Increased cerebral oxidative damage and decreased antioxidant defenses in ovariectomized and sham-operated rats supplemented with vitamin A

Cell Biology and Toxicology

Volumn 28, Issue 5, 2012, Pages 317-330

  Behr, Guilherme Antonio ^a,b,c   Schnorr, Carlos Eduardo ^a   Simões Pires, André ^a   Da Motta, Leonardo Lisbôa ^a   Frey, Benicio N ^c   Moreira, José Cláudio Fonseca ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b MINISTRY OF EDUCATION OF BRAZIL   (Brazil)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

Behavior; Central nervous system; Menopause; Ovariectomy; Redox profile; Vitamin A

Indexed keywords

CATALASE; RETINOL PALMITATE; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; THIOL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; ATROPHY; BRAIN INJURY; CONTROLLED STUDY; DRUG MEGADOSE; EXPLORATORY BEHAVIOR; FEMALE; FRONTAL CORTEX; HIPPOCAMPUS; HYPOTHALAMUS; LOCOMOTION; NONHUMAN; OVARIECTOMY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; UTERINE ATROPHY; VITAMIN SUPPLEMENTATION;

RATTUS;

EID: 84866527289     PISSN: 07422091     EISSN: 15736822     Source Type: Journal    
DOI: 10.1007/s10565-012-9226-x     Document Type: Article

References (83)

1. Abbas AM, Elsamanoudy AZ. Effects of 17beta-estradiol and antioxidant administration on oxidative stress and insulin resistance in ovariectomized rats. Can J Physiol Pharmacol. 2011;89:497-504.
2. Acosta JI, Mayer L, Talboom JS, Tsang CW, Smith CJ, Enders CK, et al. Transitional versus surgical menopause in a rodent model: Etiology of ovarian hormone loss impacts memory and the acetylcholine system. Endocrinology. 2009;150:4248-59.
3. Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121-6.
4. Agarwal A, Gupta S, Sekhon L, Shah R. Redox considerations in female reproductive function and assisted reproduction: From molecular mechanisms to health implications. Antioxid Redox Signal. 2008;10:1375-403.
5. Behr GA, Schnorr CE, Moreira JC. Increased blood oxidative stress in experimental menopause rat model: The effects of vitamin A low-dose supplementation upon antioxidant status in bilateral ovariectomized rats. Fundam Clin Pharmacol. 2012;26:235-49.
6. Berk M, Kapczinski F, Andreazza AC, Dean OM, Giorlando F, Maes M, et al. Pathways underlying neuroprogression in bipolar disorder: Focus on inflammation, oxidative stress and neurotrophic factors. Neurosci Biobehav Rev. 2011;35:804-17.
7. Bhuiyan MS, Fukunaga K. Characterization of an animal model of postmenopausal cardiac hypertrophy and novel mechanisms responsible for cardiac decompensation using ovariectomized pressure-overloaded rats. Menopause. 2010;17:213-21.
8. Borrelli F, Ernst E. Alternative and complementary therapies for the menopause. Maturitas. 2010;66:333-43.
9. Bowe J, Li XF, Kinsey-Jones J, Heyerick A, Brain S, Milligan S, et al. The hop phytoestrogen, 8-prenylnaringenin, reverses the ovariectomy-induced rise in skin temperature in an animal model of menopausal hot flushes. J Endocrinol. 2006;191:399-405.
10. Boyes WK, Dourson ML, Patterson J, Tilson HA, Sette WF, MacPhail RC, et al. EPA's neurotoxicity risk assessment guidelines. Fundam Appl Toxicol. 1997;40:175-84.
11. Bremner JD, Shearer KD, McCaffery PJ. Retinoic acid and affective disorders: The evidence for an association. J Clin Psychiatry. 2012;73:37-50.
12. Caire-Juvera G, Ritenbaugh C, Wactawski-Wende J, Snetselaar LG, Chen Z. Vitamin A and retinol intakes and the risk of fractures among participants of theWomen's Health Initiative Observational Study. Am J Clin Nutr. 2009;89:323-30.
13. Cheng S, Frank LM. New experiences enhance coordinated neural activity in the hippocampus. Neuron. 2008;57:303-13.
14. Chernoff R. Micronutrient requirements in older women. Am J Clin Nutr. 2005;81:1240S-5S.
15. Cruz-Aguado R, Almaguer-Melian W, Diaz CM, Lorigados L, Bergado J. Behavioral and biochemical effects of glutathione depletion in the rat brain. Brain Res Bull. 2001;55:327-33.
16. de Oliveira MR, Silvestrin RB, Mello EST, Moreira JC. Oxidative stress in the hippocampus, anxiety-like behavior and decreased locomotory and exploratory activity of adult rats: Effects of sub acute vitamin A supplementation at therapeutic doses. Neurotoxicology. 2007;28:1191-9.
17. de Oliveira MR, Silvestrin RB, Mello e Souza T, Moreira JC. Therapeutic vitamin A doses increase the levels of markers of oxidative insult in substantia nigra and decrease locomotory and exploratory activity in rats after acute and chronic supplementation. Neurochem Res. 2008;33:378-83.
18. de Oliveira MR, Oliveira MW, Behr GA, Hoff ML, da Rocha RF, Moreira JC. Evaluation of the effects of vitamin A supplementation on adult rat substantia nigra and striatum redox and bioenergetic states: Mitochondrial impairment, increased 3-nitrotyrosine and alpha-synuclein, but decreased D2 receptor contents. Prog Neuropsychopharmacol Biol Psychiatry. 2009a;33:353-62.
19. de Oliveira MR, OliveiraMW, Behr GA, Moreira JC. Vitamin A supplementation at clinical doses induces a dysfunction in the redox and bioenergetics states, but did change neither caspases activities nor TNF-alpha levels in the frontal cortex of adult Wistar rats. J Psychiatr Res. 2009b;43:754-62.
20. de Oliveira MR, Soares Oliveira MW, Muller Hoff ML, Behr GA, da Rocha RF, Fonseca Moreira JC. Evaluation of redox and bioenergetics states in the liver of vitamin A-treated rats. Eur J Pharmacol. 2009c;610:99-105.
21. de Oliveira MR, Oliveira MW, Da Rocha RF, Moreira JC. Vitamin A supplementation at pharmacological doses induces nitrosative stress on the hypothalamus of adult Wistar rats. Chem Biol Interact. 2009d;180:407-13.
22. de Oliveira MR, Lorenzi R, Schnorr CE, MorroneM,Moreira JC. Increased 3-nitrotyrosine levels in mitochondrial membranes and impaired respiratory chain activity in brain regions of adult female rats submitted to daily vitamin A supplementation for 2 months. Brain Res Bull. 2011;86:246-53.
23. Dennehy C, Tsourounis C. A review of select vitamins and minerals used by postmenopausal women. Maturitas. 2010;66:370-80.
24. Dilek M, Naziroglu M, Baha Oral H, Suat Ovey I, Kucukayaz M, Mungan MT, et al. Melatonin modulates hippocampus NMDA receptors, blood and brain oxidative stress levels in ovariectomized rats. J Membr Biol. 2010;233:135-42.
25. Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990;186:421-31.
26. Dresch MT, Rossato SB, Kappel VD, Biegelmeyer R, Hoff ML, Mayorga P, et al. Optimization and validation of an alternative method to evaluate total reactive antioxidant potential. Anal Biochem. 2009;385:107-14.
27. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959;82:70-7.
28. Epa US. Guidelines for neurotoxicity risk assessment. Federal Register. 1998;63:29.
29. Feng Z, Zhang JT. Long-term melatonin or 17beta-estradiol supplementation alleviates oxidative stress in ovariectomized adult rats. Free Radic Biol Med. 2005;39:195-204.
30. Feskanich D, Singh V, Willett WC, Colditz GA. Vitamin A intake and hip fractures among postmenopausal women. JAMA. 2002;287:47-54.
31. Flanagan-Cato LM. Estrogen-induced remodeling of hypothalamic neural circuitry. Front Neuroendocrinol. 2000;21:309-29.
32. Freeman EW, Guthrie KA, Caan B, Sternfeld B, Cohen LS, Joffe H, et al. Efficacy of escitalopram for hot flashes in healthy menopausal women: A randomized controlled trial. JAMA. 2011;305:267-74.
33. Frey BN, Lord C, Soares CN. Depression during menopausal transition: A review of treatment strategies and pathophysiological correlates. Menopause Int. 2008;14:123-8.
34. Frey BN, Hall GB, Attard S, Yucel K, Skelin I, Steiner M, Soares CN. Shift in the brain network of emotional regulation in midlife women: Is the menopausal transition the turning point? Menopause. 2010;17:840-5.
35. Gao B, Klumpen HJ, Gurney H. Dose calculation of anticancer drugs. Expert Opin Drug Metab Toxicol. 2008;4:1307-19.
36. Gatica L, Alvarez S, Gomez N, Zago MP, Oteiza P, Oliveros L, et al. Vitamin A deficiency induces prooxidant environment and inflammation in rat aorta. Free Radic Res. 2005;39:621-8.
37. Goss PE, Qi S, Hu H, Cheung AM. The effects of atamestane and toremifene alone and in combination comparedwith letrozole on bone, serum lipids and the uterus in an ovariectomized rat model. Breast Cancer Res Treat. 2007;103:293-302.
38. Gracia CR, Sammel MD, Freeman EW, Lin H, Langan E, Kapoor S, et al. Defining menopause status: Creation of a new definition to identify the early changes of the menopausal transition. Menopause. 2005;12:128-35.
39. Graziottin A, Serafini A. Depression and the menopause: Why antidepressants are not enough? Menopause Int. 2009;15:76-81.
40. Hagey AR, Warren MP. Role of exercise and nutrition in menopause. Clin Obstet Gynecol. 2008;51:627-41.
41. Halliwell B. Biochemistry of oxidative stress. Biochem Soc Trans. 2007;35:1147-50.
42. Harlow BL, Wise LA, Otto MW, Soares CN, Cohen LS. Depression and its influence on reproductive endocrine and menstrual cycle markers associated with perimenopause: TheHarvard study ofmoods and cycles. Arch Gen Psychiatry. 2003;60:29-36.
43. Huang YH, Zhang QH. Genistein reduced the neural apoptosis in the brain of ovariectomised rats bymodulatingmitochondrial oxidative stress. Br J Nutr. 2010;104:1297-303.
44. Irwin RW, Yao J, Ahmed SS, Hamilton RT, Cadenas E, Brinton RD. Medroxyprogesterone acetate antagonizes estrogen up-regulation of brain mitochondrial function. Endocrinology. 2011;152:556-67.
45. Jensen EV, Jacobson HI, Walf AA, Frye CA. Estrogen action: A historic perspective on the implications of considering alternative approaches. Physiol Behav. 2010;99:151-62.
46. Kennedy E,Meyers L. Dietary reference intakes: Development and uses for assessment of micronutrient status of women-a global perspective. Am J Clin Nutr. 2005;81:1194S-7S.
47. Kesner RP, Churchwell JC. An analysis of rat prefrontal cortex in mediating executive function. Neurobiol Learn Mem. 2011;96:417-31.
48. Koppenol WH. The Haber-Weiss cycle-70 years later. Redox Rep. 2001;6:229-34.
49. Kupferer EM, Dormire SL, Becker H. Complementary and alternative medicine use for vasomotor symptoms among women who have discontinued hormone therapy. J Obstet Gynecol Neonatal Nurs. 2009;38:50-9.
50. Lee YM, Cheng PY, Hong SF, Chen SY, Lam KK, Sheu JR, et al. Oxidative stress induces vascular heme oxygenase-1 expression in ovariectomized rats. Free Radic Biol Med. 2005;39:108-17.
51. Lee SD, Kuo WW, Ho YJ, Lin AC, Tsai CH, Wang HF, et al. Cardiac Fas-dependent and mitochondria-dependent apoptosis in ovariectomized rats. Maturitas. 2008;61:268-77.
52. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990;186:464-78.
53. Lissi E, Pascual C, Del Castillo MD. Luminol luminescence induced by 2,2′-azo-bis(2-amidinopropane) thermolysis. Free Radic Res Commun. 1992;17:299-311.
54. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265-75.
55. Martins DB, Mazzanti CM, Franca RT, Pagnoncelli M, Costa MM, de Souza EM, et al. 17-beta estradiol in the acetylcholinesterase activity and lipid peroxidation in the brain and blood of ovariectomized adult and middle-aged rats. Life Sci. 2012;90:351-9.
56. McCaffery PJ, Adams J, Maden M, Rosa-Molinar E. Too much of a good thing: Retinoic acid as an endogenous regulator of neural differentiation and exogenous teratogen. Eur JNeurosci. 2003;18:457-72.
57. Merzoug S, Toumi ML, Boukhris N, Baudin B, Tahraoui A. Adriamycin-related anxiety-like behavior, brain oxidative stress and myelotoxicity in male Wistar rats. Pharmacol Biochem Behav. 2011;99:639-47.
58. Miquel J, Ramirez-Bosca A, Ramirez-Bosca JV, Alperi JD. Menopause: A review on the role of oxygen stress and favorable effects of dietary antioxidants. Arch Gerontol Geriatr. 2006;42:289-306.
59. Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247:3170-5.
60. Monteiro SC, Matte C, Delwing D, Wyse AT. Ovariectomy increases Na+, K+-ATPase, acetylcholinesterase and catalase in rat hippocampus. Mol Cell Endocrinol. 2005;236:9-16.
61. Moylan S, Maes M, Wray NR, Berk M. The neuroprogressive nature of major depressive disorder: Pathways to disease evolution and resistance, and therapeutic implications. Mol Psychiatry. 2012 (in press).
62. Muthusami S, Ramachandran I, Muthusamy B, Vasudevan G, Prabhu V, Subramaniam V, et al. Ovariectomy induces oxidative stress and impairs bone antioxidant system in adult rats. Clin Chim Acta. 2005;360:81-6.
63. Ozgonul M, Oge A, Sezer ED, Bayraktar F, Sozmen EY. The effects of estrogen and raloxifene treatment on antioxidant enzymes in brain and liver of ovarectomized female rats. Endocr Res. 2003;29:183-9.
64. Pasquali MA, Gelain DP, de Oliveira MR, Behr GA, da Motta LL, da Rocha RF, et al. Vitamin A supplementation for different periods alters oxidative parameters in lungs of rats. J Med Food. 2009;12:1375-80.
65. Pasquali MA, Schnorr CE, Feistauer LB, Gelain DP, Moreira JC. Vitamin A supplementation to pregnant and breastfeeding female rats induces oxidative stress in the neonatal lung. Reprod Toxicol. 2010;30:452-6.
66. Phillips GB, Pinkernell BH, Jing TY. Relationship between serum sex hormones and coronary artery disease in postmenopausal women. Arterioscler Thromb Vasc Biol. 1997;17:695-701.
67. Prut L, Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: A review. Eur J Pharmacol. 2003;463:3-33.
68. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008;22:659-61.
69. RoccaWA, Grossardt BR, Shuster LT. Oophorectomy, menopause, estrogen treatment, and cognitive aging: Clinical evidence for a window of opportunity. Brain Res. 2011;1379:188-98.
70. Roy EJ, Buyer DR, Licari VA. Estradiol in the striatum: Effects on behavior and dopamine receptors but no evidence for membrane steroid receptors. Brain Res Bull. 1990;25:221-7.
71. Saadeh SA, Baracco R, Jain A, Kapur G, Mattoo TK, Valentini RP. Weight or body surface area dosing of steroids in nephrotic syndrome: Is there an outcome difference? Pediatr Nephrol. 2011;26:2167-71.
72. Sanchez-Rodriguez MA, Zacarias-Flores M, Arronte-Rosales A, Correa-Munoz E, Mendoza-Nunez VM. Menopause as risk factor for oxidative stress. Menopause. 2011;19:361-7.
73. Schnorr CE, da Silva Morrone M, Simoes-Pires A, da Rocha RF, Behr GA, Moreira JC. Vitamin A supplementation in rats under pregnancy and nursing induces behavioral changes and oxidative stress upon striatum and hippocampus of dams and their offspring. Brain Res. 2011a;1369:60-73.
74. Schnorr CE, Morrone Mda S, Weber MH, Lorenzi R, Behr GA, Moreira JC. The effects of vitamin A supplementation to rats during gestation and lactation upon redox parameters: Increased oxidative stress and redox modulation in mothers and their offspring. Food Chem Toxicol. 2011b;49:2645-54.
75. Shepherd GM. Behaviour: Smells, brains and hormones. Nature. 2006;439:149-51.
76. Soules MR, Sherman S, Parrott E, Rebar R, Santoro N, UtianW, et al. Stages of Reproductive Aging Workshop (STRAW). J Womens Health Gend Based Med. 2001;10:843-8.
77. Thompson EA. Alternative and complementary therapies for the menopause: A homeopathic approach. Maturitas. 2010;66:350-4.
78. Vukovic J, Blackmore DG, Jhaveri D, Bartlett PF. Activation of neural precursors in the adult neurogenic niches. Neurochem Int. 2011;59:341-6.
79. Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc. 2007a;2:322-8.
80. Walf AA, Frye CA. Administration of estrogen receptor betaspecific selective estrogen receptor modulators to the hippocampus decrease anxiety and depressive behavior of ovariectomized rats. Pharmacol Biochem Behav. 2007b;86:407-14.
81. Waters EM, Mitterling K, Spencer JL, Mazid S, McEwen BS, Milner TA. Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus. Brain Res. 2009;1290:1-11.
82. Wong VC, Lim CE, Luo X, Wong WS. Current alternative and complementary therapies used in menopause. Gynecol Endocrinol. 2009;25:166-74.
83. Ziaei S, Kazemnejad A, Zareai M. The effect of vitamin E on hot flashes in menopausal women. Gynecol Obstet Invest. 2007;64:204-7.