Estradiol prevents olfactory dysfunction induced by A-β 25-35 injection in hippocampus

BMC Neuroscience

Volumn 14, Issue , 2013, Pages

  Bernal Mondragón, Carlos ^a   Rivas Arancibia, Selva ^a   Kendrick, Keith M ^b   Guevara Guzmán, Rosalinda ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF ELECTRONIC SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

Alzheimer's disease; Amyloid beta; Estrogen; Neurodegeneration; Neuroprotection; Olfactory disfunction

Indexed keywords

AMYLOID BETA PROTEIN[25-35]; ESTRADIOL; NEUROPROTECTIVE AGENT;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; HIPPOCAMPAL CA1 REGION; LIPID PEROXIDATION; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OXIDATIVE STRESS; RAT; SMELLING; SMELLING DISORDER; SPATIAL MEMORY; WESTERN BLOTTING;

AMYLOID BETA-PEPTIDES; ANIMALS; BLOTTING, WESTERN; CA1 REGION, HIPPOCAMPAL; ESTRADIOL; FEMALE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; OLFACTION DISORDERS; OXIDATIVE STRESS; RATS; RATS, WISTAR;

EID: 84884485824     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-14-104     Document Type: Article

References (68)

1. Irvine GB, El-Agnaf OM, Shankar GM, Walsh DM. Protein aggregation in the brain: the molecular basis for Alzheimer's and Parkinson's diseases. Mol Med 2008, 14(7-8):451-464. 2274891, 18368143.
2. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991, 82(4):239-259. 10.1007/BF00308809, 1759558.
3. Talamo BR, Rudel R, Kosik KS, Lee VM, Neff S, Adelman L, Kauer JS. Pathological changes in olfactory neurons in patients with Alzheimer's disease. Nature 1989, 337(6209):736-739. 10.1038/337736a0, 2465496.
4. Xu Y, Jack CR, O'Brien PC, Kokmen E, Smith GE, Ivnik RJ, Boeve BF, Tangalos RG, Petersen RC. Usefulness of MRI measures of enthorhinal cortex versus hippocampus in AD. Neurology 2000, 54(9):1760-1767. 10.1212/WNL.54.9.1760, 10802781.
5. Eichenbaum H, Morton TH, Potter H, Corkin S. Selective olfactory deficits in case H.M. Brain 1983, 106(2):459-472. 10.1093/brain/106.2.459, 6850278.
6. Koss E, Weiffenbach JM, Haxby JV, Friedland RP. Olfactory detection and recognition in Alzheimer's disease. Lancet 1987, 1(8533):622.
7. Serby M, Larson P, Kallkstein D. The nature and course of olfactory deficits in Alzheimer's disease. Am J Psychiatry 1991, 148(3):357-360.
8. Devanand DP, Michaels-Marston KS, Liu X, Pelton GH, Padilla M, Marder K, Bell K, Stern Y, Mayeux R. Olfactory deficits in patients with mild cognitive impairment predict Alzheimer's disease at follow-up. Am J Psychiatry 2000, 157(9):1399-1405. 10.1176/appi.ajp.157.9.1399, 10964854.
9. Djordjevic J, Jones-Gotman M, De Sousa K, Chertkow H. Olfaction in patients with mild cognitive impairment and Alzheimer's disease. Neurobiol Aging 2008, 29:693-706. 10.1016/j.neurobiolaging.2006.11.014, 17207898.
10. Tabner BJ, Turnbull S, El-Agnaf OM, Allsop D. Formation of hydrogen peroxide and hydroxyl radicals from A(beta) and alpha-synuclein as a possible mechanism of cell death in Alzheimer's disease and Parkinson's disease. Free Radic Biol Med 2002, 32:1076-1083. 10.1016/S0891-5849(02)00801-8, 12031892.
11. Maccioni RB, Muñoz JP, Barbelto L. The molecular bases of Alzheimer's disease and other neurodegenerative disorders. Arch Med Res 2001, 32(5):367-381. 10.1016/S0188-4409(01)00316-2, 11578751.
12. Gulyaeva NV, Stepanichev MY. Aβ(25-35) as proxyholder for amyloidogenic peptides: in vivo evidence. Exp Neurol 2010, 222:6-9. 10.1016/j.expneurol.2009.12.019, 20043907.
13. Kamisnky YG, Kosenko EA. Effects of amyloid-beta peptides on hydrogen peroxide-metabolizing enzymes in rat brain in vivo. Free Radic Res 2008, 42(6):564-573. 10.1080/10715760802159057, 18569014.
14. Kaminsky YG, Marlatt MW, Smith MA, Kosenko EA. Subcellular and metabolic examination of amyloid-beta peptides in Alzheimer disease pathogenesis: evidence for abeta(25-35). Exp Neurol 2010, 221(1):26-37. 10.1016/j.expneurol.2009.09.005, 19751725.
15. Stepanichev MY, Moiseeva YV, Lazareva NA, Onufriev MV, Gulyaeva NV. Single intracerebroventricular administration of amyloid-beta (25-35) peptide induces impairment in short-term rather thanlong-term memory in rats. Brain Res Bull 2003, 61(2):197-205. 10.1016/S0361-9230(03)00118-7, 12832007.
16. Del Mar M-SM, Villalaín J, Gómez-Fernández JC. Structure of the Alzheimer beta-amyloid peptide (25-35) and its interaction with negatively charged phospholipid vesicles. Eur J Biochem 1999, 265(2):744-753. 10.1046/j.1432-1327.1999.00775.x, 10504406.
17. Iversen LL, Mortishire-Smith RJ, Pollack SJ, Shearman MS. The toxicity in vitro of beta-amyloid protein. Biochem J 1995, 311:1-16. 1136112, 7575439.
18. Terzi E, Hölzemann G, Seelig J. Alzheimer beta-amyloid peptide 25-35: electrostatic interactions with phospholipid membranes. Biochemistry 1994, 33(23):7434-7441. 10.1021/bi00189a051, 8003508.
19. Catricala S, Torti M, Ricevuti G. Alzheimer disease and platelets: how's that relevant. Immun Ageing 2012, 9:20. 10.1186/1742-4933-9-20, 3545835, 22985434.
20. Yankner BA, Dawes LR, Fisher S, Villa-Komaroff L, Oster-Granite ML, Neve RL. Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer's disease. Science 1989, 245:417-420. 10.1126/science.2474201, 2474201.
21. Maurice T, Lockhart BP, Privat A. Amnesia induced in mice by centrally administered beta-amyloid peptides involves cholinergic dysfunction. Brain Res 1996, 706(2):181-193. 10.1016/0006-8993(95)01032-7, 8822355.
22. Delobette S, Privat A, Maurice T. In vitro aggregation facilities beta-amyloid peptide-(25-35)-induced amnesia in the rat. Eur J Pharmacol 1997, 319(1):1-4. 10.1016/S0014-2999(96)00922-3, 9030890.
23. Terranova JP, Kan JP, Storme JJ, Perreaut P, Le Fur G, Soubrié P. Administration of amyloid beta-peptides in the rat medial septum causes memory deficits: reversal by SR 57746A, a non-peptide neurotrophic compound. Neurosci Lett 1996, 213(2):79-82. 10.1016/0304-3940(96)12859-7, 8858613.
24. Klementiev B, Novikova T, Novitskaya V, Walmod PS, Dmytriyeva O, Pakkenberg B, Berezin V, Bock E. A neural cell adhesion molecule-derived peptide reduces neuropathological signs and cognitive impairment induced by Abeta25-35. Neuroscience 2007, 145(1):209-224. 10.1016/j.neuroscience.2006.11.060, 17223274.
25. Mugantseva EA, Podol'skiǐ II. Central administration of the amyloid beta-peptide (25-35) and individual features of cognitive behavior of rats. ZhVyssh Nerv DeiatIm I P Pavlova 2009, 59(5):616-621.
26. Meunier J, Ieni J, Maurice T. The anti-amnesic and neuroprotective effects of donepezil against amyloid b25-35 peptide-induced toxicity in mice involve an interaction with the σ1 receptor. Br J Pharmacol 2006, 149(8):998-1012. 2014636, 17057756.
27. Villard V, Espallergues J, Keller E, Alkam T, Nitta A, Yamada K, Nabeshima T, Vamvakides A, Maurice T. Antiamnesic and neuroprotective effects of the aminotetrahydrofuran derivative ANAVEX1-41 against amyloid beta(25-35)-induced toxicity in mice. Neuropsychopharmacol 2009, 34:1552-1566.
28. Yamaguchi Y, Kawashima S. Effects of amyloid-beta-(25-35) on passive avoidance, radial-arm maze learning and choline acetyltransferase activity in the rat. Eur J Pharmacol 2001, 412:265-272. 10.1016/S0014-2999(01)00730-0, 11166290.
29. Behl C. Oestrogen as a neuroprotective hormone. Nature Rev Neurosci 2002, 3:433-442.
30. Tang MT, Jacobs D, Stern Y, Marder K, Schofield P, Gurland B, Andrews H, Mayeux R. Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 1996, 348:429-432. 10.1016/S0140-6736(96)03356-9, 8709781.
31. Xu H, Gouras GK, Greenfield JP, Vincent B, Naslund J, Mazzarelli L, Fried G, Jovanovic JN, Seeger M, Relkin NR, Liao F, Checler F, Buxbaum JD, Chait BT, Thinakaran G, Sisodia SS, Wang R, Greengard P, Gandy S. Estrogen reduces neuronal generation of Alzheimer A-β 25-35 peptides. Nat Med 1998, 4:447-451. 10.1038/nm0498-447, 9546791.
32. Ayres S, Abplanal W, Liu JH, Subbiah MT. Mechanisms involved in the protective effect of estradiol-17β on lipid peroxidation and DNA damage. Part. Am J Physiol 1998, 274:1002-1008.
33. Harris-White ME, Chu T, Miller SA, Simmons M, Teter B, Nash D, Cole GM, Frautschy SA. Estrogen (E2) and glucocorticoid (Gc) effects on microglia and Aβ clearance in vitro and in vivo. Neurochem Int 2001, 39(5-6):435-448.
34. Paxinos G, Watson C. The rat brain in stereotaxic coordinates 1986, San Diego California: Academic Press INC, 2.
35. Reyes-Guerrero G, Vázquez-García M, Elías-Viñas D, Donatti-Albarrán OA, Guevara-Guzmán R. Effects of 17 β-estradiol and extremely low-frequency electromagnetic fields on social recognition memory in female rats: A possible interaction?. Brain Res 2006, 1:131-138.
36. Larrazolo-López A, Kendrick KM, Aburto-Arciniega M, Arriaga-Ávila V, Morimoto S, Frías M, Guevara-Guzmán R. Vaginocervical stimulation enhances social recognition memory in rats via oxytocin release in the olfactory bulb. Neurosci 2008, 152(3):585-593.
37. Clipperton-Allen AE, Lee AW, Reyes A, Devidze N, Phan A, Pfaff DW, Choleris E. Oxytocin, vasopressin and estrogen receptor gene expression in relation to social recognition in female mice. Physiol Behav 2012, 105(4):915-924. 10.1016/j.physbeh.2011.10.025, 3401543, 22079582.
38. Paolini AG, McKenzie JS. Effects of lesions in the horizontal diagonal band nucleus on olfactory habituation in the rat. Neuroscience 1993, 57(3):717-724. 10.1016/0306-4522(93)90017-A, 8309533.
39. Dember WN, Fowler H. Spontaneous alternation behavior. Psychol Bull 1958, 55(6):412-428.
40. Lalonde R. The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 2002, 26(1):91-104. 10.1016/S0149-7634(01)00041-0, 11835987.
41. Wesson DW, Levy E, Nixon RA, Wilson DA. Olfactory dysfunction correlates with amyloid-beta burden in an Alzheimer's disease mouse model. J Neurosci 2010, 30(2):505-514. 10.1523/JNEUROSCI.4622-09.2010, 2826174, 20071513.
42. Pike CJ, Burdick D, Walencewicz AJ, Glabe CG, Cotman CW. Neurodegeneration induced by A-β myloid peptides in vitro: the role of peptide assembly state. J Neurosci 1993, 13(4):1676-1687.
43. Selkoe DJ. Alzheimer's disease: genes, protein and therapy. Physiol Rev 2001, 81(2):741-766.
44. Lois C, Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148. 10.1126/science.8178174, 8178174.
45. Danielyan L, Schäfer R, Von Ameln-Mayerhofer A, Buadze M, Geisler J, Klopfer T, Burkhardt U, Proksch B, Verleysdonk S, Ayturan M, Buniatian GH, Gleiter CH, Frey WH. Intranasal delivery of cells to the brain. Eur J Cell Biol 2009, 88(6):315-324. 10.1016/j.ejcb.2009.02.001, 19324456.
46. Kogan JH, Frankland PW, Silva AJ. Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 2000, 10(1):47-56. 10.1002/(SICI)1098-1063(2000)10:1<47::AID-HIPO5>3.0.CO;2-6, 10706216.
47. Eichenbaum H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 2004, 44(1):109-120. 10.1016/j.neuron.2004.08.028, 15450164.
48. Levy DA, Hopkins RO, Squire LR. Impaired odor recognition memory in patients with hippocampal lesions. Learn Mem 2004, 11(6):794-796. 10.1101/lm.82504, 534708, 15537736.
49. Kesner RP, Hunsaker MR, Ziegler W. The role of the dorsal and ventral hippocampus in olfactory working memory. Neurobiol Learn Mem 2011, 96(2):361-366. 10.1016/j.nlm.2011.06.011, 21742047.
50. Sánchez-Andrade G, Kendrick KM. The main olfactory system and social learning in mammals. Behav Brain Res 2009, 200(2):323-335. 10.1016/j.bbr.2008.12.021, 19150375.
51. Wang X, Pal R, Chen XW, Limpeanchob N, Kumar KN, Michaelis EK. High intrinsic oxidative stress may underlie selective vulnerability of the hippocampal CA1 region. Mol Brain Res 2005, 140(1-2):120-126.
52. Kowall NW, McKee AC, Yankner BA, Beal MF. In vivo neurotoxicity of beta-amyloid [β(1-40)] and the β(25-35) fragment. Neurobiol Aging 1992, 13(5):537-542. 10.1016/0197-4580(92)90053-Z, 1461341.
53. Stepanichev MY, Zdobnova IM, Zarubenko II, Moiseeva YV, Lazareva NA, Onufriev MV, Gulyaeva NV. Amyloid-β(25-35)-induced memory impairments correlate with cell loss in rat hippocampus. Physiol Behav 2004, 80(5):647-655. 10.1016/j.physbeh.2003.11.003, 14984798.
54. Sigurdsson EM, Lee JM, Dong XW, Hejna MJ, Lorens SA. Laterality in the histological effects of injections of amyloid-beta 25-35 into the amygdala of young Fischer rats. J Neuropathol Exp Neurol 1997, 56(6):714-725.
55. Stark G. Functional consequences of oxidative membrane damage. J Membr Biol 2005, 205(1):1-16. 10.1007/s00232-005-0753-8, 16245038.
56. Jenner P, Olanow CW. Understanding cell death in Parkinson's disease. Ann Neurol 1998, 44(3 suppl 1):72-84.
57. Rivas-Arancibia S, Dorado-Martinez C, Colin-Barenque L, Kendrick KM, De la Riva C, Guevara-Guzman R. Effect of acute ozone exposure on locomotor behavior and striatal function. Pharmacol Biochem Behav 2003, 74(4):891-900. 10.1016/S0091-3057(03)00011-X, 12667904.
58. Guevara-Guzmán R, Arriaga V, Kendrick KM, Bernal C, Vega X, Mercado-Gómez OF, Rivas-Arancibia S. Estradiol prevents ozone-induced increases in brain lipid peroxidation and impaired social recognition memory in female rats. Neuroscience 2009, 159(3):940-950. 10.1016/j.neuroscience.2009.01.047, 19356678.
59. Sharp FR, Liu J, Bernabeu R. Neurogenesis following brain ischemia. Brain Res Dev Brain Res 2002, 134(1-2):23-30.
60. Butterfield DA, Reed T, Newman SF, Sultana R. Roles of amyloid β-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment. Free Radic Biol Med 2007, 43(5):658-677. 10.1016/j.freeradbiomed.2007.05.037, 2031860, 17664130.
61. Limón ID, Mendieta L, Díaz A, Chamorro G, Espinosa B, Zenteno E, Guevara J. Neuroprotective effect of alpha-asarone on spatial memory and nitric oxide levels in rats injected with amyloid-beta ((25-35)). Neurosci Lett 2009, 453:98-103. 10.1016/j.neulet.2009.02.011, 19356601.
62. Sharp FR, Liu J, Bernabeu R. Neurogenesis following brain ischemia. Dev Brain Res 2002, 134(1-2):23-30.
63. Schmued LC, Albertson C, Slikker W. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 1997, 751(1):37-46. 10.1016/S0006-8993(96)01387-X, 9098566.
64. Wharton W, Gleason CE, Lorenze KR, Markgraf TS, Ries ML, Carlsson M, Asthana S. Potential role of estrogen in the pathobiology and prevention of Alzheimer's disease. Am J Trans Res 2009, 1(2):131-147.
65. Henderson VW, Brinton RD. Menopause and mitochondria: windows into estrogen effects on Alzheimer's disease risk and therapy. Prog Brain Res 2010, 182:77-96.
66. Craig MC, Murphy DG. Estrogen therapy and Alzheimer's dementia. Ann N Y Acad Sci 2010, 1205:245-253. 10.1111/j.1749-6632.2010.05673.x, 20840280.
67. Yue X, Lu M, Lancaster T, Cao P, Honda S, Staufenbiel M, Harada N, Zhong Z, Shen Y, Li R. Brain estrogen deficiency accelerates Abeta plaque formation in Alzheimer's disease animal model. Proc Natl Acad Sci U S A 2005, 102(52):19198-19203. 10.1073/pnas.0505203102, 1323154, 16365303.
68. Wang JM, Irwin RW, Brinton RD. Activation of estrogen receptor α increases and estrogen receptor β decreases apolipoprotein E expression in hippocampus in vitro and in vivo. Proc Natl Acad Sci U S A 2006, 103:16983-16988. 10.1073/pnas.0608128103, 1636565, 17077142.