
8. [8] Hashimoto, J.G., Wiren, K.M., Neurotoxic consequences of chronic alcohol withdrawal: expression profiling reveals importance of gender over withdrawal severity. Neuropsychopharmacology 33 (2008), 1084–1096.
9. [9] Deshmukh, A., Rosenbloom, M.J., Sassoon, S., O'Reilly, A., Pfefferbaum, A., Sullivan, E.V., Alcoholic men endorse more DSM-IV withdrawal symptoms than alcoholic women matched in drinking history. J. Stud. Alcohol 64 (2003), 375–379.
10. [10] Varlinskaya, E.I., Spear, L.P., Acute ethanol withdrawal (hangover) and social behavior in adolescent and adult male and female Sprague-Dawley rats. Alcohol Clin. Exp. Res. 28 (2004), 40–50.
11. [11] Devaud, L.L., Purdy, R.H., Morrow, A.L., The neurosteroid 3 alpha-hydroxy-5 alpha-pregnan-20-one, protects against bicuculline-induced seizures during ethanol withdrawal in rats. Alcohol Clin. Exp. Res. 19 (1995), 350–355.
12. [12] Alele, P.E., Devaud, L.L., Sex differences in steroid modulation of ethanol withdrawal in male and female rats. J. Pharmacol. Exp. Ther. 320 (2007), 427–436.
13. [13] Engler-Chiurazzi, E.B., Brown, C.M., Povroznik, J.M., Simpkins, J.W., Estrogens as neuroprotectants: estrogenic actions in the context of cognitive aging and brain injury. Prog. Neurobiol., 2016 (in press).
14. [14] Bruce-Keller, A.J., Dimayuga, F.O., Reed, J.L., Wang, C., Angers, R., Wilson, M.E., Dimayuga, V.M., Scheff, S.W., Gender and estrogen manipulation do not affect traumatic brain injury in mice. J. Neurotrauma 24 (2007), 203–215.
15. [15] Lebesgue, D., LeBold, D.G., Surles, N.O., Morales, D.M., Etgen, A.M., Zukin, R.S., Saatman, K.E., Effects of estradiol on cognition and hippocampal pathology after lateral fluid percussion brain injury in female rats. J. Neurotrauma 23 (2006), 1814–1827.
16. [16] Prokai-Tatrai, K., Prokai, L., Simpkins, J.W., Jung, M.E., Phenolic compounds protect cultured hippocampal neurons against ethanol-withdrawal induced oxidative stress. Int. J. Mol. Sci. 10 (2009), 1773–1787.
17. [17] Simpkins, J.W., Yi, K.D., Yang, S.H., Dykens, J.A., Mitochondrial mechanisms of estrogen neuroprotection. Biochim. Biophys. Acta 1800 (2010), 1113–1120.
18. [18] Borras, C., Sastre, J., Garcia-Sala, D., Lloret, A., Pallardo, F.V., Vina, J., Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic. Biol. Med. 34 (2003), 546–552.
19. [19] Jung, M.E., Yang, S.H., Brun-Zinkernagel, A.M., Simpkins, J.W., Estradiol protects against cerebellar damage and motor deficit in ethanol-withdrawn rats. Alcohol 26 (2002), 83–93.
20. [20] Becker, H.C., Hale, R.L., Repeated episodes of ethanol withdrawal potentiate the severity of subsequent withdrawal seizures: an animal model of alcohol withdrawal kindling. Alcohol Clin. Exp. Res. 17 (1993), 94–98.
21. [21] George, D.T., Nutt, D.J., Dwyer, B.A., Linnoila, M., Alcoholism and panic disorder: is the comorbidity more than coincidence. Acta Psychiatr. Scand. 81 (1990), 97–107.
22. [22] NIAAA, The Physicians' Guide to Helping Patients With Alcohol Problems National Institute on Alcohol Abuse and Alcoholism, Rockville, MD, 1995.
23. [23] Stephens, D.N., Brown, G., Duka, T., Ripley, T.L., Impaired fear conditioning but enhanced seizure sensitivity in rats given repeated experience of withdrawal from alcohol. Eur. J. Neurosci. 14 (2001), 2023–2031.
24. [24] Brown, M.E., Anton, R.F., Malcolm, R., Ballenger, J.C., Alcohol detoxification and withdrawal seizures: clinical support for a kindling hypothesis. Biol. Psychiatry 23 (1988), 507–514.
25. [25] McDonald, S.R., Sohal, R.S., Forster, M.J., Concurrent administration of coenzyme Q10 and alpha-tocopherol improves learning in aged mice. Free Radic. Biol. Med. 38 (2005), 729–736.
26. [26] Smolen, A., Marks, M.J., Smolen, T.N., Collins, A.C., Dose and route of administration alter the relative elimination of ethanol by long-sleep and short-sleep mice. Alcohol Clin. Exp. Res. 10 (1986), 198–204.
27. [27] Forster, M.J., Dubey, A., Dawson, K.M., Stutts, W.A., Lal, H., Sohal, R.S., Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 4765–4769.
28. [28] Rewal, M., Jung, M., Wen, Y., Brun-Zinkernagel, A., Simpkins, J., Role of the GABAA system in behavioral, motoric, and cerebellar protection by estrogen during ethanol withdrawal. Alcohol 31 (2003), 49–61.
29. [29] Morris, R., Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11 (1984), 47–60.
30. [30] Walls, S.A., Rosenwasser, A.M., Devaud, L.L., Sex and regional differences in effects of chronic intermittent ethanol exposure on subsequent excitotoxic challenges in hippocampal slice cultures. Neurosci. Lett. 550 (2013), 6–11.
31. [31] Yan, L.J., Yang, S.H., Shu, H., Prokai, L., Forster, M.J., Histochemical staining and quantification of dihydrolipoamide dehydrogenase diaphorase activity using blue native PAGE. Electrophoresis 28 (2007), 1036–1045.
32. [32] Christophe, M., Nicolas, S., Mitochondria: a target for neuroprotective interventions in cerebral ischemia-reperfusion. Curr. Pharm. Des. 12 (2006), 739–757.
33. [33] Turrens, J.F., Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 17 (1997), 3–8.
34. [34] Azzi, A., Montecucco, C., Richter, C., The use of acetylated ferricytochrome c for the detection of superoxide radicals produced in biological membranes. Biochem. Biophys. Res. Commun. 65 (1975), 597–603.
35. [35] Kwong, L.K., Kamzalov, S., Rebrin, I., Bayne, A.C., Jana, C.K., Morris, P., Forster, M.J., Sohal, R.S., Effects of coenzyme Q(10) administration on its tissue concentrations, mitochondrial oxidant generation, and oxidative stress in the rat. Free Radic. Biol. Med. 33 (2002), 627–638.
36. [36] Huber, W., Kraupp-Grasl, B., Esterbauer, H., Schulte-Hermann, R., Role of oxidative stress in age dependent hepatocarcinogenesis by the peroxisome proliferator nafenopin in the rat. Cancer Res. 51 (1991), 1789–1792.
37. [37] Ledwozyw, A., Michalak, J., Stepien, A., Kadziolka, A., The relationship between plasma triglycerides cholesterol, total lipids and lipid peroxidation products during human atherosclerosis. Clin. Chim. Acta 155 (1986), 275–283.
38. [38] Grimsrud, P.A., Xie, H., Griffin, T.J., Bernlohr, D.A., Oxidative stress and covalent modification of protein with bioactive aldehydes. J. Biol. Chem. 283 (2008), 21837–21841.
39. [39] Amici, A., Levine, R.L., Tsai, L., Stadtman, E.R., Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions. J. Biol. Chem. 264 (1989), 3341–3346.
40. [40] Levine, R.L., Garland, D., Oliver, C.N., Amici, A., Climent, I., Lenz, A.G., Ahn, B.W., Shaltiel, S., Stadtman, E.R., Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 186 (1990), 464–478.
41. [41] Yan, L.J., Christians, E.S., Liu, L., Xiao, X., Sohal, R.S., Benjamin, I.J., Mouse heat shock transcription factor 1 deficiency alters cardiac redox homeostasis and increases mitochondrial oxidative damage. EMBO J. 21 (2002), 5164–5172.
42. [42] Jung, M.E., Ju, X., Metzger, D.B., Simpkins, J.W., Ethanol withdrawal hastens the aging of cytochrome c oxidase. Neurobiol. Aging, 33, 2011, 618 e21–32.
43. [43] Li, Y., Maher, P., Schubert, D., Phosphatidylcholine-specific phospholipase C regulates glutamate-induced nerve cell death. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 7748–7753.
44. [44] Thomas, M.P., Monaghan, D.T., Morrisett, R.A., Evidence for a causative role of N-methyl-D-aspartate receptors in an in vitro model of alcohol withdrawal hyperexcitability. J. Pharmacol. Exp. Ther. 287 (1998), 87–97.
45. [45] Perez, E., Liu, R., Yang, S.H., Cai, Z.Y., Covey, D.F., Simpkins, J.W., Neuroprotective effects of an estratriene analog are estrogen receptor independent in vitro and in vivo. Brain Res. 1038 (2005), 216–222.
46. [46] Jung, M.E., Wilson, A.M., Ju, X., Wen, Y., Metzger, D.B., Simpkins, J.W., Ethanol withdrawal provokes opening of the mitochondrial membrane permeability transition pore in an estrogen-preventable manner. J. Pharmacol. Exp. Ther. 328 (2009), 692–698.
47. [47] Marchi, S., Giorgi, C., Suski, J.M., Agnoletto, C., Bononi, A., Bonora, M., De Marchi, E., Missiroli, S., Patergnani, S., Poletti, F., Rimessi, A., Duszynski, J., Wieckowski, M.R., Pinton, P., Mitochondria-Ros crosstalk in the control of cell death and aging. J. Signal Transduct., 2012, 2012, 10.1155/2012/329635 (Article ID 329635).
48. [48] Galindo, M.F., Jordan, J., Gonzalez-Garcia, C., Cena, V., Reactive oxygen species induce swelling and cytochrome c release but not transmembrane depolarization in isolated rat brain mitochondria. Br. J. Pharmacol. 139 (2003), 797–804.
49. [49] Ebrahimian, T., He, Y., Schiffrin, E.L., Touyz, R.M., Differential regulation of thioredoxin and NAD(P)H oxidase by angiotensin II in male and female mice. J. Hypertens 25 (2007), 1263–1271.
50. [50] Borras, C., Gambini, J., Lopez-Grueso, R., Pallardo, F.V., Vina, J., Direct antioxidant and protective effect of estradiol on isolated mitochondria. Biochim. Biophys. Acta 1802 (2010), 205–211.
51. [51] Esposito, L.A., Melov, S., Panov, A., Cottrell, B.A., Wallace, D.C., Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 4820–4825.
52. [52] Zorov, D.B., Filburn, C.R., Klotz, L.O., Zweier, J.L., Sollott, S.J., Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J. Exp. Med. 192 (2000), 1001–1014.
53. [53] Volkow, N.D., Wang, G.J., Fowler, J.S., Hitzemann, R., Pappas, N., Pascani, K., Wong, C., Gender differences in cerebellar metabolism: test-retest reproducibility. Am. J. Psychiatry 154 (1997), 119–121.
54. [54] Kornack, D.R., Lu, B., Black, I.B., Sexually dimorphic expression of the NGF receptor gene in the developing rat brain. Brain Res. 542 (1991), 171–174.
55. [55] Llewellyn, K.J., Nalbandian, A., Gomez, A., Wei, D., Walker, N., Kimonis, V.E., Administration of CoQ10 analogue ameliorates dysfunction of the mitochondrial respiratory chain in a mouse model of Angelman syndrome. Neurobiol. Dis. 76 (2015), 77–86.
56. [56] Giedd, J.N., Snell, J.W., Lange, N., Rajapakse, J.C., Casey, B.J., Kozuch, P.L., Vaituzis, A.C., Vauss, Y.C., Hamburger, S.D., Kaysen, D., Rapoport, J.L., Quantitative magnetic resonance imaging of human brain development: ages 4–18. Cereb. Cortex 6 (1996), 551–560.
57. [57] Yamamoto, M., Wada, N., Kitabatake, Y., Watanabe, D., Anzai, M., Yokoyama, M., Teranishi, Y., Nakanishi, S., Reversible suppression of glutamatergic neurotransmission of cerebellar granule cells in vivo by genetically manipulated expression of tetanus neurotoxin light chain. J. Neurosci. 12 (2003), 6759–6767.
58. [58] Hadj-Sahraoui, N., Frederic, F., Delhaye-Bouchaud, N., Mariani, J., Gender effect on Purkinje cell loss in the cerebellum of the heterozygous reeler mouse. J. Neurogenet. 11 (1996), 45–58.
59. [59] Durham, J.L., Jordan, K.A., Devos, M.J., Williams, E.K., Sandstrom, N.J., Estradiol protects against hippocampal damage and impairments in fear conditioning resulting from transient global ischemia in mice. Brain Res. 1443 (2012), 64–74.
60. [60] Madeira, M.D., Lieberman, A.R., Sexual dimorphism in the mammalian limbic system. Prog. Neurobiol. 45 (1995), 275–333.
61. [61] Bowers, J.M., Waddell, J., McCarthy, M.M., A developmental sex difference in hippocampal neurogenesis is mediated by endogenous oestradiol. Biol. Sex Differ., 1, 2010, 8, 10.1186/2042-6410-1-8.
62. [62] Smith, M.D., Jones, L.S., Wilson, M.A., Sex differences in hippocampal slice excitability: role of testosterone. Neuroscience 109 (2002), 517–530.
63. [63] Astur, R.S., Ortiz, M.L., Sutherland, R.J., A characterization of performance by men and women in a virtual Morris water task: a large and reliable sex difference. Behav. Brain Res. 93 (1998), 185–190.
64. [64] Dahchour, A., De Witte, P., Effect of repeated ethanol withdrawal on glutamate microdialysate in the hippocampus. Alcohol Clin. Exp. Res. 23 (1999), 1698–1703.
65. [65] Dahchour, A., De Witte, P., Effects of acamprosate on excitatory amino acids during multiple ethanol withdrawal periods. Alcohol Clin. Exp. Res. 27 (2003), 465–470.
66. [66] Nagy, J., Muller, F., Laszlo, L., Cytotoxic effect of alcohol-withdrawal on primary cultures of cortical neurones. Drug Alcohol Depend. 61 (2001), 155–162.
67. [67] Prendergast, M.A., Harris, B.R., Mullholland, P.J., Blanchard, J.A. 2nd, Gibson, D.A., Holley, R.C., Littleton, J.M., Hippocampal CA1 region neurodegeneration produced by ethanol withdrawal requires activation of intrinsic polysynaptic hippocampal pathways and function of N-methyl-D-aspartate receptors. Neuroscience 124 (2004), 869–877.
68. [68] Wong, M., Moss, R.L., Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J. Neurosci. 12 (1992), 3217–3225.
69. [69] Diaz, F., Cytochrome c oxidase deficiency: patients and animal models. Biochim. Biophys. Acta 1802 (2010), 100–110.
70. [70] Ju, X., Wen, Y., Metzger, D.B., Jung, M.E., The role of p38 in mitochondrial respiration in male and female mice. Neurosci. Lett. 544 (2013), 152–156.