Interaction of APOE genotype and testosterone on episodic memory in middle-aged men

Neurobiology of Aging

Volumn 35, Issue 7, 2014, Pages 1778.e1-1778.e8

  Panizzon, Matthew S ^a,b   Hauger, Richard ^a,c   Xian, Hong ^d,e   Vuoksimaa, Eero ^a,b,f   Spoon, Kelly M ^g   Mendoza, Sally P ^h   Jacobson, Kristen C ⁱ   Vasilopoulos, Terrie ⁱ   Rana, Brinda K ^a,b   McKenzie, Ruth ^j   McCaffery, Jeanne M ^k   Lyons, Michael J ^j   Kremen, William S ^a,b,c   Franz, Carol E ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^d SAINT LOUIS UNIVERSITY   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f UNIVERSITY OF HELSINKI   (Finland)

^g SAN DIEGO STATE UNIVERSITY   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ UNIVERSITY OF CHICAGO   (United States)

^j BOSTON UNIVERSITY   (United States)

^k BROWN UNIVERSITY   (United States)

more..

Author keywords

APOE; Episodic memory; Gene hormone interaction; Middle age; Testosterone

Indexed keywords

TESTOSTERONE;

ADULT; AGING; ALLELE; APOE GENE; ARTICLE; CAUCASIAN; DEMENTIA; EPISODIC MEMORY; GENE; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENOTYPE; HETEROZYGOTE; HUMAN; HUMAN EXPERIMENT; LONGITUDINAL STUDY; MALE; MIDDLE AGED; PRIORITY JOURNAL; SOLDIER; VIET NAM;

APOE; EPISODIC MEMORY; GENE-HORMONE INTERACTION; MIDDLE-AGE; TESTOSTERONE;

AGING; ALLELES; APOLIPOPROTEIN E4; COGNITION; COGNITION DISORDERS; DEMENTIA; GENETIC PREDISPOSITION TO DISEASE; HETEROZYGOTE; HUMANS; MALE; MEMORY, EPISODIC; MIDDLE AGED; RISK FACTORS; TESTOSTERONE; TWIN STUDIES AS TOPIC; VERBAL BEHAVIOR;

EID: 85058205835     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.12.025     Document Type: Article

References (99)

1. Abdelgadir S.E., Roselli C.E., Choate J.V., Resko J.A. Androgen receptor messenger ribonucleic acid in brains and pituitaries of male rhesus monkeys: studies on distribution, hormonal control, and relationship to luteinizing hormone secretion. Biol. Reprod. 1999, 60:1251-1256.
2. Bachmann G., Bancroft J., Braunstein G., Burger H., Davis S., Dennerstein L., Goldstein I., Guay A., Leiblum S., Lobo R., Notelovitz M., Rosen R., Sarrel P., Sherwin B., Simon J., Simpson E., Shifren J., Spark R., Traish A. Female androgen insufficiency: the Princeton consensus statement on definition, classification, and assessment. Fertil. Sterility 2002, 77:660-665.
3. Barrett-Connor E., Goodman-Gruen D., Patay B. Endogenous sex hormones and cognitive function in older men. J.Clin. Endocrinol. Metab. 1999, 84:3681-3685.
4. Beauchet O. Testosterone and cognitive function: current clinical evidence of a relationship. Eur. J. Endocrinol. 2006, 155:773-781.
5. Belsky J., Bakermans-Kranenburg M.J., van IJzendoorn M.H. For better and for worse: differential susceptibility to environmental influences. Psychol. Sci. 2007, 16:300-304.
6. Belsky J., Jonassaint C., Pluess M., Stanton M., Brummett B., Williams R. Vulnerability genes or plasticity genes?. Mol. Psychiatry 2009, 14:746-754.
7. Bender A.R., Raz N. Age-related differences in episodic memory: a synergistic contribution of genetic and physiological vascular risk factors. Neuropsychology 2012, 26:442-450.
8. Bennett N.C., Gardiner R.A., Hooper J.D., Johnson D.W., Gobe G.C. Molecular cell biology of androgen receptor signalling. Int. J. Biochem. Cell Biol. 2010, 42:813-827.
9. Beyenburg S., Watzka M., Clusmann H., Blumcke I., Bidlingmaier F., Elger C.E., Stoffel-Wagner B. Androgen receptor mRNA expression in the human hippocampus. Neurosci. Lett. 2000, 294:25-28.
10. Bezdickova M., Molikova R., Bebarova L., Kolar Z. Distribution of nuclear receptors for steroid hormones in the human brain: a preliminary study. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 2007, 151:69-71.
11. Bondi M.W., Jak A.J., Delano-Wood L., Jacobson M.W., Delis D.C., Salmon D.P. Neuropsychological contributions to the early identification of Alzheimer's disease. Neuropsychological Rev. 2008, 18:73-90.
12. Brinton R.D. Investigative models for determining hormone therapy-induced outcomes in brain: evidence in support of a healthy cell bias of estrogen action. Ann. New York Acad. Sci. 2005, 1052:57-74.
13. Brooks B.L., Weaver L.E., Scialfa C.T. Does impaired executive functioning differentially impact verbal memory measures in older adults with suspected dementia?. Clin. Neuropsychol. 2006, 20:230-242.
14. Buckner R.L. Memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron 2004, 44:195-208.
15. Burkhardt M.S., Foster J.K., Clarnette R.M., Chubb S.A., Bruce D.G., Drummond P.D., Martins R.N., Yeap B.B. Interaction between testosterone and apolipoprotein E epsilon4 status on cognition in healthy older men. J.Clin. Endocrinol. Metab. 2006, 91:1168-1172.
16. Public health and aging: trends in aging-United States and worldwide. MMWR CDC Surveill. Summ. 2003, 52:101-106. Centers for Disease Control and Prevention.
17. Charlson M., Szatrowski T.P., Peterson J., Gold J. Validation of a combined comorbidity index. J.Clin. Epidemiol. 1994, 47:1245-1251.
18. Charlson M.E., Pompei P., Ales K.L., MacKenzie C.R. Anew method of classifying prognostic comorbidity in longitudinal studies: development and validation. J.Chronic Dis. 1987, 40:373-383.
19. Cherrier M.M., Matsumoto A.M., Amory J.K., Ahmed S., Bremner W., Peskind E.R., Raskind M.A., Johnson M., Craft S. The role of aromatization in testosterone supplementation: effects on cognition in older men. Neurology 2005, 64:290-296.
20. Chu L.W., Tam S., Lee P.W., Wong R.L., Yik P.Y., Tsui W., Song Y., Cheung B.M., Morley J.E., Lam K.S. Bioavailable testosterone is associated with a reduced risk of amnestic mild cognitive impairment in older men. Clin. Endocrinol. 2008, 68:589-598.
21. Chu L.W., Tam S., Wong R.L., Yik P.Y., Song Y., Cheung B.M., Morley J.E., Lam K.S. Bioavailable testosterone predicts a lower risk of Alzheimer's disease in older men. J.Alzheimer's Dis. 2010, 21:1335-1345.
22. Dalton J.T., Gao W. Androgen receptor. Nuclear Receptors, Proteins and Cell Regulation 2010, 143-182. Springer Science and Business Media, London, UK. C.M. Bunce, M.J. Campbell (Eds.).
23. de Frias C.M., Bunce D., Wahlin A., Adolfsson R., Sleegers K., Cruts M., Van Broeckhoven C., Nilsson L.G. Cholesterol and triglycerides moderate the effect of apolipoprotein E on memory functioning in older adults. J.Gerontol. B Psychol. Sci. Soc. Sci. 2007, 62:112-118.
24. Delis D.C., Kramer J.H., Kaplan E., Ober B.A. California Verbal Learning Test-Second Edition 2000, The Psychological Corporation, San Antonio, Texas.
25. Diver M.J., Imtiaz K.E., Ahmad A.M., Vora J.P., Fraser W.D. Diurnal rhythms of serum total, free and bioavailable testosterone and of SHBG in middle-aged men compared with those in young men. Clin. Endocrinol. 2003, 58:710-717.
26. Edinger K.L., Frye C.A. Androgens' performance-enhancing effects in the inhibitory avoidance and water maze tasks may involve actions at intracellular androgen receptors in the dorsal hippocampus. Neurobiol. Learn. Mem. 2007, 87:201-208.
27. Edinger K.L., Lee B., Frye C.A. Mnemonic effects of testosterone and its 5alpha-reduced metabolites in the conditioned fear and inhibitory avoidance tasks. Pharmacol. Biochem. Behav. 2004, 78:559-568.
28. Emi M., Wu L.L., Robertson M.A., Myers R.L., Hegele R.A., Williams R.R., White R., Lalouel J.M. Genotyping and sequence analysis of apolipoprotein E isoforms. Genomics 1988, 3:373-379.
29. Feldman H.A., Longcope C., Derby C.A., Johannes C.B., Araujo A.B., Coviello A.D., Bremner W.J., McKinlay J.B. Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts male aging study. J.Clin. Endocrinol. Metab. 2002, 87:589-598.
30. Fernandez-Guasti A., Kruijver F.P., Fodor M., Swaab D.F. Sex differences in the distribution of androgen receptors in the human hypothalamus. J.Comparitive Neurol. 2000, 425:422-435.
31. Ferrini R.L., Barrett-Connor E. Sex hormones and age: a cross-sectional study of testosterone and estradiol and their bioavailable fractions in community-dwelling men. Am. J. Epidemiol. 1998, 147:750-754.
32. Finley S.K., Kritzer M.F. Immunoreactivity for intracellular androgen receptors in identified subpopulations of neurons, astrocytes and oligodendrocytes in primate prefrontal cortex. J.Neurobiol. 1999, 40:446-457.
33. Franz C.E., York T.P., Eaves L.J., Mendoza S.P., Hauger R.L., Hellhammer D.H., Jacobson K.C., Levine S., Lupien S.J., Lyons M.J., Prom-Wormley E., Xian H., Kremen W.S. Genetic and environmental influences on cortisol regulation across days and contexts in middle-aged men. Behav. Genet. 2010, 40:467-479.
34. Garcia-Ovejero D., Azcoitia I., Doncarlos L.L., Melcangi R.C., Garcia-Segura L.M. Glia-neuron crosstalk in the neuroprotective mechanisms of sex steroid hormones. Brain Res. Rev. 2005, 48:273-286.
35. Gerritsen L., Comijs H.C., Deeg D.J., Penninx B.W., Geerlings M.I. Salivary cortisol, APOE-epsilon4 allele and cognitive decline in a prospective study of older persons. Neurobiol. Aging 2011, 32:1615-1625.
36. Goldberg J., Curran B., Vitek M.E., Henderson W.G., Boyko E.J. The Vietnam era twin registry. Twin Res. Hum. Genet. 2002, 5:476-481.
37. Gouras G.K., Xu H., Gross R.S., Greenfield J.P., Hai B., Wang R., Greengard P. Testosterone reduces neuronal secretion of Alzheimer's beta-amyloid peptides. Proc. Natl. Acad. Sci. 2000, 97:1202-1205.
38. Granger D.A., Schwartz E.B., Booth A., Arentz M. Salivary testosterone determination in studies of child health and development. Horm. Behav. 1999, 35:18-27.
39. Haan M.N., Shemanski L., Jagust W.J., Manolio T.A., Kuller L. The role of APOE epsilon 4 in modulating effects of other risk factors for cognitive decline in elderly persons. J.Am. Med. Assoc. 1999, 282:40-46.
40. Harman S.M., Metter E.J., Tobin J.D., Pearson J., Blackman M.R. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore Longitudinal Study of Aging. J.Clin. Endocrinol. Metab. 2001, 86:724-731.
41. Head D., Snyder A., Girton L., Morris J., Buckner R. Frontal-hippocampal double dissociation between normal aging and Alzheimer's disease. Cereb. Cortex 2005, 15:732-739.
42. Hixson J.E., Vernier D.T. Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J.Lipid Res. 1990, 31:545-548.
43. Hogervorst E., Bandelow S., Combrinck M., Smith A.D. Low free testosterone is an independent risk factor for Alzheimer's disease. Exp. Gerontol. 2004, 39:1633-1639.
44. Hogervorst E., Combrinck M., Smith A.D. Testosterone and gonadotropin levels in men with dementia. Neuro. Endocrinol. Lett. 2003, 24:203-208.
45. Hogervorst E., Lehmann D.J., Warden D.R., McBroom J., Smith A.D. Apolipoprotein E epsilon4 and testosterone interact in the risk of Alzheimer's disease in men. Int. J. Geriat. Psychiatry 2002, 17:938-940.
46. Hogervorst E., Williams J., Budge M., Barnetson L., Combrinck M., Smith A.D. Serum total testosterone is lower in men with Alzheimer's disease. Neuro. Endocrinol. Lett. 2001, 22:163-168.
47. Holland J., Bandelow S., Hogervorst E. Testosterone levels and cognition in elderly men: a review. Maturitas 2011, 69:322-337.
48. Kerr J.E., Allore R.J., Beck S.G., Handa R.J. Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology 1995, 136:3213-3221.
49. Kremen W.S., Franz C.E., Lyons M.J. VETSA: the Vietnam era twin study of aging. Twin Res. Hum. Genet. 2013, 16:399-402.
50. Kremen W.S., Thompson-Brenner H., Leung Y.J., Grant M.D., Franz C.E., Eisen S.A., Jacobson K.C., Boake C., Lyons M.J. Genes, environment, and time: theVietnam era twin study of aging (VETSA). Twin Res. Hum. Genet. 2006, 9:1009-1022.
51. Kritzer M. The distribution of immunoreactivity for intracellular androgen receptors in the cerebral cortex of hormonally intact adult male and female rats: localization in pyramidal neurons making corticocortical connections. Cereb. Cortex 2004, 14:268-280.
52. Kritzer M.F., McLaughlin P.J., Smirlis T., Robinson J.K. Gonadectomy impairs T-maze acquisition in adult male rats. Horm. Behav. 2001, 39:167-174.
53. Lee B.K., Glass T.A., James B.D., Bandeen-Roche K., Schwartz B.S. Neighborhood psychosocial environment, apolipoprotein E genotype, and cognitive function in older adults. Arch. Gen. Psychiatry 2011, 68:314-321.
54. Lee B.K., Glass T.A., McAtee M.J., Wand G.S., Bandeen-Roche K., Bolla K.I., Schwartz B.S. Associations of salivary cortisol with cognitive function in the Baltimore memory study. Arch. Gen. Psychiatry 2007, 64:810-818.
55. Lee B.K., Glass T.A., Wand G.S., McAtee M.J., Bandeen-Roche K., Bolla K.I., Schwartz B.S. Apolipoprotein e genotype, cortisol, and cognitive function in community-dwelling older adults. Am. J. Psychiatry 2008, 165:1456-1464.
56. Lupien S.J., Leon M.D., Santi S.D., Convit A., Tarshish C., Nair N.P.V., Thakur M., McEwen B.S., Hauger R.L., Meaney M.J. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat. Neurosci. 1998, 1:69-73.
57. Lyons M.J., Genderson M., Grant M.D., Logue M., Zink T., McKenzie R., Franz C.E., Panizzon M.S., Lohr J.B., Jerskey B., Kremen W.S. Gene-environment interaction of ApoE genotype and combat exposure on PTSD. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2013, 162B:762-769.
58. Lyons M.J., York T.P., Franz C.E., Grant M.D., Eaves L.J., Jacobson K., Schaie K.W., Panizzon M.S., Boake C., Xian H., Toomey R., Eisen S.A., Kremen W.S. Genes determine stability and the environment determines change in cognitive ability during 35 years of adulthood. Psychol. Sci. 2009, 20:1146-1152.
59. Maggio M., Dall'Aglio E., Lauretani F., Cattabiani C., Ceresini G., Caffarra P., Valenti G., Volpi R., Vignali A., Schiavi G., Ceda G.P. The hormonal pathway to cognitive impairment in older men. J.Nutr. Health Aging 2012, 16:40-54.
60. McGrevy D.F., Knouse S.B., Thompson R.A. Relationships Among an Individual Intelligence Test and Two Air Force Screening and Selection Tests. Personnel Research Division, Air Force Human Resources Laboratory Technical Report, AFHRL-tr-74-25 1974, Brooks Air Force Base, TX.
61. Moffat S.D., Zonderman A.B., Metter E.J., Blackman M.R., Harman S.M., Resnick S.M. Longitudinal assessment of serum free testosterone concentration predicts memory performance and cognitive status in elderly men. J.Clin. Endocrinol. Metab. 2002, 87:5001-5007.
62. Moffat S.D., Zonderman A.B., Metter E.J., Kawas C., Blackman M.R., Harman S.M., Resnick S.M. Free testosterone and risk for Alzheimer disease in older men. Neurology 2004, 62:188-193.
63. Morley J.E. Androgens and aging. Maturitas 2001, 38:61-71.
64. Muller M., den Tonkelaar I., Thijssen J.H., Grobbee D.E., van der Schouw Y.T. Endogenous sex hormones in men aged 40-80 years. Eur. J. Endocrinol. 2003, 149:583-589.
65. Nguyen T.V., Jayaraman A., Quaglino A., Pike C.J. Androgens selectively protect against apoptosis in hippocampal neurons. J.Neuroendocrinol. 2010, 22:1013-1022.
66. Panizzon M.S., Hauger R., Dale A.M., Eaves L.J., Eyler L.T., Fischl B., Fennema-Notestine C., Franz C.E., Grant M.D., Jak A.J., Jacobson K., Lyons M.J., Mendoza S.P., Neale M.C., Prom-Wormley E., Seidman L., Tsuang M.T., Xian H., Kremen W.S. Testosterone modifies the effect of APOE genotype on hippocampal volume in middle-aged men. Neurology 2010, 75:874-880.
67. Panizzon M.S., Hauger R., Jacobson K.C., Eaves L.J., York T.P., Prom-Wormley E., Grant M.D., Lyons M.J., McKenzie R., Mendoza S.P., Xian H., Franz C.E., Kremen W.S. Genetic and environmental influences of daily and intra-individual variation in testosterone levels in middle-aged men. Psychoneuroendocrinology 2013, 38:2163-2172.
68. Paoletti A.M., Congia S., Lello S., Tedde D., Orru M., Pistis M., Pilloni M., Zedda P., Loddo A., Melis G.B. Low androgenization index in elderly women and elderly men with Alzheimer's disease. Neurology 2004, 62:301-303.
69. Papasozomenos S., Shanavas A. 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. U.S.A 2002, 99:1140-1145.
70. Park S.Y., Tournell C., Sinjoanu R.C., Ferreira A. Caspase-3- and calpain-mediated tau cleavage are differentially prevented by estrogen and testosterone in beta-amyloid-treated hippocampal neurons. Neuroscience 2007, 144:119-127.
71. Peavy G.M., Lange K.L., Salmon D.P., Patterson T.L., Goldman S., Gamst A.C., Mills P.J., Khandrika S., Galasko D. The effects of prolonged stress and APOE genotype on memory and cortisol in older adults. Biol. Psychiatry 2007, 62:472-478.
72. Pike C.J. Testosterone attenuates beta-amyloid toxicity in cultured hippocampal neurons. Brain Res. 2001, 919:160-165.
73. Pike C.J., Rosario E.R., Nguyen T.V. Androgens, aging, and Alzheimer's disease. Endocrine 2006, 29:233-241.
74. Puy L., MacLusky N.J., Becker L., Karsan N., Trachtenberg J., Brown T.J. Immunocytochemical detection of androgen receptor in human temporal cortex characterization and application of polyclonal androgen receptor antibodies in frozen and paraffin-embedded tissues. J.Steroid Biochem. Mol. Biol. 1995, 55:197-209.
75. Raber J. Androgens, apoE, and Alzheimer's disease. Sci. Aging Knowledge Environ. 2004, 2004:1-11.
76. Raber J. AR, apoE, and cognitive function. Horm. Behav. 2008, 53:706-715.
77. Raber J., Bongers G., LeFevour A., Buttini M., Mucke L. Androgens protect against apolipoprotein E4-induced cognitive deficits. J.Neurosci. 2002, 22:5204-5209.
78. Radloff L.S. The CES-D scale: a self-report depression scale for research in the general population. Appl. Psychol. Meas. 1977, 1:385-401.
79. Rizk-Jackson A., Robertson J., Raber J. Tfm-AR modulates the effects of ApoE4 on cognition. J.Neurochem. 2008, 105:63-67.
80. Rosario E.R., Carroll J.C., Oddo S., LaFerla F.M., Pike C.J. Androgens regulate the development of neuropathology in a triple transgenic mouse model of Alzheimer's disease. J.Neurosci. 2006, 26:13384-13389.
81. Rosario E.R., Chang L., Head E.H., Stanczyk F.Z., Pike C.J. Brain levels of sexsteroid hormones in men and women during normal aging and in Alzheimer's disease. Neurobiol. Aging 2011, 32:604-613. 10.1016/j.neurobiolaging.2009.04.008.
82. Roy T.A., Blackman M.R., Harman S.M., Tobin J.D., Schrager M., Metter E.J. Interrelationships of serum testosterone and free testosterone index with FFM and strength in aging men. Am. J. Physiol. Endocrinol. Metab. 2002, 283:E284-E294.
83. Sarrieau A., Mitchell J.B., Lal S., Olivier A., Quirion R., Meaney M.J. Androgen binding sites in human temporal cortex. Neuroendocrinology 1990, 51:713-716.
84. Saunders A.M., Strittmatter W.J., Schmechel D., George-Hyslop P.H., Pericak-Vance M.A., Joo S.H., Rosi B.L., Gusella J.F., Crapper-MacLachlan D.R., Alberts M.J., Hulette C., Crain B., Goldgaber D., Roses A.D. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology 1993, 43:1467-1472.
85. Schafer J.H., Glass T.A., Bolla K.I., Mintz M., Jedlicka A.E., Schwartz B.S. Homocysteine and cognitive function in a population-based study of older adults. J.Am. Geriatr. Soc. 2005, 53:381-388.
86. Simerly R.B., Chang C., Muramatsu M., Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J.Comp. Neurol. 1990, 294:76-95.
87. Spritzer M.D., Daviau E.D., Coneeny M.K., Engelman S.M., Prince W.T. Effects of testosterone on spatial learning and memory in adult male rats. Horm. Behav. 2011, 59:484-496.
88. Stanworth R.D., Jones T.H. Testosterone for the aging male; current evidence and recommended practice. Clin. Interv. Aging 2008, 3:25-44.
89. Thilers P.P., Macdonald S.W., Herlitz A. The association between endogenous free testosterone and cognitive performance: a population-based study in 35 to 90 year-old men and women. Psychoneuroendocrinology 2006, 31:565-576.
90. Tohgi H., Utsugisawa K., Yamagata M., Yoshimura M. Effects of age on messenger RNA expression of glucocorticoid, thyroid hormone, androgen, and estrogen receptors in postmortem human hippocampus. Brain Res. 1995, 700:245-253.
91. Tremont G., Halpert S., Javorsky D.J., Stern R.A. Differential impact of executive dysfunction on verbal list learning and story recall. Clin. Neuropsychol. 2000, 14:295-302.
92. Veiga S., Melcangi R.C., Doncarlos L.L., Garcia-Segura L.M., Azcoitia I. Sex hormones and brain aging. Exp. Gerontol. 2004, 39:1623-1631.
93. Vermeulen A. Andropause. Maturitas 2000, 34:5-15.
94. Watanabe T., Koba S., Kawamura M., Itokawa M., Idei T., Nakagawa Y., Iguchi T., Katagiri T. Small dense low-density lipoprotein and carotid atherosclerosis in relation to vascular dementia. Metabolism 2004, 53:476-482.
95. Wechsler D. Manual for the Wechsler Memory Scale-Third Edition 1997, Psychological Corporation, San Antonio, TX.
96. Wisdom N.M., Callahan J.L., Hawkins K.A. The effects of apolipoprotein E on non-impaired cognitive functioning: a meta-analysis. Neurobiol. Aging 2011, 32:63-74.
97. Zade D., Beiser A., McGlinchey R., Au R., Seshadri S., Palumbo C., Wolf P.A., Decarli C., Milberg W. Interactive effects of apolipoprotein E type 4 genotype and cerebrovascular risk on neuropsychological performance and structural brain changes. J.Stroke Cerebrovasc. Disord. 2010, 19:261-268.
98. Zarrouf F.A., Artz S., Griffith J., Sirbu C., Kommor M. Testosterone and depression: systematic review and meta-analysis. J.Psychiatr. Pract. 2009, 15:289-305.
99. Zimmerman M.E., Lipton R.B., Santoro N., McConnell D.S., Derby C.A., Katz M.J., Baigi K., Saunders-Pullman R. Endogenous estradiol is associated with verbal memory in nondemented older men. Brain Cogn. 2011, 76:158-165.