Long-term melatonin or 17β-estradiol supplementation alleviates oxidative stress in ovariectomized adult rats

Free Radical Biology and Medicine

Volumn 39, Issue 2, 2005, Pages 195-204

  Feng, Zheng ^a,b   Zhang, Jun Tian ^a  

^a INSTITUTE OF MATERIA MEDICA   (China)

^b University of California   (United States)

Author keywords

Alzheimer's disease; Apoptosis; Melatonin; Ovariectomized; Oxidative stress

Indexed keywords

CASPASE 3; ESTRADIOL; GLUTATHIONE; MELATONIN; PROTEIN BAX; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DEMENTIA; ENZYME ACTIVITY; FEMALE; IMMUNOHISTOCHEMISTRY; LONG TERM CARE; NONHUMAN; OVARIECTOMY; OXIDATIVE STRESS; POSTMENOPAUSE; PRIORITY JOURNAL; RAT; SUPPLEMENTATION; UPREGULATION;

ANIMALS; ANTIOXIDANTS; APOPTOSIS REGULATORY PROTEINS; BRAIN; CASPASE 3; CASPASES; DIETARY SUPPLEMENTS; ELECTRON TRANSPORT; ESTRADIOL; FEMALE; GLUTATHIONE; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID PEROXIDATION; MELATONIN; MITOCHONDRIA; OVARY; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCES; TIME FACTORS; UP-REGULATION;

MUS MUSCULUS; SESAMUM INDICUM;

EID: 20444470290     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2005.03.007     Document Type: Article

References (66)

1. R.A. Floyd, and K. Hensley Oxidative stress in brain aging. Implications for therapeutics of neurodegenerative diseases Neurobiol. Aging 23 2002 795 807
2. A.J. Hung, M.G. Stanbury, M. Shanabrough, T.L. Horvath, L.M. Garcia-Segura, and F. Naftolin Estrogen, synaptic plasticity and hypothalamic reproductive aging Exp. Gerontol. 38 2003 53 59
3. J. Nilsen, and R. Diaz Brinton Mechanism of estrogen-mediated neuroprotection: regulation of mitochondrial calcium and Bcl-2 expression Proc. Natl. Acad. Sci. U. S. A. 100 2003 2842 2847
4. C. Behl Oestrogen as a neuroprotective hormone Nat. Rev. Neurosci. 3 2002 433 442
5. B.R. Bhavnani Estrogens and menopause: pharmacology of conjugated equine estrogens and their potential role in the prevention of neurodegenerative diseases such as Alzheimer's J. Steroid Biochem. Mol. Biol. 85 2003 473 482
6. B. Cholerton, C.E. Gleason, L.D. Baker, and S.R. Asthana Estrogen and Alzheimer's disease: the story so far Drugs Aging 19 2002 405 427
7. L.M. Garcia-Segura, I. Azcoitia, and L.L. DonCarlos Neuroprotection by estradiol Prog. Neurobiol. 63 2001 29 60
8. M. Ozgonul, A. Oge, E.D. Sezer, F. Bayraktar, and E.Y. Sozmen The effects of estrogen and raloxifene treatment on antioxidant enzymes in brain and liver of ovarectomized female rats Endocr. Res. 29 2003 183 189
9. M.A. Pappolla, M.J. Simovich, T. Bryant-Thomas, Y.J. Chyan, B. Poeggeler, M. Dubocovich, R. Bick, G. Perry, F. Cruz-Sanchez, and M.A. Smith The neuroprotective activities of melatonin against the Alzheimer β-protein are not mediated by melatonin membrane receptors J. Pineal Res. 32 2002 135 142
10. E. Matsubara, T. Bryant-Thomas, J. Pacheco Quinto, T.L. Henry, B. Poeggeler, D. Herbert, F. Cruz-Sanchez, Y.J. Chyan, M.A. Smith, and G. Perry Melatonin increases survival and inhibits oxidative and amyloid pathology in a transgenic model of Alzheimer's disease J. Neurochem. 85 2003 1101 1108
11. C. Behl, and B. Moosmann Antioxidant neuroprotection in Alzheimer's disease as preventive and therapeutic approach Free Radic. Biol. Med. 33 2002 182 191
12. Z. Feng, Y. Chang, Y. Cheng, B.L. Zhang, Z.W. Qu, C. Qin, and J.T. Zhang Melatonin alleviates behavioral deficits associated with apoptosis and cholinergic system dysfunction in the APP 695 transgenic mouse model of Alzheimer's disease J. Pineal Res. 37 2004 129 136
13. Z. Feng, Y. Cheng, and J.T. Zhang Long-term effects of Melatonin and 17β-estradiol on improving spatial memory performance in cognitively impaired ovariectomized adult rats J. Pineal. Res. 37 2004 198 206
14. Z. Feng, and J.T. Zhang Protective effect of melatonin on β-amyloid induced apoptosis in pheochromocytoma (PC12) cells J. Pineal Res. 37 2004 257 266
15. Z. Feng, and J.T. Zhang Protective effects of melatonin on β-amyloid induced apoptosis in rat astroglioma C6 cells Free Radic. Biol. Med. 37 2004 1790 1801
16. R. Sandyk, P.G. Anastasiadis, P.A. Anninos, and N. Tsagas Is postmenopausal osteoporosis related to pineal gland functions? Int. J. Neurosci. 62 1992 215 225
17. A. Wakatsuki, Y. Okatani, N. Ikenoue, C. Kaneda, and T. Fukaya Effects of short-term melatonin administration on lipoprotein metabolism in normolipidemic postmenopausal women Maturitas 38 2001 171 177
18. A. Brzezinski "Melatonin replacement therapy" for postmenopausal women: is it justified? Menopause 5 1998 60 64
19. M. Singh, E.M. Meyer, W.J. Millard, and J.W. Simpkins Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats Brain Res. 644 1994 305 312
20. Q. Wang, R. Santizo, V.L. Baughman, and D.A. Pelligrino Estrogen provides neuroprotection in transient forebrain ischemia through perfusion-independent mechanisms in rats Stroke 30 1999 630 637
21. K. Ozawa, K. Seta, H. Takeda, K. Ando, H. Handa, and C. Araki On the isolation of mitochondria with high respiratory control from rat brain J. Biochem. 59 1966 501 510
22. H.H. Ku, U.T. Brunk, and R.S. Sohal Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species Free Radic. Biol. Med. 15 1993 621-627
23. R. Moreno-Sanchez, B.A. Hogue, C. Bravo, A.H. Newman, A.S. Basile, and P.K. Chiang R Inhibition of substrate oxidation in mitochondria by the peripheral-type benzodiazepine receptor ligand AHN 086 Biochem. Pharmacol. 41 1991 1479-1484
24. G.L. Sottocasa, B. Kuylenstierna, L. Ernster, and A. Bergstrand An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study J. Cell Biol. 32 1967 415 438
25. H.H. Draper, and M. Hadley Malondialdehyde determination as index of lipid peroxidation Methods Enzymol. 186 1990 421 431
26. F. Paoletti, and A. Mocali Determination of superoxide dismutase activity by purely chemical system based on NAD (P) H oxidation Methods Enzymol. 186 1990 209 220
27. V.H. Cohn, and J. Lyle A fluorimetric assay for glutathione Anal. Biochem. 14 1966 434 440
28. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
29. P.J. Shughrue, and I. Merchenthaler Estrogen is more than just a "sex hormone": novel sites for estrogen action in the hippocampus and cerebral cortex Front. Neuroendocrinol. 21 2000 95 101
30. P.M. Wise, D.B. Dubal, M.E. Wilson, S.W. Rau, and M. Bottner Minireview: neuroprotective effects of estrogen-new insights into mechanisms of action Endocrinology 142 2001 969 973
31. B.B. Sherwin Estrogen and cognitive functioning in women Endocr. Rev. 24 2003 133 151
32. S. Asthana, S. Craft, L.D. Baker, M.A. Raskind, R.S. Birnbaum, C.P. Lofgreen, R.C. Veith, and S.R. Plymate Cognitive and neuroendocrine response to transdermal estrogen in postmenopausal women with Alzheimer's disease: results of a placebo-controlled, double-blind, pilot study Psychoneuroendocrinology 24 1999 657 677
33. S. Asthana, L.D. Baker, S. Craft, F.Z. Stanczyk, R.C. Veith, M.A. Raskind, and S.R. Plymate High-dose estradiol improves cognition for women with AD: results of a randomized study Neurology 57 2001 605 612
34. A.J. Levine, and M. Battista Estrogen replacement therapy: effects on the cognitive functioning and clinical course of women with Alzheimer's disease Arch. Clin. Neuropsychol. 19 2004 769 778
35. J. Dunkin, N. Rasgon, K. Wagner-Steh, S. David, L. Altshuler, and A. Rapkin Reproductive events modify the effects of estrogen replacement therapy on cognition in healthy postmenopausal women Psychoneuroendocrinology 30 2005 284 296
36. S. Wassertheil-Smoller, S.L. Hendrix, M. Limacher, G. Heiss, C. Kooperberg, A. Baird, T. Kotchen, J.D. Curb, H. Black, J.E. Rossouw, A. Aragaki, M. Safford, E. Stein, S. Laowattana, W.J. Mysiw WHI Investigators Effect of estrogen plus progestin on stroke in postmenopausal women: the Women's Health Initiative: a randomized trial JAMA 289 2003 2673 2684
37. M.I. Geerlings, L.J. Launer, F.H. de Jong, A. Ruitenberg, T. Stijnen, J.C. van Swieten, A. Hofman, J.C. Witteman, H.A. Pols, M.M. Breteler Rotterdam, Study Endogenous estradiol and risk of dementia in women and men: the Rotterdam Study Ann. Neurol. 53 2003 607 615
38. R.J. Reiter, J. Cabrera, R.M. Sainz, J.C. Mayo, L.C. Manchester, and D.X. Tan Melatonin as a pharmacological agent against neuronal loss in experimental models of Huntington's disease, Alzheimer's disease and parkinsonism Ann. N. Y. Acad. Sci. 890 1999 471 485
39. T. Sato, T. Teramoto, K. Tanaka, Y. Ohnishi, M. Irifune, and T. Nishikawa Effects of ovariectomy and calcium deficiency on learning and memory of eight-arm radial maze in middle-aged female rats Behav. Brain Res. 142 2003 207 216
40. V.N. Luine, S.T. Richards, V.Y. Wu, and K.D. Beck Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters Horm. Behav. 34 1998 149 162
41. J. Sastre, F.V. Pallardo, and J. Vina The role of mitochondrial oxidative stress in aging Free Radic. Biol. Med. 35 2003 1 8
42. M.P. Mattson, N. Robinson, and Q. Guo Estrogens stabilize mitochondrial function and protect neural cells against the pro-apoptotic action of mutant presenilin-1 Neuroreport 8 1997 3817 3821
43. M. Martin, M. Macias, G. Escames, R.J. Reiter, M.T. Agapito, G.G. Ortiz, and D. Acuna-Castroviejo Melatonin-induced increased activity of the respiratory chain complexes I and IV can prevent mitochondrial damage induced by ruthenium red in vivo J. Pineal Res. 28 2000 242 248
44. M. Martin, M. Macias, J. Leon, G. Escames, H. Khaldy, and D. Acuna-Castroviejo Melatonin increases the activity of the oxidative phosphorylation enzymes and the production of ATP in rat brain and liver mitochondria Int. J. Biochem. Cell Biol. 34 2002 348 357
45. D. Acuna-Castroviejo, G. Escames, J. Leon, A. Carazo, and H. Khaldy Mitochondrial regulation by melatonin and its metabolites Adv. Exp. Med. Biol. 527 2003 549 557
46. G.E. Hoffman Ambiguity of estrogen receptor antagonists: good guys don't always wear white hats. or do they? Exp. Neurol. 188 2004 193 194
47. S. Xia, Z.Y. Cai, L.L. Thio, J.S. Kim-Han, L.L. Dugan, D.F. Covey, and S.M. Rothman The estrogen receptor is not essential for all estrogen neuroprotection: new evidence from a new analog Neurobiol. Dis. 9 2002 282 293
48. L.E. Haynes, C.L. Lendon, D.J. Barber, and I.J. Mitchell 17β-Oestradiol attenuates dexamethasone-induced lethal and sublethal neuronal damage in the striatum and hippocampus Neuroscience 120 2003 799 806
49. B. Moosmann, and C. Behl The antioxidant neuroprotective effects of estrogens and phenolic compounds are independent from their estrogenic properties Proc. Natl. Acad. Sci. USA 96 1999 8867 8872
50. L. Prokai, K. Prokai-Tatrai, P. Perjesi, A.D. Zharikova, E.J. Perez, R. Liu, and J.W. Simpkins Quinol-based cyclic antioxidant mechanism in estrogen neuroprotection Proc. Natl. Acad. Sci. USA 100 2003 11741 11746
51. S.B. Pajovic, Z.S. Saicic, M.B. Spasic, V.M. Petrovic, and J.V. Martinovic Effects of progesterone and estradiol benzoate on glutathione dependent antioxidant enzyme activities in the brain of female rats Gen. Physiol. Biophys. 18 1999 35 44
52. S. Shimohama Mechanisms of antiapoptotic effects of estrogens in nigral dopaminergic neurons FASEB J. 14 2000 1202 1214
53. P.C. Waldmeier Prospects for antiapoptotic drug therapy of neurodegenerative diseases Prog. Neuropsychopharmacol. Biol. Psychiatry 27 2003 303 321
54. S.E. Stoltzner, N.C. Berchtold, C.W. Cotman, and C.J. Pike Estrogen regulates bcl-x expression in rat hippocampus Neuroreport 12 2001 2797 2800
55. I. Silva, L.E. Mello, E. Freymuller, M.A. Haidar, and E.C. Baracat Estrogen, progestogen and tamoxifen increase synaptic density of the hippocampus of ovariectomized rats Neurosci. Lett. 291 2000 183 186
56. C.S. Woolley, N.G. Weiland, B.S. McEwen, and P.A. Schwartzkroin Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density J. Neurosci. 17 1997 1848 1859
57. N.J. Sandstrom, and C.L. Williams Memory retention is modulated by acute estradiol and progesterone replacement Behav. Neurosci. 115 2001 384 393
58. D.D. Murphy, N.B. Cole, and M. Segal Brain-derived neurotrophic factor mediates estradiol-induced dendritic spine formation in hippocampal neurons Proc. Natl. Acad. Sci. USA 95 1998 11412 11417
59. T. Heikkinen, J. Puolivali, L. Liu, A. Rissanen, and H. Tanila Effects of ovariectomy and estrogen treatment on learning and hippocampal neurotransmitters in mice Horm. Behav. 41 2002 22 32
60. C. Li, W.G. Brake, R.D. Romeo, J.C. Dunlop, M. Gordon, R. Buzescu, A.M. Magarinos, P.B. Allen, P. Greengard, V. Luine, and B.S. McEwen Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice Proc. Natl. Acad. Sci. USA 101 2004 2185 2190
61. P.R. Rapp, J.H. Morrison, and J.A. Roberts Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys J. Neurosci. 23 2003 5708 5714
62. Q. Guo, J. Xie, X. Chang, and H. Du Prostate apoptosis response-4 enhances secretion of amyloid beta peptide 1-42 in human neuroblastoma IMR-32 cells by a caspase-dependent pathway J. Biol. Chem. 276 2001 16040 16044
63. R.M. White, D.J. Kennaway, and R.F. Seamark Estrogenic effects on urinary 6-sulphatoxymelatonin excretion in the female rat J. Pineal Res. 22 1997 124 129
64. A. Cagnacci, S. Arangino, M. Angiolucci, G.B. Melis, R. Tarquini, A. Renzi, and A. Volpe Different circulatory response to melatonin in postmenopausal women without and with hormone replacement therapy J. Pineal Res. 29 2000 152 158
65. Y. Gilgun-Sherki, E. Melamed, and D. Offen Oxidative stress induced-neurodegenerative diseases: the need for antioxidants that penetrate the blood brain barrier Neuropharmacology 40 2001 959 975
66. B.J. Holliman, and P.A. Chyka Problems in assessment of acute melatonin overdose South Med. J. 90 1997 451 453