Molecular events during the induction of neurodegeneration and memory loss in estrogen-deficient rats

General and Comparative Endocrinology

Volumn 181, Issue 1, 2013, Pages 316-323

  Anukulthanakorn, Kanya ^a   Malaivijitnond, Suchinda ^a   Kitahashi, Takashi ^b   Jaroenporn, Sukanya ^a   Parhar, Ishwar ^b  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b MONASH UNIVERSITY MALAYSIA   (Malaysia)

Author keywords

Amyloid plaques; Hippocampus; Neurofibrillary tangles; Ovariectomy; TAU

Indexed keywords

ADAM10 ENDOPEPTIDASE; AMYLOID; BETA SECRETASE 1; ESTRADIOL; FOLLITROPIN; LUTEINIZING HORMONE; MESSENGER RNA;

ADAM10 GENE; ADULT ANIMAL; AMNESIA; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; APP GENE; ARTICLE; BACE1 GENE; COGNITIVE DEFECT; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; ESTROGEN DEFICIENCY; FEMALE; FOLLITROPIN BLOOD LEVEL; GENE; GENE EXPRESSION; HORMONE DETERMINATION; LATENT PERIOD; LUTEINIZING HORMONE BLOOD LEVEL; MAZE TEST; MOLECULAR PATHOLOGY; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPATIAL MEMORY; TAU3 GENE; TAU4 GENE;

EID: 84873056782     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2012.07.034     Document Type: Article

References (56)

1. Andreadis A., Brown W.M., Kosik K.S. Structure and novel exons of the human tau gene. Biochemistry 1992, 31:10626-10633.
2. Arai K., Watanabe G., Taya K., Sasamoto S. Roles of inhibin and estradiol in the regulation of follicle-stimulating hormone and luteinizing hormone secretion during the estrous cycle of the rat. Biology of Reproduction 1996, 55:127-133.
3. Boutajangout A., Boom A., Leroy K., Brion J.P. Expression of tau mRNA and soluble tau isoforms in affected and non-affected brain areas in Alzheimer's disease. FEBS Letters 2004, 576:183-189.
4. Brann D.W., Dhandapani K., Chandramohan W., Mahesh V.B., Khan M.M. Neurotrophic and neuroprotective actions of estrogen: basic mechanism and clinical implications. Steroids 2007, 72:381-405.
5. Brenner D.E., Kukull W.A., Stergachis A., van Belle G., Bowen J.D., McCormick W.C., Teri L., Larson E.B. Postmenopausal estrogen replacement therapy and the risk of Alzheimer's disease: a population-based case-control study. American Journal of Epidemiology 1994, 140:262-267.
6. Buee L., Bussiere T., Buee-Scherrer V., Delacourte A., Hof P.R. Tau protein isoforms, phosphorylation and role in neurodegenerative disorder. Brain Research Reviews 2000, 33:95-130.
7. Casadesus G., Webber K.M., Atwood C.S., Pappolla M.A., Perry G., Bowen R.L., Smith M.A. Luteinizing hormone modulates cognition and amyloid-beta deposition in Alzheimer APP transgenic mice. Biochimica Et Biophysica Acta 2006, 1762:447-452.
8. Cheon M.S., Dierssen M., Kim S.H., Lubec G. Protein expression of BACE1, BACE2 and APP in Down syndrome brains. Amino Acids 2008, 35:339-343.
9. Chu C., Gao G., Huang W. A study on co-localization of FSH and its receptor in rat hippocampus. Journal of Molecular Histology 2008, 39:49-55.
10. Donmez G., Wang D., Cohen D.E., Guarente L. SIRT1 suppress beta-amyloid production by activating the alpha-secretase gene ADAM10. Cell 2010, 142:320-332.
11. Endres K., Fahrenholz F. Regulation of alpha-secretase ADAM10 expression and activity. Experimental Brain Research 2012, 217:343-352.
12. Feng Z., Cheng Y., Zhang J. Long-term effects of melatonin or 17β-estradiol on improving spatial memory performance in cognitively impaired, ovariectomized adult rats. Journal of Pineal Research 2004, 37:198-206.
13. Forman M.S., Trojanowski J.Q., Lee V.M.Y. Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nature Medicine 2004, 10:1055-1063.
14. Fukuzaki E., Takuma K., Himeno Y., Yoshida S., Funatsu Y., Kitahara Y., Mizoguchi H., Ibi D., Koike K., Inoue M., Yamada K. Enhanced activity of hippocampal BACE1 in a mouse model of postmenopausal memory deficits. Neuroscience Letters 2008, 433:141-145.
15. Gandy S. Estrogen and neurodegeneration. Neurochemical Research 2003, 28:1003-1008.
16. Ginsberg S.D., Che S., Counts S.E., Mufson E.J. Shift in the ratio of three-repeat and four-repeat tau mRNAs in individual cholinergic basal neurons in mild cognitive impairment and Alzheimer's disease. Journal of Neurochemistry 2006, 96:1401-1408.
17. Glatz D.C., Rujescu D., Tang Y., Berendt F.J., Hartmann A.M., Faltraco F., Rosenberg C., Hulette C., Jellinger K., Hampel H., Riederer P., Moller H.J., Andreadis A., Henkel K., Stamm S. The alternative splicing of tau exon 10 and its regulatory proteins CLK2 and TRA2-BETA1 changes in sporadic Alzheimer's disease. Journal of Neurochemistry 2006, 96:635-644.
18. Goedert M., Spilantini M.G., Jakes R., Rutherford D., Crowther R.A. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989, 3:519-526.
19. Goedert M., Spillantini M.G., Davie S.W. Filamentous nerve cell inclusions in neurodegenerative diseases. Current Opinion in Neurobiology 1998, 8:619-632.
20. Goedert M., Spillantini M.G. Pathogenesis of the tauopathies. Journal of Molecular Neuroscience 2011, 45:425-431.
21. Goedert M. Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends in Neurosciences 1993, 16:460-465.
22. Gotz J., Chen F., van Dorpe J., Nitsch R.M. Formation of neurofibrillary tangles in p301l tau transgenic mice induced by beta 42 fibrils. Science 2001, 293:1491-1495.
23. Henderson V.W., Paganini-Hill A., Miller B.L., Elble R.J., Reyes P.F., Shoupe D., McCleary C.A., Klein R.A., Hake A.M., Farlow M.R. Estrogen for Alzheimer's disease in women; randomized, double-blind, placebo-controlled trial. Neurology 2000, 54:295-301.
24. Holsinger R.M., McLean C.A., Beyreuther K., Masters C.L., Evin G. Increased expression of the amyloid precursor beta-secretase in Alzheimer's disease. Annals of Neurology 2002, 51:783-786.
25. Hou Y., Bao X.-Q., Wei H.-L., Luo Y., Liu G.-T. Long-term deprivation of gonadal hormone accelerates brain aging in mice. Neurological Research 2011, 33:43-50.
26. Jaroenporn S., Horii Y., Akieda-Asai S., Wang K., Nagaoka K., Ohta R., Shirota M., Watanabe G., Taya K. Endocrine mechanisms responsible for different follicular development during the estrous cycle in Hatano high- and low-avoidance rats. Journal of Reproduction and Development 2011, 57:690-699.
27. Johnson M.H. Essential Reproduction 2007, Blackwell Publishing, Massachusetts. sixth ed.
28. Kandalepas P.C., Vasar R. Identification and biology of β-secretase. Journal of Neurochemistry Supplement 2012, 1:55-61.
29. Korenman S.G., Stevens R.H., Carpenter L.A., Robb M., Niswender G.D., Sherman B.M. Estradiol radioimmunoassay without chromatography: procedure, validation and normal values. Journal of Clinical Endocrinology and Metabolism 1974, 38:718-720.
30. Korol D.L. Role of estrogen in balancing contributions from multiple memory systems. Neurobiology of Learning and Memory 2004, 82:309-323.
31. Kosik K.S. The molecular and cellular biology of tau. Brain Pathology 1993, 3:39-43.
32. Lathe R. Hormones and the hippocampus. Journal of Endocrinology 2001, 169:205-231.
33. Li R., Lindholm K., Yang L.B., Yue X., Citron M., Yan R., Beach T., Sue L., Sabbagh M., Cai H., Wong P., Price D., Shen Y. Amyloid beta peptide load is correlated with increased beta-secretase activity in sporadic Alzheimer's disease patients. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:3632-3637.
34. Lin J., Li X., Yuan F., Lin L., Cook C.L., Rao C.V., Lei Z. Genetic ablation of luteinizing hormone receptor improves the amyloid pathology in a mouse model of Alzheimer disease. Journal of Neuropathology and Experimental Neurology 2010, 69:253-261.
35. Malaivijitnond S., Kiatthaipipat P., Cherdshewasart W., Watanabe G., Taya K. Different effects of Pueraria mirifica, a herb containing phytoestrogens, on LH and FSH secretion in gonadectomized female and male rats. Journal of Pharmacological Sciences 2004, 96:428-435.
36. Mulnard R.A., Cotman C.W., Kawas C., van Dyck C.H., Sano M., Doody R., Koss E., Pfeiffer E., Jin S., Gamst A., Grundman M., Thomas R., Thal L.J. Estrogen replacement therapy for treatment of mild to moderate Alzheimer's disease: a randomized controlled trial, Alzheimer's disease cooperative study. The Journal of the American Medical Association 2000, 23:1007-1015.
37. Nord L.C., Sundqvist J., Andersson E., Fried G. Analysis of oestrogen regulation of alpha-, beta- and gamma-secretase gene and protein expression in cultured human neuronal and glial cells. Neurodegenerative Diseases 2010, 7:349-364.
38. Paganini-Hill A., Henderson W.W. Estrogen deficiency and risk of Alzheimer's disease in women. American Journal of Epidemiology 1994, 140:256-261.
39. Petanceska S.S., Nagy V., Frail D., Gandy S. Ovariectomy and 17beta-estradiol modulate the levels of Alzheimer's amyloid beta peptides in brain. Neurology 2000, 54:2212-2217.
40. Prox J., Rittger A., Saftig P. Physiological functions of the amyloid precursor protein secretases ADAM10, BACE1, and presenilin. Experimental Brain Research 2012, 217:331-341.
41. Roberson E.D., Scearce-Levie K., Palop J.J., Yan F., Cheng I.H., Wu T., Gerstein H., Yu G.Q., Mucke L. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 2007, 316:750-754.
42. Robert M., Mathuranath P.S. Tau and tauopathies. Neurology India 2007, 55:11-16.
43. Shi J., Qian W., Yin X., Iqbal K., Grundke-Iqbal I., Gu X., Ding F., Gong C.X., Liu F. Cyclic AMP-dependent protein kinase regulates the alternative splicing of Tau exon 10: a mechanism involved in Tau pathology of Alzheimer disease. Journal of Biological Chemistry 2011, 286:14639-14648.
44. Short R.A., Bowen R.L., O'Brien P.C., Graff-Radford N.R. Elevated gonadotropin levels in patients with Alzheimer's disease. Mayo Clinic Proceedings 2001, 76:906-909.
45. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. Journal of Comparative Neurology 1997, 388:507-525.
46. Spillantini M.G., Murrell J.R., Goedert M., Farlow M.R., Klug A., Ghetti B. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:7737-7741.
47. Sun X., Bromley-Brits K., Song W. Regulation of β-site APP-cleaving enzyme 1 gene expression and its role in Alzheimer's disease. Journal of Neurochemistry Supplement 2012, 1:62-70.
48. Trinczek B., Biernat J., Baumann K., Mandeldow E.M., Mandelkow E. Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules. Molecular Biology of the Cell 1995, 6:1887-1902.
49. Vorhees C.V., Williams M.T. Morris water maze: procedure for assessing spatial and related forms of learning and memory. Nature Protocol 2006, 1:848-858.
50. Wahjoepramono E.J., Wijaya L.K., Taddei K., Bates K.A., Howard M., Martins G., de Ruyck K., Matthews P.M., Verdile G., Martins R.N. Direct exposure of guinea pig CNS to human luteinizing hormone increases cerebrospinal fluid and cerebral beta amyloid levels. Neuroendocrinology 2011, 94:313-322.
51. Webb R.L., Murphy M.P. β-Secretases, Alzheimer's disease, and down syndrome. Current Gerontology and Geriatrics Research 2012, 10.1155/2012/362839.
52. Wu J., Zhu Y., Wu J. Effects of estrogen and estrogenic compounds on cognition in ovariectomized rats. Climacteric 2008, 11:212-220.
53. Yang H.Q., Sun Z.K., Jiang Q.H., Shang Q., Xu J. Effect of estrogen-depletion and 17β-estradiol replacement therapy upon rat hippocampus β-amyloid generation. Zhonghua Yi Xue Za Zhi 2009, 89:2658-2661.
54. Yasojima K., McGeer E.G., McGeer P.L. Tangled areas of Alzheimer brain have upregulated levels of exon 10 containing tau mRNA. Brain Research 1999, 831:301-305.
55. 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 an Alzheimer's disease animal model. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:19198-19203.
56. Zheng H., Xu H., Uljon S.N., Gross R., Hardy K., Gaynor J., Lafrancois J., Simpkins J., Refolo L.M., Petanceska S., Wang R., Duff K. Modulation of A(beta) peptides by estrogen in mouse model. Journal of Neurochemistry 2002, 80:191-196.