Testosterone regulation of Alzheimer-like neuropathology in male 3xTg-AD mice involves both estrogen and androgen pathways

Brain Research

Volumn 1359, Issue , 2010, Pages 281-290

  Rosario, Emily R ^a   Carroll, Jenna ^a   Pike, Christian J ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Amyloid; Alzheimer's disease; Sex steroid hormone; Tau hyperphosphorylation; Transgenic mouse

Indexed keywords

AMYLOID BETA PROTEIN; ANDROSTANOLONE; ESTRADIOL; TAU PROTEIN; TESTOSTERONE;

AGE DISTRIBUTION; ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ESTROGEN ACTIVITY; GONADECTOMY; HIPPOCAMPUS; HORMONAL REGULATION; MALE; MOUSE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SUBICULUM;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; DIHYDROTESTOSTERONE; DISEASE MODELS, ANIMAL; ESTRADIOL; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TAU PROTEINS; TESTOSTERONE;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 77957982982     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.08.068     Document Type: Article

References (72)

1. T.A. Almeida, and N. Papadopoulos Progression model of prostate cancer Methods Mol. Biol. 222 2003 211 222
2. M. Alvarez-de-la-Rosa, I. Silva, J. Nilsen, M.M. Perez, L.M. Garcia-Segura, J. Avila, and F. Naftolin Estradiol prevents neural tau hyperphosphorylation characteristic of Alzheimer's disease Ann. N.Y. Acad. Sci. 1052 2005 210 224
3. B. Attardi, L.N. Geller, and S. Ohno Androgen and estrogen receptors in brain cytosol from male, female, and testicular feminized (tfm/y hermaphrodite) mice Endocrinology 98 1976 864 874
4. T.S. Benice, and J. Raber Testosterone and dihydrotestosterone differentially improve cognition in aged female mice Learn. Mem. 16 2009 479 485
5. S. Bhasin, G.R. Cunningham, F.J. Hayes, A.M. Matsumoto, P.J. Snyder, R.S. Swerdloff, and V.M. Montori Testosterone therapy in adult men with androgen deficiency syndromes: an endocrine society clinical practice guideline J. Clin. Endocrinol. Metab. 91 2006 1995 2010
6. S. Bhasin, R.A. Parker, F. Sattler, R. Haubrich, B. Alston, T. Umbleja, C.M. Shikuma Team, A.C.T.G.P.A.S Effects of testosterone supplementation on whole body and regional fat mass and distribution in human immunodeficiency virus-infected men with abdominal obesity J. Clin. Endocrinol. Metab. 92 2007 1049 1057
7. H.A. Bimonte-Nelson Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats Exp. Neurol. 181 2003 301 312
8. R.L. Bowen, J.P. Isley, and R.L. Atkinson An association of elevated serum gonadotropin concentrations and Alzheimer disease? J. Neuroendocrinol. 12 2000 351 354
9. A. Caccamo, S. Oddo, L.X. Tran, and F.M. LaFerla Lithium reduces tau phosphorylation but not A beta or working memory deficits in a transgenic model with both plaques and tangles Am. J. Pathol. 170 2007 1669 1675
10. J.C. Carroll, and C.J. Pike Selective estrogen receptor modulators differentially regulate Alzheimer-like changes in female 3xTg-AD mice Endocrinology 149 2008 2607 2611
11. J.C. Carroll, E.R. Rosario, L. Chang, F.Z. Stanczyk, S. Oddo, F.M. LaFerla, and C.J. Pike Progesterone and estrogen regulate Alzheimer-like neuropathology in female 3xTg-AD mice J. Neurosci. 27 2007 13357 13365
12. M.M. Cherrier, S. Craft, and A.M. Matsumoto Cognitive changes associated with supplementation of testosterone or dihydrotestosterone in mildly hypogonadal men: a preliminary report J. Androl. 24 2003 568 576
13. M.M. Cherrier, A.M. Matsumoto, J.K. Amory, S. Asthana, W. Bremner, E.R. Peskind, M.A. Raskind, and S. Craft Testosterone improves spatial memory in men with Alzheimer disease and mild cognitive impairment Neurology 64 2005 2063 2068
14. B. Cooke, C.D. Hegstrom, L.S. Villeneuve, and S.M. Breedlove Sexual differentiation of the vertebrate brain: principles and mechanisms Front. Neuroendocrinol. 19 1998 323 362
15. B.J. Cummings, A. Manson, R. Kim, P. Sheu, and A. Anderson Optimization of techniques for the maximal detection and quantification of Alzheimer's-related neuropathology with digital imaging Neurobiol. Aging 23 2002 161 170
16. K.L. Edinger, and C.A. Frye Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5alpha-reduced metabolites in the hippocampus Behav. Neurosci. 118 2004 1352 1364
17. D.A. Evans, H.H. Funkenstein, M.S. Albert, P.A. Scherr, N.R. Cook, M.J. Chown, L.E. Hebert, C.H. Hennekens, and J.O. Taylor Prevalence of Alzheimer's disease in a community population of older persons. Higher than previously reported Jama 262 1989 2551 2556
18. E. Falkenstein, H.C. Tillmann, M. Christ, M. Feuring, and M. Wehling Multiple actions of steroid hormones-a focus on rapid, nongenomic effects Pharmacol. Rev. 52 2000 513 556
19. N.G. Forger Cell death and sexual differentiation of the nervous system Neuroscience 138 2006 929 938
20. C.A. Frye 5alpha-Reduced androgens may have actions in the hippocampus to enhance cognitive performance of male rats Psychoneuroendocrinology 29 2004 1019 1027
21. S. Gandy, O.P. Almeida, J. Fonte, D. Lim, A. Waterrus, N. Spry, L. Flicker, and R.N. Martins Chemical andropause and amyloid-beta peptide JAMA 285 2001 2195 2196
22. M.J. Gillett, R.N. Martins, R.M. Clarnette, S.A. Chubb, D.G. Bruce, and B.B. Yeap Relationship between testosterone, sex hormone binding globulin and plasma amyloid beta peptide 40 in older men with subjective memory loss or dementia J. Alzheimers Dis. 5 2003 267 269
23. S. Goodenough, S. Engert, and C. Behl Testosterone stimulates rapid secretory amyloid precursor protein release from rat hypothalamic cells via the activation of the mitogen-activated protein kinase pathway Neurosci. Lett. 296 2000 49 52
24. G.K. Gouras, H. Xu, R.S. Gross, J.P. Greenfield, B. Hai, R. Wang, and P. Greengard Testosterone reduces neuronal secretion of Alzheimer's beta-amyloid peptides PNAS 97 2000 1202 1205
25. R.J. Handa, T.R. Pak, A.E. Kudwa, T.D. Lund, and L. Hinds An alternate pathway for androgen regulation of brain function: activation of estrogen receptor beta by the metabolite of dihydrotestosterone, 5alpha-androstane-3beta, 17beta-diol Horm. Behav. 53 2008 741 752
26. R.J. Handa, M.J. Weiser, and D.G. Zuloaga A role for the androgen metabolite, 5alpha-androstane-3beta, 17beta-diol, in modulating oestrogen receptor beta-mediated regulation of hormonal stress reactivity J. Neuroendocrinol. 21 2009 351 358
27. J. Hardy Amyloid, the presenilins and Alzheimer's disease Trends Neurosci. 20 1997 154 159
28. E. Hogervorst, and S. Bandelow The controversy over levels of sex steroids in cases with Alzheimer's disease J. Neuroendocrinol. 16 2004 93 94
29. J.S. Janowsky The role of androgens in cognition and brain aging in men Neuroscience 138 2006 1015 1020
30. J.S. Janowsky Thinking with your gonads: testosterone and cognition Trends Cogn. Sci. 10 2006 77 82
31. A.F. Jorm, A.E. Korten, and A.S. Henderson The prevalence of dementia: a quantitative integration of the literature Acta Psychiatr. Scand. 76 1987 465 479
32. J.M. Kaufman, and A. Vermeulen The decline of androgen levels in elderly men and its clinical and therapeutic implications Endocr. Rev. 26 2005 833 876
33. J.E. Kerr, R.J. Allore, S.G. Beck, and R.J. Handa Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus Endocrinology 136 1995 3213 3221
34. M. Kitazawa, S. Oddo, T.R. Yamasaki, K.N. Green, and F.M. LaFerla Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease J. Neurosci. 25 2005 8843 8853
35. C. Leranth, O. Petnehazy, and N.J. MacLusky Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats J. Neurosci. 23 2003 1588 1592
36. C. Leranth, T. Hajszan, and N.J. MacLusky Androgens increase spine synapse density in the CA1 hippocampal subfield of ovariectomized female rats J. Neurosci. 24 2004 495 499 (Pubitemid 38112381)
37. X.A. Liu, L.Q. Zhu, Q. Zhang, H.R. Shi, S.H. Wang, Q. Wang, and J.Z. Wang Estradiol attenuates tau hyperphosphorylation induced by upregulation of protein kinase-A Neurochem. Res. 33 2008 1811 1820
38. T.D. Lund, L.R. Hinds, and R.J. Handa The androgen 5alpha- dihydrotestosterone and its metabolite 5alpha-androstan-3beta, 17beta-diol inhibit the hypothalamo-pituitary-adrenal response to stress by acting through estrogen receptor beta-expressing neurons in the hypothalamus J. Neurosci. 26 2006 1448 1456
39. S.V. Meethal, M.A. Smith, R.L. Bowen, and C.S. Atwood The gonadotropin connection in Alzheimer's disease Endocrinology 26 2005 317 326
40. R.D. Mehra, K. Sharma, C. Nyakas, and U. Vij Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study Brain Res. 1056 2005 22 35
41. S.D. Moffat Effects of testosterone on cognitive and brain aging in elderly men Ann. N.Y. Acad. Sci. 1055 2005 80 92
42. S. Oddo, A. Caccamo, M. Kitazawa, B.P. Tseng, and F.M. LaFerla Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease Neurobiol. Aging 24 2003 1063 1070
43. S. Oddo, A. Caccamo, J.D. Shepherd, M.P. Murphy, T.E. Golde, R. Kayed, R. Metherate, M.P. Mattson, Y. Akbari, and F.M. LaFerla Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction Neuron 39 2003 409 421
44. S. Oddo, V. Vasilevko, A. Caccamo, M. Kitazawa, D.H. Cribbs, and F.M. Laferla Reduction of soluble Abeta and tau, but not soluble Abeta alone, ameliorates cognitive decline in transgenic mice with plaques and tangles J. Biol. Chem. 281 2006 39413 39423
45. T.R. Pak, W.C. Chung, T.D. Lund, L.R. Hinds, C.M. Clay, and R.J. Handa The androgen metabolite, 5alpha-androstane-3beta, 17beta-diol, is a potent modulator of estrogen receptor-beta1-mediated gene transcription in neuronal cells Endocrinology 146 2005 147 155
46. S.C. Papasozomenos The heat shock-induced hyperphosphorylation of tau is estrogen-independent and prevented by androgens: implications for Alzheimer disease Proc. Natl. Acad. Sci. USA 94 1997 6612 6617
47. S.C.h. Papasozomenos, and A. Shanavas Testosterone prevents the heat shock-induced overactivation of glycogen synthase kinase-3 beta but not of cyclin-dependent kinase 5 and c-Jun NH2-terminal kinase and concomitantly abolishes hyperphosphorylation of tau: implications for Alzheimer's disease Proc. Natl. Acad. Sci. USA 99 2002 1140 1145
48. C.J. Pike Estrogen modulates neuronal Bcl-xL expression and beta-amyloid-induced apoptosis: relevance to Alzheimer's disease J. Neurochem. 72 1999 1552 1563
49. C.J. Pike Testosterone attenuates beta-amyloid toxicity in cultured hippocampal neurons Brain Res. 919 2001 160 165
50. C.J. Pike, J.C. Carroll, E.R. Rosario, and A.M. Barron Protective actions of sex steroid hormones in Alzheimer's disease Front. Neuroendocrinol. 30 2009 239 258
51. J. Raber AR, apoE, and cognitive function Horm. Behav. 53 2008 706 715
52. M. Ramsden, A.C. Nyborg, M.P. Murphy, L. Chang, F.Z. Stanczyk, T.E. Golde, and C.J. Pike Androgens modulate beta-amyloid levels in male rat brain J. Neurochem. 87 2003 1052 1055
53. M. Ramsden, T.M. Shin, and C.J. Pike Androgens modulate neuronal vulnerability to kainate lesion Neuroscience 122 2003 573 578
54. W.A. Rocca, L.A. Amaducci, and B.S. Schoenberg Epidemiology of clinically diagnosed Alzheimer's disease Ann. Neurol. 19 1986 415 424
55. E.R. Rosario, and C.J. Pike Androgen regulation of beta-amyloid protein and the risk of Alzheimer's disease Brain Res. Rev. 57 2008 444 453
56. E.R. Rosario, L. Chang, F.Z. Stanczyk, and C.J. Pike Age-related testosterone depletion and the development of Alzheimer disease JAMA 292 2004 1431 1432
57. E.R. Rosario, J.C. Carroll, S. Oddo, F.M. LaFerla, and C.J. Pike Androgens regulate the development of neuropathology in a triple transgenic mouse model of Alzheimer's disease J. Neurosci. 26 2006 13384 13389
58. Rosario, E.R., Chang, L., Head, E.H., Stanczyk, F. Z., Pike, C. J., 2009. Brain levels of sex steroid hormones in men and women during normal aging and in Alzheimer's disease Neurobiol Aging. Electronic publication ahead of print (May 9th 2009).
59. P.J. Shughrue, M.V. Lane, and I. Merchenthaler Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system J. Comp. Neurol. 388 1997 507 525
60. R.B. Simerly, C. Chang, M. Muramatsu, and L.W. Swanson Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study J. Comp. Neurol. 294 1990 76 95
61. 125I-iodinated estrogen derivatives in human breast cancer cells (MCF-7) J. Steroid Biochem. Mol. Biol. 44 1993 105 112
62. J.O. Strom, A. Theodorsson, and E. Theodorsson Order of magnitude differences between methods for maintaining physiological 17beta-oestradiol concentrations in ovariectomized rats Scand. J. Clin. Lab. Invest. 68 2008 814 822
63. J.O. Strom, A. Theodorsson, and E. Theodorsson Dose-related neuroprotective versus neurodamaging effects of estrogens in rat cerebral ischemia: a systematic analysis J. Cereb. Blood Flow Metab. 29 2009 1359 1372
64. E.J. Wahjoepramono, L.K. Wijaya, K. Taddei, G. Martins, M. Howard, K. de Ruyck, K. Bates, S.S. Dhaliwal, G. Verdile, M. Carruthers, and R.N. Martins Distinct effects of testosterone on plasma and cerebrospinal fluid amyloid-beta levels J. Alzheimers Dis. 15 2008 129 137
65. Z. Weihua, S. Makela, L.C. Andersson, S. Salmi, S. Saji, J.I. Webster, E.V. Jensen, S. Nilsson, M. Warner, and J. Gustafsson A role for estrogen receptor β in the regulation of growth of the ventral prostate Proc. Natl. Acad. Sci. 2001 6330 6335
66. Z. Weihua, R. Lathe, M. Warner, and J.A. Gustafsson An endocrine pathway in the prostate, ERbeta, AR, 5alpha-androstane-3beta, 17beta-diol, and CYP7B1, regulates prostate growth Proc. Natl. Acad. Sci. USA 99 2002 13589 13594
67. C.S. Woolley, and B.S. McEwen Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat J. Neurosci. 12 1992 2549 2554
68. C.S. Woolley, and B.S. McEwen Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism J. Neurosci. 14 1994 7680 7687
69. T. Yamane, Y. Kitamura, N. Terada, and K. Matsumoto Proliferative response of seminal vesicle cells to androgen and estrogen in neonatally castrated mice J. Steroid Biochem. 24 1986 703 708
70. M. Yao, T.V. Nguyen, E.R. Rosario, M. Ramsden, and C.J. Pike Androgens regulate neprilysin expression: role in reducing beta-amyloid levels J. Neurochem. 105 2008 2477 2488
71. Q.G. Zhang, R. Wang, M. Khan, V. Mahesh, and D.W. Brann Role of Dickkopf-1, an antagonist of the Wnt/beta-catenin signaling pathway, in estrogen-induced neuroprotection and attenuation of tau phosphorylation J. Neurosci. 28 2008 8430 8441
72. L. Zhao, J. Yao, Z. Mao, S. Chen, Y. Wang, and R.D. Brinton 17beta-Estradiol regulates insulin-degrading enzyme expression via an ERbeta/PI3-K pathway in hippocampus: Relevance to Alzheimer's prevention Neurobiol. Aging 2010 Electronic publication ahead of print (Jan. 4th 2010)