Genistein improves 3-NPA-induced memory impairment in ovariectomized rats: Impact of its antioxidant, anti-inflammatory and acetylcholinesterase modulatory properties

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Menze, Esther T ^a   Esmat, Ahmed ^a   Tadros, Mariane G ^a   Abdel Naim, Ashraf B ^a   Khalifa, Amani E ^a  

^a African Union Organization St Abbassia   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROPROPIONIC ACID; ACETYLCHOLINESTERASE; ADENOSINE TRIPHOSPHATE; CYCLOOXYGENASE 2; ESTRADIOL; GENISTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; PHYTOESTROGEN; 3-NITROPROPIONIC ACID; ANTIOXIDANT; BIOLOGICAL MARKER; CATALASE; GLUTATHIONE; NITRO DERIVATIVE; PROPIONIC ACID DERIVATIVE;

AMNESIA; ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; COGNITION; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL HYPOACTIVITY; FEMALE; HIPPOCAMPUS; LOCOMOTION; MEMORY DISORDER; MITOCHONDRION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PASSIVE AVOIDANCE; PREMOTOR CORTEX; PROTEIN EXPRESSION; RAT; ANIMAL; ANIMAL BEHAVIOR; CHEMICALLY INDUCED; CORPUS STRIATUM; DRUG EFFECTS; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; MEMORY; MEMORY DISORDERS; METABOLISM; MOTOR ACTIVITY; OVARIECTOMY; PATHOLOGY; PSYCHOLOGY;

RATTUS; RODENTIA;

ACETYLCHOLINESTERASE; ANIMALS; ANTIOXIDANTS; BEHAVIOR, ANIMAL; BIOMARKERS; CATALASE; CORPUS STRIATUM; CYCLOOXYGENASE 2; FEMALE; GENISTEIN; GLUTATHIONE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; MEMORY; MEMORY DISORDERS; MOTOR ACTIVITY; NITRIC OXIDE SYNTHASE TYPE II; NITRO COMPOUNDS; OVARIECTOMY; OXIDATIVE STRESS; PROPIONATES; RATS;

EID: 84923253377     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117223     Document Type: Article

References (82)

1. Folstein SE (1989) Huntington's disease: a disorder of families. Baltimore: Johns Hopkins University Press. PMID: 25144100
2. Bonelli RM, Hofmann P (2004) A review of the treatment options for Huntington's disease. Expert Opin Pharmacother 5: 767-776. PMID: 15102562
3. Hahn-Barma V, Deweer B, Durr A, Dode C, Feingold J, et al. (1998) Are cognitive changes the first symptoms of Huntington's disease? A study of gene carriers. J Neurol Neurosurg Psychiatry 64: 172-177. PMID: 9489526
4. Phillips W, Shannon KM, Barker RA (2008) The current clinical management of Huntington's disease. Mov Disord 23: 1491-1504. doi: 10.1002/mds.21971 PMID: 18581443
5. Ho AK, Sahakian BJ, Brown RG, Barker RA, Hodges JR, et al. (2003) Profile of cognitive progression in early Huntington's disease. Neurology 61:1702-1706. PMID: 14694033
6. Novak MJ, Tabrizi SJ (2011) Huntington's disease: clinical presentation and treatment. Int Rev Neurobiol 98: 297-323. doi: 10.1016/B978-0-12-381328-2.00013-4 PMID: 21907093
7. Spokes EG (1980) Neurochemical alterations in Huntington's chorea: a study of post-mortem brain tissue. Brain 103: 179-210. PMID: 6102490
8. Lange KW, Javoy-Agid F, Agid Y, Jenner P, Marsden CD (1992) Brain muscarinic cholinergic receptors in Huntington's disease. J Neurol 239: 103-104. PMID: 1532417
9. Montoya A, Price BH, Menear M, Lepage M (2006) Brain imaging and cognitive dysfunctions in Huntington's disease. J Psychiatry Neurosci 31: 21-29. PMID: 16496032
10. Coles CJ, Edmondson DE, Singer TP (1979) Inactivation of succinate dehydrogenase by 3-nitropropionate. J Biol Chem 254: 5161-5167. PMID: 447637
11. James LF, Hartley WJ, Williams MC, Van Kampen KR (1980) Field and experimental studies in cattle and sheep poisoned by nitro-bearing Astragalus or their toxins. Am J Vet Res 41: 377-382. PMID: 7369611
12. Ludolph AC, He F, Spencer PS, Hammerstad J, Sabri M (1991) 3-Nitropropionic acid-exogenous animal neurotoxin and possible human striatal toxin. Can J Neurol Sci 18: 492-498. PMID: 1782616
13. Ming L (1995) Moldy sugarcane poisoning-a case report with a brief review. J Toxicol Clin Toxicol 33: 363-367. PMID: 7629905
14. Brouillet E, Guyot MC, Mittoux V, Altairac S, Conde F, et al. (1998) Partial inhibition of brain succinate dehydrogenase by 3-nitropropionic acid is sufficient to initiate striatal degeneration in rat. J Neurochem 70: 794-805. PMID: 9453576
15. Beal MF (1992) Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann Neurol 31: 119-130. PMID: 1349466
16. Beal MF, Brouillet E, Jenkins BG, Ferrante RJ, Kowall NW, et al. (1993) Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J Neurosci 13: 4181-4192. PMID: 7692009
17. Borlongan CV, Koutouzis TK, Sanberg PR (1997) 3-Nitropropionic acid animal model and Huntington's disease. Neurosci Biobehav Rev 21: 289-293. PMID: 9168265
18. Browne SE, Ferrante RJ, Beal MF (1999) Oxidative stress in Huntington's disease. Brain Pathol 9: 147-163. PMID: 9989457
19. Turgeon JL, McDonnell DP, Martin KA, Wise PM (2004) Hormone therapy: physiological complexity belies therapeutic simplicity. Science 304: 1269-1273. PMID: 15166356
20. McEwen B (2002) Estrogen actions throughout the brain. Recent Prog Horm Res 57: 357-384. PMID: 12017552
21. Sherwin BB (2003) Estrogen and cognitive functioning in women. Endocr Rev 24: 133-151. PMID: 12700177
22. Beresford SA, Weiss NS, Voigt LF, McKnight B (1997) Risk of endometrial cancer in relation to use of oestrogen combined with cyclic progestagen therapy in postmenopausal women. Lancet 349: 458-461. PMID: 9040575
23. Coolaborative Group on Hormonal Factors in Breast Cancer (1997) Breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Lancet 350: 1047-1059. PMID: 10213546
24. Barnes S, Kim H, Darley-Usmar V, Patel R, Xu J, et al. (2000) Beyond ERalpha and ERbeta: estrogen receptor binding is only part of the isoflavone story. J Nutr 130: 656S-657S. PMID: 10702602
25. An J, Tzagarakis-Foster C, Scharschmidt TC, Lomri N, Leitman DC (2001) Estrogen receptor beta-selective transcriptional activity and recruitment of coregulators by phytoestrogens. J Biol Chem 276: 17808-17814. PMID: 11279159
26. Xu J, Zhu J, Shi C, Guo K, Yew DT (2007) Effects of genistein on hippocampal neurodegeneration of ovariectomized rats. J Mol Neurosci 31: 101-112. PMID: 17478884
27. File SE, Jarrett N, Fluck E, Duffy R, Casey K, et al. (2001) Eating soya improves human memory. Psychopharmacology (Berl) 157: 430-436. PMID: 11605103
28. Xu SZ, Zhong W, Ghavideldarestani M, Saurabh R, Lindow SW, et al. (2009) Multiple mechanisms of soy isoflavones against oxidative stress-induced endothelium injury. Free Radic Biol Med 47: 167-175. doi: 10.1016/j.freeradbiomed.2009.04.021 PMID: 19393315
29. Shughrue PJ, Lane MV, Merchenthaler I (1997) Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388: 507-525. PMID: 9388012
30. Wang L, Andersson S, Warner M, Gustafsson JA (2001) Morphological abnormalities in the brains of estrogen receptor beta knockout mice. Proc Natl Acad Sci USA 98 (5): 2792-2796. PMID: 11226319
31. Day M, Sung A, Logue S, Bowlby M, Arias R (2005) Beta estrogen receptor knockout (BERKO) mice present attenuated hippocampal CA1 long-term potentiation and related memory deficits in contextual fear conditioning. Beh brain res 164: 128-131. PMID: 16054246
32. Adlercreutz CH, Goldin BR, Gorbach SL, Hockerstedt KA, Watanabe S, et al. (1995) Soybean phytoestrogen intake and cancer risk. J Nutr 125: 757S-770S. PMID: 7884562
33. Zava DT, Duwe G (1997) Estrogenic and antiproliferative properties of genistein and other flavonoids in human breast cancer cells in vitro. Nutr Cancer 27: 31-40. PMID: 8970179
34. Poumeau-Delille G (1953) Techniques biologiques en endocrinologie experimentale chez rat. Masson and Cie, Paris. PMID: 13123806
35. Tunéz I, Collado JA, Medina FJ, Pena J, Del CMM, et al. (2006) 17 beta-Estradiol may affect vulnerability of striatum in a 3-nitropropionic acid-induced experimental model of Huntington's disease in ovariectomized rats. Neurochem Int 48: 367-373. PMID: 16420966
36. Bagheri M, Joghataei MT, Mohseni S, Roghani M (2011) Genistein ameliorates learning and memory deficits in amyloid beta(1-40) rat model of Alzheimer's disease. Neurobiol Learn Mem 95: 270-276. doi: 10.1016/j.nlm.2010.12.001 PMID: 21144907
37. Banchroft JD, Stevens A, Turner DR (1996) Theory and practice of histological techniques. Fourth Ed Churchil Livingstone, New York, London, San Francisco, Tokyo. PMID: 25121335
38. Mihara M, Uchiyama M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86: 271-278. PMID: 655387
39. Aebi H (1984) Catalase in vitro. Methods Enzymol 105: 121-126. PMID: 6727660
40. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82: 70-77. PMID: 13650640
41. Ellman GL, Courtney KD, Andres V Jr., Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7: 88-95. PMID: 13726518
42. Johansson AC, Hegardt P, Janelidze S, Visse E, Widegren B, et al. (2002) Enhanced expression of iNOS intratumorally and at the immunization site after immunization with IFNgamma-secreting rat glioma cells. J Neuroimmunol 123: 135-143. PMID: 11880158
43. Yuan GJ, Zhou XR, Gong ZJ, Zhang P, Sun XM, et al. (2006) Expression and activity of inducible nitric oxide synthase and endothelial nitric oxide synthase correlate with ethanol-induced liver injury. World J Gastroenterol 12: 2375-2381. PMID: 16688828
44. Zhao L, Wu TW, Brinton RD (2004) Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Res 1010: 22-34. PMID: 15126114
45. Bang OY, Hong HS, Kim DH, Kim H, Boo JH, et al. (2004) Neuroprotective effect of genistein against beta amyloid-induced neurotoxicity. Neurobiol Dis 16: 21-28. PMID: 15207258
46. Kyuhou S (2008) Preventive effects of genistein on motor dysfunction following 6-hydroxydopamine injection in ovariectomized rats. Neurosci Lett 448: 10-14. doi: 10.1016/j.neulet.2008.10.045 PMID: 18952148
47. Castello-Ruiz M, Torregrosa G, Burguete MC, Salom JB, Gil JV, et al. (2011) Soy-derived phytoestrogens as preventive and acute neuroprotectors in experimental ischemic stroke: influence of rat strain. Phytomedicine 18: 513-515. doi: 10.1016/j.phymed.2011.02.001 PMID: 21420287
48. Huang YH, Zhang QH (2010) Genistein reduced the neural apoptosis in the brain of ovariectomised rats by modulating mitochondrial oxidative stress. Br J Nutr 104: 1297-1303. doi: 10.1017/S0007114510002291 PMID: 20579403
49. Seaman RL (2000) Effects of acute systemic 3-nitropropionic acid administration on rat activity and acoustic startle. Neurosci Lett 280: 183-186. PMID: 10675791
50. Tadros MG, Khalifa AE, Abdel-Naim AB, Arafa HM (2005) Neuroprotective effect of taurine in 3-nitropropionic acid-induced experimental animal model of Huntington's disease phenotype. Pharmacol Biochem Behav 82: 574-582. PMID: 16337998
51. Ahuja M, Bishnoi M, Chopra K (2008) Protective effect of minocycline, a semi-synthetic second-generation tetracycline against 3-nitropropionic acid (3-NP)-induced neurotoxicity. Toxicology 244: 111-122. doi: 10.1016/j.tox.2007.11.003 PMID: 18164115
52. Kumar P, Kumar A (2009) Neuroprotective effect of cyclosporine and FK506 against 3-nitropropionic acid induced cognitive dysfunction and glutathione redox in rat: possible role of nitric oxide. Neurosci Res 63: 302-314. PMID: 19367792
53. Al Mutairy A, Al Kadasah S, Elfaki I, Arshaduddin M, Malik D, et al. (2010) Trolox ameliorates 3-nitropropionic acid-induced neurotoxicity in rats. Neurotoxicol Teratol 32: 226-233. doi: 10.1016/j.ntt.2009.09. 003 PMID: 19755148
54. Morissette M, Al Sweidi S, Callier S, Di Paolo T (2008) Estrogen and SERM neuroprotection in animal models of Parkinson's disease. Mol Cell Endocrinol 290: 60-69. doi: 10.1016/j.mce.2008.04.008 PMID: 18515001
55. Baraka AM, Korish AA, Soliman GA, Kamal H (2011) The possible role of estrogen and selective estrogen receptor modulators in a rat model of Parkinson's disease. Life Sci 88: 879-885. doi: 10.1016/j.lfs. 2011.03.010 PMID: 21420980
56. Curzon P, Zhang M, Radek RJ, Fox GB (2009) The Behavioral Assessment of Sensorimotor Processes in the Mouse: Acoustic Startle, Sensory Gating, Locomotor Activity, Rotarod, and Beam Walking.
57. Silva RH, Abilio VC, Kameda SR, Takatsu-Coleman AL, Carvalho RC, et al. (2007) Effects of 3-nitropropionic acid administration on memory and hippocampal lipid peroxidation in sleep-deprived mice. Prog Neuropsychopharmacol Biol Psychiatry 31: 65-70. PMID: 16876303
58. Sato T, Tanaka K, Ohnishi Y, Teramoto T, Irifune M, et al. (2004) Effects of steroid hormones on (Na+, K+)-ATPase activity inhibition-induced amnesia on the step-through passive avoidance task in gonadectomized mice. Pharmacol Res 49: 151-159. PMID: 14643695
59. Duan W, Guo Z, Mattson MP (2000) Participation of par-4 in the degeneration of striatal neurons induced by metabolic compromise with 3-nitropropionic acid. Exp Neurol 165: 1-11. PMID: 10964480
60. Lorenzini CA, Baldi E, Bucherelli C, Sacchetti B, Tassoni G (1996) Role of dorsal hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response: a tetrodotoxin functional inactivation study. Brain Res 730: 32-39. PMID: 8883885
61. Mahdy HM, Tadros MG Mohamed MR, Karim AM, Khalifa AE (2011) The effect of Ginkgo biloba extract on 3-nitropropionic acid-induced neurotoxicity in rats. Neurochem Int. 59(6):770-778. doi: 10.1016/j. neuint.2011.07.012 PMID: 21827809
62. Smets LA, Van den Berg J, Acton D, Top B, Van Rooij H, et al. (1994) BCL-2 expression and mitochondrial activity in leukemic cells with different sensitivity to glucocorticoid-induced apoptosis. Blood 84: 1613-1619. PMID: 8068950
63. Villa P, Miehe M, Sensenbrenner M, Pettmann B (1994) Synthesis of specific proteins in trophic factordeprived neurons undergoing apoptosis. J Neurochem 62: 1468-1475. PMID: 8133275
64. Brinton RD (2008) The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci 31: 529-537. doi: 10.1016/j.tins.2008.07.003 PMID: 18774188
65. Brinton RD (2009) Estrogen-induced plasticity from cells to circuits: predictions for cognitive function. Trends Pharmacol Sci 30: 212-222. doi: 10.1016/j.tips.2008.12.006 PMID: 19299024
66. Arce C, Arteaga JL, Sánchez-Mendoza E, Oset-Gasque MJ, Cañadas S,González MP (2010) Added after Anoxia-Reoxigenation Stress, Genistein Rescues from Death the Rat Embryo Cortical Neurons. Neuroscience & Medicine 1: 50-59. doi: 10.1155/2015/598496 PMID: 25632397
67. Miller PJ, Zaborszky L (1997) 3-Nitropropionic acid neurotoxicity: visualization by silver staining and implications for use as an animal model of Huntington's disease. Exp Neurol 146: 212-229. PMID: 9225755
68. Schulz JB, Henshaw DR, MacGarvey U, Beal MF (1996) Involvement of oxidative stress in 3-nitropropionic acid neurotoxicity. Neurochem Int 29: 167-171. PMID: 8837046
69. Sharma M, Sharma N, Sharma R (2012) Neuroprotective effect of Zingiber officinale in 3-np-induced huntington disease. IOSR Journal of Pharmacy 2: 61-70.
70. Mooradian AD (1993).Antioxidant of steroids. J Steroid Biochem Mol Biol 45: 509-511. PMID: 8518206
71. Gomez-Zubeldia MA, Arbués JJ, Hinchando G, Nogales A G, Millan L C (2001) Influence of estrogen replacement therapy on plasma lipid peroxidation. Menopause 8: 274-280. PMID: 11449085
72. Prokai L, Prokai-Tatrai K, Perjesi P, Simpkins JW(2006) Mechanistic insights into the direct antioxidant effects of estrogens. Drug Development Research 66: 118-125.
73. Qian Y, Guan T, Huang M, Cao L, Li Y, et al. (2012) Neuroprotection by the soy isoflavone, genistein, via inhibition of mitochondria-dependent apoptosis pathways and reactive oxygen induced-NF-kappaB activation in a cerebral ischemia mouse model. Neurochem Int 60: 759-767. doi: 10.1016/j.neuint. 2012.03.011 PMID: 22490611
74. Jones DN, Barnes JC, Kirkby DL, Higgins GA (1995) Age-associated impairments in a test of attention: evidence for involvement of cholinergic systems. J Neurosci 15: 7282-7292. PMID: 7472482
75. Martins DB, Mazzanti CM, Franca RT, Pagnoncelli M, Costa MM, et al. (2012) 17-beta estradiol in the acetylcholinesterase activity and lipid peroxidation in the brain and blood of ovariectomized adult and middle-aged rats. Life Sci 90: 351-359. doi: 10.1016/j.lfs.2011.12.006 PMID: 22227472
76. Kalpana S, Raju A.B, Merugu M.S. (2013) Genistein, a phytoestrogen fot the treatment of schizophrenia. International Journal of Scientific & Engineering Research 4: 296-321.
77. Meda L, Baron P, Scarlato G (2001) Glial activation in Alzheimer's disease: the role of Abeta and its associated proteins. Neurobiol Aging 22: 885-893. PMID: 11754995
78. Okun E, Griffioen KJ, Lathia JD, Tang SC, Mattson MP, et al. (2009) Toll-like receptors in neurodegeneration. Brain Res Rev 59: 278-292. doi: 10.1016/j.brainresrev.2008.09.001 PMID: 18822314
79. Diaz A, Mendieta L, Zenteno E, Guevara J, Limon ID (2011) The role of NOS in the impairment of spatial memory and damaged neurons in rats injected with amyloid beta 25-35 into the temporal cortex. Pharmacol Biochem Behav 98: 67-75. doi: 10.1016/j.pbb.2010.12.005 PMID: 21163295
80. Jang M, Lee MJ, Cho IH (2014) Ethyl pyruvate ameliorates 3-nitropropionic acid-induced striatal toxicity through anti-neuronal cell death and anti-inflammatory mechanisms. Brain Behav Immun 38: 151-165. doi: 10.1016/j.bbi.2014.01.015 PMID: 24576481
81. Vallesa S L, Dolz-Gaitona P, Gambinia J, Borrasa C, LLoreta A et al. (2010) Estradiol or genistein prevent Alzheimer's disease-associated inflammation correlating with an increase PPARγ expression in cultured astrocytes. Brain Res 1312: 138-144. doi: 10.1016/j.brainres.2009.11.044 PMID: 19948157
82. Lu H, Shi JX, Zhang DM, Wang HD, Hang CH, et al. (2009) Inhibition of hemolysate-induced iNOS and COX-2 expression by genistein through suppression of NF-small ka, CyrillicB activation in primary astrocytes. J Neurol Sci 278: 91-95. doi: 10.1016/j.jns.2008.12.007 PMID: 19162281