Protective Role of Endogenous Ovarian Hormones Against Learning and Memory Impairments and Brain Tissues Oxidative Damage Induced by Lipopolysaccharide

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To Cite : Pourganji M, Hosseini M, Soukhtanloo M, Zabihi H, Hadjzadeh M A. et al. Protective Role of Endogenous Ovarian Hormones Against Learning and Memory Impairments and Brain Tissues Oxidative Damage Induced by Lipopolysaccharide, Iran Red Crescent Med J. 2014 ;16(3):e13954. doi: 10.5812/ircmj.13954.
Abstract
1. Background
2. Objectives
3. Materials and Methods
4. Results
5. Discussion
Acknowledgements
Footnotes
References
  • 1. Mangialasche F, Kivipelto M, Solomon A, Fratiglioni L. Dementia prevention: current epidemiological evidence and future perspective. Alzheimers Res Ther. 2012; 4(1): 6[DOI][PubMed]
  • 2. Bedell HE. Directionalization of visual targets during involuntary eye movement. Optom Vis Sci. 1990; 67(8): 583-9[PubMed]
  • 3. Geldmacher DS. Treatment guidelines for Alzheimer's disease: redefining perceptions in primary care. Prim Care Companion J Clin Psychiatry. 2007; 9(2): 113-21[PubMed]
  • 4. Cornil CA, Ball GF, Balthazart J. Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res. 2006; 1126(1): 2-6[DOI][PubMed]
  • 5. Mehra RD, Sharma K, Nyakas C, Vij U. Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study. Brain Res. 2005; 1056(1): 22-35[DOI][PubMed]
  • 6. Joffe H, Hall JE, Gruber S, Sarmiento IA, Cohen LS, Yurgelun-Todd D, et al. Estrogen therapy selectively enhances prefrontal cognitive processes: a randomized, double-blind, placebo-controlled study with functional magnetic resonance imaging in perimenopausal and recently postmenopausal women. Menopause. 2006; 13(3): 411-22[DOI][PubMed]
  • 7. Good M, Day M, Muir JL. Cyclical changes in endogenous levels of oestrogen modulate the induction of LTD and LTP in the hippocampal CA1 region. Eur J Neurosci. 1999; 11(12): 4476-80[PubMed]
  • 8. Warren SG, Humphreys AG, Juraska JM, Greenough WT. LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res. 1995; 703(1–2): 26-30[DOI]
  • 9. Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J Neurosci. 1997; 17(5): 1848-59[PubMed]
  • 10. Romeo RD, McCarthy JB, Wang A, Milner TA, McEwen BS. Sex differences in hippocampal estradiol-induced N-methyl-D-aspartic acid binding and ultrastructural localization of estrogen receptor-alpha. Neuroendocrinology. 2005; 81(6): 391-9[DOI][PubMed]
  • 11. Weitz TM, Town T. Microglia in Alzheimer's Disease: It's All About Context. Int J Alzheimers Dis. 2012; 2012: 314185[DOI][PubMed]
  • 12. Akiyama H, Arai T, Kondo H, Tanno E, Haga C, Ikeda K. Cell mediators of inflammation in the Alzheimer disease brain. Alzheimer Dis Assoc Disord. 2000; 14 Suppl 1-53[PubMed]
  • 13. Schlachetzki JC, Hull M. Microglial activation in Alzheimer's disease. Curr Alzheimer Res. 2009; 6(6): 554-63[PubMed]
  • 14. Sardi F, Fassina L, Venturini L, Inguscio M, Guerriero F, Rolfo E, et al. Alzheimer's disease, autoimmunity and inflammation. The good, the bad and the ugly. Autoimmun Rev. 2011; 11(2): 149-53
  • 15. Verri M, Pastoris O, Dossena M, Aquilani R, Guerriero F, Cuzzoni G, et al. Mitochondrial alterations, oxidative stress and neuroinflammation in Alzheimer's disease. Int J Immunopathol Pharmacol. 2011; 25(2): 345-53
  • 16. Henry CJ, Huang Y, Wynne AM, Godbout JP. Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1beta and anti-inflammatory IL-10 cytokines. Brain Behav Immun. 2009; 23(3): 309-17[DOI][PubMed]
  • 17. Morihara T, Teter B, Yang F, Lim GP, Boudinot S, Boudinot FD, et al. Ibuprofen suppresses interleukin-1beta induction of pro-amyloidogenic alpha1-antichymotrypsin to ameliorate beta-amyloid (Abeta) pathology in Alzheimer's models. Neuropsychopharmacology. 2005; 30(6): 1111-20[DOI][PubMed]
  • 18. Cole GM, Morihara T, Lim GP, Yang F, Begum A, Frautschy SA. NSAID and antioxidant prevention of Alzheimer's disease: lessons from in vitro and animal models. Ann N Y Acad Sci. 2004; 1035: 68-84[DOI][PubMed]
  • 19. Song C, Horrobin D. Omega-3 fatty acid ethyl-eicosapentaenoate, but not soybean oil, attenuates memory impairment induced by central IL-1beta administration. J Lipid Res. 2004; 45(6): 1112-21[DOI][PubMed]
  • 20. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science. 2003; 302(5651): 1760-5[DOI][PubMed]
  • 21. Hritcu L, Ciobica A, Stefan M, Mihasan M, Palamiuc L, Nabeshima T. Spatial memory deficits and oxidative stress damage following exposure to lipopolysaccharide in a rodent model of Parkinson's disease. Neurosci Res. 2011; 71(1): 35-43
  • 22. Vegeto E, Bonincontro C, Pollio G, Sala A, Viappiani S, Nardi F, et al. Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. J Neurosci. 2001; 21(6): 1809-18[PubMed]
  • 23. Smith JA, Das A, Butler JT, Ray SK, Banik NL. Estrogen or estrogen receptor agonist inhibits lipopolysaccharide induced microglial activation and death. Neurochem Res. 2011; 36(9): 1587-93[DOI][PubMed]
  • 24. Behl C, Moosmann B. Antioxidant neuroprotection in Alzheimer’s disease as preventive and therapeutic approach. Free Radic Biol Med. 2002; 33(2): 182-91[DOI]
  • 25. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ, et al. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol. 1997; 51(4): 535-41[PubMed]
  • 26. Behl C, Widmann M, Trapp T, Holsboer F. 17-beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem Biophys Res Commun. 1995; 216(2): 473-82[DOI][PubMed]
  • 27. Green PS, Gridley KE, Simpkins JW. Nuclear estrogen receptor-independent neuroprotection by estratrienes: a novel interaction with glutathione. Neurosci. 1998; 84(1): 7-10[DOI]
  • 28. Hosseini M, Sadeghnia HR, Salehabadi S, Alavi H, Gorji A. The effect of L-arginine and L-NAME on pentylenetetrazole induced seizures in ovariectomized rats, an in vivo study. Seizure. 2009; 18(10): 695-8[DOI][PubMed]
  • 29. Wagner AK, Willard LA, Kline AE, Wenger MK, Bolinger BD, Ren D, et al. Evaluation of estrous cycle stage and gender on behavioral outcome after experimental traumatic brain injury. Brain Res. 2004; 998(1): 113-21[PubMed]
  • 30. Naghibi SM, Hosseini M, Khani F, Rahimi M, Vafaee F, Rakhshandeh H, et al. Effect of Aqueous Extract of Crocus sativus L. on Morphine-Induced Memory Impairment. Adv Pharmacol Sci. 2012; 2012: 494367[DOI][PubMed]
  • 31. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959; 82(1): 70-7[DOI]
  • 32. Hosseinzadeh H, Sadeghnia HR. Safranal, a constituent of Crocus sativus (saffron), attenuated cerebral ischemia induced oxidative damage in rat hippocampus. J Pharm Pharm Sci. 2005; 8(3): 394-9[PubMed]
  • 33. Janero DR. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med. 1990; 9(6): 515-40[DOI]
  • 34. Sharma JB, Sharma A, Bahadur A, Vimala N, Satyam A, Mittal S. Oxidative stress markers and antioxidant levels in normal pregnancy and pre-eclampsia. Int J Gynaecol Obstet. 2006; 94(1): 23-7[DOI][PubMed]
  • 35. Hosseini M, Hadjzadeh MA, Derakhshan M, Havakhah S, Rassouli FB, Rakhshandeh H, et al. The beneficial effects of olibanum on memory deficit induced by hypothyroidism in adult rats tested in Morris water maze. Arch Pharm Res. 2010; 33(3): 463-8[DOI][PubMed]
  • 36. Saffarzadeh F, Eslamizade MJ, Nemati Karimooy HA, Hadjzadeh MA, Khazaei M, Hosseini M. The effect of L-arginine on Morris water maze tasks of ovariectomized rats. Acta Physiol Hung. 2010; 97(2): 216-23[DOI][PubMed]
  • 37. Singh M, Meyer EM, Millard WJ, Simpkins JW. Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res. 1994; 644(2): 305-12[DOI]
  • 38. Azizi-Malekabadi H, Hosseini M, Soukhtanloo M, Sadeghian R, Fereidoni M, Khodabandehloo F. Different effects of scopolamine on learning, memory, and nitric oxide metabolite levels in hippocampal tissues of ovariectomized and Sham-operated rats. Arq Neuropsiquiatr. 2012; 70(6): 447-52
  • 39. Markham JA, Pych JC, Juraska JM. Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm Behav. 2002; 42(3): 284-93[PubMed]
  • 40. Bimonte HA, Denenberg VH. Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology. 1999; 24(2): 161-73[DOI]
  • 41. El-Bakri NK, Islam A, Zhu S, Elhassan A, Mohammed A, Winblad B, et al. Effects of estrogen and progesterone treatment on rat hippocampal NMDA receptors: relationship to Morris water maze performance. J Cell Mol Med. 2004; 8(4): 537-44[PubMed]
  • 42. Weiland NG. Estradiol selectively regulates agonist binding sites on the N-methyl-D-aspartate receptor complex in the CA1 region of the hippocampus. Endocrinology. 1992; 131(2): 662-8[DOI][PubMed]
  • 43. Cyr M, Ghribi O, Di Paolo T. Regional and selective effects of oestradiol and progesterone on NMDA and AMPA receptors in the rat brain. J Neuroendocrinol. 2000; 12(5): 445-52[PubMed]
  • 44. Chesler EJ, Juraska JM. Acute administration of estrogen and progesterone impairs the acquisition of the spatial morris water maze in ovariectomized rats. Horm Behav. 2000; 38(4): 234-42[DOI][PubMed]
  • 45. Galea LA, Kavaliers M, Ossenkopp KP, Hampson E. Gonadal hormone levels and spatial learning performance in the Morris water maze in male and female meadow voles, Microtus pennsylvanicus. Horm Behav. 1995; 29(1): 106-25[DOI][PubMed]
  • 46. Sherwin BB. Estrogen and cognitive functioning in women. Endocr Rev. 2003; 24(2): 133-51[DOI][PubMed]
  • 47. Huh K, Shin US, Choi JW, Lee SI. Effect of sex hormones on lipid peroxidation in rat liver. Arch Pharm Res. 1994; 17(2): 109-14[PubMed]
  • 48. Lacort M, Leal AM, Liza M, Martin C, Martinez R, Ruiz-Larrea MB. Protective effect of estrogens and catecholestrogens against peroxidative membrane damage in vitro. Lipids. 1995; 30(2): 141-6[PubMed]
  • 49. Niki E, Nakano M. Methods in Enzymology. 1990; : 330-3[DOI]
  • 50. Green PS, Gordon K, Simpkins JW. Phenolic A ring requirement for the neuroprotective effects of steroids. J Steroid Biochem Mol Biol. 1997; 63(4–6): 229-35[DOI]
  • 51. Miller CP, Jirkovsky I, Hayhurst DA, Adelman SJ. In vitro antioxidant effects of estrogens with a hindered 3-OH function on the copper-induced oxidation of low density lipoprotein. Steroid. 1996; 61(5): 305-8[DOI]
  • 52. Prokai L, Oon SM, Prokai-Tatrai K, Abboud KA, Simpkins JW. Synthesis and biological evaluation of 17beta-alkoxyestra-1,3, 5(10)-trienes as potential neuroprotectants against oxidative stress. J Med Chem. 2001; 44(1): 110-4[PubMed]
  • 53. Aspestrand F, Tofte AJ, Igesund A. [The value of computer tomography in assessing operability in advanced bladder cancer]. Tidsskr Nor Laegeforen. 1981; 101(26): 1445-7[PubMed]
  • 54. Esser K. [The phenoloxydases of the ascomycete Podospora anserina. 3. Quantitative and qualitative enzyme differences after mutation in non-linked loci]. Z Vererbungsl. 1966; 97(4): 327-44[PubMed]
  • 55. Monteiro SC, Matte C, Bavaresco CS, Netto CA, Wyse AT. Vitamins E and C pretreatment prevents ovariectomy-induced memory deficits in water maze. Neurobiol Learn Mem. 2005; 84(3): 192-9[DOI][PubMed]
  • 56. Sato T, Teramoto T, Tanaka K, Ohnishi Y, Irifune M, Nishikawa T. Effects of ovariectomy and calcium deficiency on learning and memory of eight-arm radial maze in middle-aged female rats. Behav Brain Res. 2003; 142(1–2): 207-16[DOI]
  • 57. 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(1-3): 135-42[DOI][PubMed]
  • 58. Naziroglu M, Simsek M, Simsek H, Aydilek N, Ozcan Z, Atilgan R. The effects of hormone replacement therapy combined with vitamins C and E on antioxidants levels and lipid profiles in postmenopausal women with Type 2 diabetes. Clin Chim Acta. 2004; 344(1-2): 63-71[DOI][PubMed]
  • 59. Kuyumcu ME, Yesil Y, Ozturk ZA, Kizilarslanoglu C, Etgul S, Halil M, et al. The evaluation of neutrophil-lymphocyte ratio in Alzheimer's disease. Dement Geriatr Cogn Disord. 2012; 34(2): 69-74[DOI][PubMed]
  • 60. Johnston H, Boutin H, Allan SM. Assessing the contribution of inflammation in models of Alzheimer's disease. Biochem Soc Trans. 2011; 39(4): 886-90[DOI][PubMed]
  • 61. Pugh CR, Kumagawa K, Fleshner M, Watkins LR, Maier SF, Rudy JW. Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain Behav Immun. 1998; 12(3): 212-29[DOI][PubMed]
  • 62. Cacquevel M, Lebeurrier N, Cheenne S, Vivien D. Cytokines in neuroinflammation and Alzheimer's disease. Curr Drug Targets. 2004; 5(6): 529-34[PubMed]
  • 63. Metoki K, Hommes FA. The pH of mitochondria of fibroblasts from a hyperornithinaemia, hyperammonaemia, homocitrullinuria-syndrome patient. J Inherit Metab Dis. 1984; 7(1): 9-11[PubMed]
  • 64. Bilbo SD, Biedenkapp JC, Der-Avakian A, Watkins LR, Rudy JW, Maier SF. Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition. J Neurosci. 2005; 25(35): 8000-9[DOI][PubMed]
  • 65. Cui CA, Jin DQ, Hwang YK, Lee IS, Hwang JK, Ha I, et al. Macelignan attenuates LPS-induced inflammation and reduces LPS-induced spatial learning impairments in rats. Neurosci Lett. 2008; 448(1): 110-4[DOI][PubMed]
  • 66. Singh AK, Jiang Y. How does peripheral lipopolysaccharide induce gene expression in the brain of rats? Toxicology. 2004; 201(1-3): 197-207[DOI][PubMed]
  • 67. Lante F, Meunier J, Guiramand J, De Jesus Ferreira MC, Cambonie G, Aimar R, et al. Late N-acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation. Hippocampus. 2008; 18(6): 602-9[DOI][PubMed]
  • 68. Bokov AF, Ko D, Richardson A. The effect of gonadectomy and estradiol on sensitivity to oxidative stress. Endocr Res. 2009; 34(1-2): 43-58[DOI][PubMed]
  • 69. Tang XL, Liu XJ, Tian Q, Zhang W. Dynamic oxidative stress and DNA damage induced by oestrogen deficiency and protective effects of puerarin and 17beta-oestradiol in ovariectomized rats. Basic Clin Pharmacol Toxicol. 2012; 111(2): 87-91[DOI][PubMed]
  • 70. Giddabasappa A, Bauler M, Yepuru M, Chaum E, Dalton JT, Eswaraka J. 17-beta estradiol protects ARPE-19 cells from oxidative stress through estrogen receptor-beta. Invest Ophthalmol Vis Sci. 2010; 51(10): 5278-87[DOI][PubMed]
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