Gender-specific neuroimmunoendocrine aging in a triple-transgenic 3×Tg-AD mouse model for Alzheimer's disease and its relation with longevity

NeuroImmunoModulation

Volumn 15, Issue 4-6, 2008, Pages 331-343

  Giménez Llort, Lydia ^a,c   Arranz, Lorena ^b   Maté, Ianire ^b   De La Fuente, Mónica ^b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c INSTITUT DE NEUROCIÈNCIES   (Spain)

Author keywords

3 Tg AD mice; Anxiety; Behavioral and psychological symptoms of dementia; Chemotaxis; Immunosenescence; Leukocytes; Lymphoproliferation; Stress; Triple transgenic

Indexed keywords

CHEMOKINE; CYTOKINE; INTERLEUKIN 1; NITROGEN DERIVATIVE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ASTROCYTE; BEHAVIOR; CYTOKINE PRODUCTION; ENDOCRINE SYSTEM; FEMALE; HOMEOSTASIS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE SYSTEM; IMMUNOMODULATION; INFLAMMATION; LIFESPAN; MALE; MICROGLIA; MORBIDITY; MORTALITY; MOUSE; NERVOUS SYSTEM; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SENESCENCE; SEX DIFFERENCE; TRANSGENIC MOUSE;

EID: 57149089661     PISSN: 10217401     EISSN: None     Source Type: Journal    
DOI: 10.1159/000156475     Document Type: Review

References (90)

1. DeKosky ST, Scheff SW: Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 1990;27:457-464.
2. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R: Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991;30:572-580.
3. Dringenberg HC: Alzheimer's disease:more than a 'cholinergic disorder' - evidence that cholinergic-monoaminergic interactions contribute to EEG slowing and dementia. Behav Brain Res 2000;115:235-249.
4. McGeer PL, Itagaki S, McGeer EG: Expression of the histocompatibility glycoprotein HLA-DR in neurological disease. Acta Neuropathol 1988;76:550-557.
5. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer Pl, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, Van Muiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T: Inflammation and Alzheimer's disease. Neurobiol Aging 2000;21:383-421.
6. Sasaki A, Shoji M, Harigaya Y, Kawarabayashi T, Ikeda M, Naito M, Matsubara E, Abe K, Nakazato Y: Amyloid cored plaques in Tg2576 transgenic mice are characterized by giant plaques, slightly activated microglia, and the lack of paired helical filament-typed, dystrophic neurites. Virchows Arch 2002;441:358-367.
7. Eikelenboom P, Veerhuis R, Scheper W, Rozemuller AJ, van Gool WA, Hoozemans JJ: The significance of neuroinflammation in understanding Alzheimer's disease. J Neural Transm 2006;113:1685-1695.
8. Kitazawa M, Oddo S, Yamasaki TR, Green KN, LaFerla FM: Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J Neurosci 2005;25:8843-8853.
9. Mattson MP: Pathways towards and away from Alzheimer's disease. Nature 2004;430:631-639.
10. Giménez-Llort L, Blázquez G, Cañete T, Johansson B, Oddo S, Tobeña A, LaFerla FM, Fernández-Teruel A: Modeling behavioral and neuronal symptoms of Alzheimer's disease in mice: a role for intraneuronal amyloid. Neurosci Biobehav Rev 2007;31:125-147.
11. Selkoe DJ: Toward a comprehensive theory for Alzheimer's disease. Hypothesis: Alzheimer's disease is caused by the cerebral accumulation and cytotoxicity of amyloid β-protein. Ann NY Acad Sci 2000;924:17-25.
12. Bartus RT: On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol 2000;163:495-529.
13. Lai F, Williams RS: A prospective study of Alzheimer disease in Down syndrome. Archives Neurol 1989;46:849-853.
14. Janus C, Westaway D: Transgenic mouse models of Alzheimer's disease. Physiol Behav 2001;73:873-886.
15. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM: Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Aβ and synaptic dysfunction. Neurone 2003;39:409-421.
16. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM: Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 2003;24:1063-1070.
17. Oddo S, Caccamo A, Green, KN, Liang K, Tran L, Chen Y, Leslie FM, LaFerla FM: Chronic nicotine administration exacerbates tau pathology in transgenic model of Alzheimer's disease. Proc Natl Acad Sci USA 2005;102:3046-3051.
18. Billings L, Oddo S, Green KN, McGaugh JL, LaFerla FM: Intraneuronal Aβ causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neurone 2005;45:675-688.
19. Fabris N: A neuroendocrine-immune theory of aging. Int J Neurosci 1990;51:373-375.
20. Bellinger DL, Madden KS, Lorton D, Thyagarajan S, Felten DL: Age-related alterations in neural-immune interactions and neural strategies in immunosenescence; in Ader R, Felten DL, Cohen N (eds): Psychoneuroimmunology. San Diego, Academic Press, 2001, pp 241-286.
21. De la Fuente M, Medina S: NPY and phagocytic cell functions; in Zukowska Z, Feuerstein GZ (eds): The NPY Family of Peptides in Immune Disorders, Inflammation, Angiogenesis and Cancer. Basel, Birkhäuser Verlag, 2005, pp 107-122.
22. De la Fuente M, Hernanz A, Vallejo, MC: The immune system in the oxidation stress conditions of aging and hypertension: favorable effects of antioxidants and physical exercise. Antioxid Redox Signal 2005;7:1356-1366.
23. Merril JE: Production and influence of inflammatory cytokines in diseases of the adult central nervous system; in Ader R, Felten DL, Cohen N (eds): Psychoneuroimmunology. San Diego, Academic Press, 2001, pp 547-561.
24. De la Fuente M, Del Rio M, Medina S: Changes with aging in the modulation by neuropeptide Y of murine peritoneal macrophage functions. J Neuroimmunol 2001;116:156-167.
25. Puerto M, Guayerbas N, Alvarez P, De la Fuente M: Modulation of neuropeptide Y and norepinephrine on several leucocyte functions in adult, old and very old mice. J Neuroimmunol 2005;165:33-40.
26. Rosenblitt JC, Soler H, Johnson SE, Quadagno DM: Sensation seeking and hormones in men and women: exploring the link. Horm Behav 2001;40:396-402.
27. Kraemer S: The fragile male. BMJ 2000;321:1609-1612.
28. Owens IP: Ecology and evolution: sex differences in mortality rate. Science 2002;297:2008-2009.
29. Mazur A: Biosocial models of deviant behavior among male army veterans. Biol Psychol 1995;41:271-293.
30. Atkinson HC, Waddell BJ: Circadian variation in basal plasma corticosterone and adrenocorticotropin in the rat: sexual dimorphism and changes across the estrous cycle. Endocrinology 1997;138:3842-3848.
31. Stefanski V, Grüner S: Gender difference in basal and stress levels of peripheral blood leukocytes in laboratory rats. Brain Behav Immun 2006;20:369-377.
32. Burgess LH, Handa RJ: Chronic estrogen-induced alterations in adrenocorticotropin and corticosterone secretion, and glucocorticoid receptor-mediated functions in female rats. Endocrinology 1992;131:1261-1269.
33. Zietz B, Hrach S, Schölmerich J, Straub RH: Differential age-related changes of hypothalamus-pituitary-adrenal axis hormones in healthy women and men: role of interleukin 6. Exp Clin Endocrinol Diabetes 2001;109:93-101.
34. Walston J, Fried LP: Frailty and the older man. Med Clin North Am 1999;83:1173-1194.
35. Wilkinson CW, Petrie EC, Murray SR, Colasurdo EA, Raskind MA, Peskind ER: Human glucocorticoid feedback inhibition is reduced in older individuals: evening study. J Clin Endocrinol Metab 2001;86:545-550.
36. Landfield PW, Blalock EM, Chen KC, Porter NM: A new glucocorticoid hypothesis of brain aging: Implications for Alzheimer's disease. Curr Alzheimer Res 2007;4:205-212.
37. Aspinall R: Longevity and the immune response. Biogerontology 2000;1:273-278.
38. Weinstein Y, Ran S, Segal S: Sex-associated differences in the regulation of immune responses controlled by the MHC of the mouse. J Immunol 1984;132:656-661.
39. De la Fuente M, Baeza I, Guayerbas N, Puerto M, Castillo C, Salazar V, Ariznavarreta C, Tresguerres JAF: Changes with aging in several leukocyte functions of male and female rats. Biogerontology 2004;5:389-400.
40. Keller ET, Zhang J, Yao Z, Qi Y: The impact of chronic estrogen deprivation on immunologic parameters in the ovariectomized Rhesus monkey (Macaca mulatta) model of menopause. J Reprod Immunol 2001;50:41-55.
41. Borrás C, Gambini J, Viña J: Mitochondrial oxidant generation is involved in determining why females live longer than males. Front Biosci 2007;12:1008-1013.
42. Guayerbas N, Puerto M, Alvarez P, De la Fuente M: Improvement of the macrophage functions in premature ageing mice by a diet supplemented with thiolic antioxidants. Cell Mol Biol 2004;50:OL677-OL681.
43. De la Fuente M: The immune system as a marker of health and longevity. Antiaging Medicine 2004;1:31-41.
44. De la Fuente M, Hernanz A, Guayerbas N, Puerto M, Alvarez P, Alvarado C: Changes with age in peritoneal macrophage functions. Implication of leukocytes in the oxidative stress of senescence. Cell Mol Biol 2004b;50:OL683-OL690.
45. Matsuoka Y, Picciano M, Malester B, LaFrancois J, Zehr C, Daeschner JM Olschowka JA, Fonseca MI, O'Banion MK, Tenner AJ, Lemere CA, Duff K: Inflammatory responses to amyloidosis in a transgenic mouse model of Alzheimer's disease. Am J Pathol 2001;158:1345-1354.
46. Giovannini MG, Scali C, Prosperi C, Bellucci A, Vannucchi MG, Rosi S, Pepeu G, Casamenti F: β-Amyloid-induced inflammation and cholinergic hypofunction in the rat brain in vivo: involvement of the p38MAPK pathway. Neurobiol Dis 2002;11:257-274.
47. Streit WJ: Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 2002;40:133-139.
48. Grammas P, Ovase R: Cerebrovascular transforming growth factor-β contributes to inflammation in the Alzheimer's disease brain. Am J Pathol 2002;160:1583-1587.
49. Mrak RE, Sheng JGW, Griffin ST: Glial cytokines in Alzheimer's disease: review and pathogenetic implications. Hum Pathol 1995;26:816-823.
50. Hüll M, Strauss S, Berger M, Volk B, Bauer J: Inflammatory mechanisms in Alzheimer's disease. Eur Arch Psychiatry Clin Neurosci 1996;246:124-128.
51. Tarkowski E, Blennow K, Wallin A, Tarkowski A: Intracerebral production of tumour necrosis factor-α, a local neuroprotective agent in Alzheimer's disease and vascular dementia. J Clin Immunol 1999;19:223-230.
52. Richartz E, Stransky E, Batra A, Simon P, Lewczuk P, Buchkremer G, Bartels M, Schott K: Decline of immune responsiveness: A pathogenic factor in Alzheimer's disease? J Psychiatr Res 2005;39:535-543.
53. Remarque EJ, Bollen ELEM, Weverling-Rijnsburger AWE, Laterveer JC, Blauw GJ, Westendorp RGJ: Patients with Alzheimer's disease display a pro-inflammatory phenotype. Exp Gerontol 2001;36:171-176.
54. Rogers J, Strohmeyer R, Kovelowski CJ, Li R: Microglia and inflammatory mechanisms in the clearance of amyloid beta peptide. Glia 2002;40:260-269.
55. Breitner JC, Gau BA, Welsh KA, Plassman BL, McDonald WM, Helms MJ, Anthony JC: Inverse association of anti-inflammatory treatments and Alzheimer's disease: initial results of a co-twin control study. Neurology 1994;44:227-232.
56. Cirrito JR, Holtzmann DM: Amyloid β and Alzheimer's disease therapeutics: the devil may be in the details. J Clin Invest 2003;112:321-323.
57. McKee AC, Carreras I, Hossain L, Ryu H, Klein WL, Oddo S, LaFerla FM, Jenkins BG, Kowall NW, Dedeoglu A: Ibuprofen reduces Aβ, hyperphosphorylated tau and memory deficits in Alzheimer mice. Brain Res 2008;1207:225-236.
58. Papassotiropoulos A, Bagli M, Jessen F, Bayer TA, Maier W, Rao ML, Heun R: A genetic variation of the inflammatory cytokine interleukin-6 delays the initial onset and reduces the risk for sporadic Alzheimer's disease. Ann Neurol 1999;45:666-668.
59. Nicoll JAR, Mrak RE, Graham DJ, Steward J, Wilcock G, MacGowan S, Esiri MM, Murray LS, Dewar D, Love S, Moss T, Griffin WST: Association of interleukin-1 gene polymorphisms with Alzheimer's disease. Ann Neurol 2000;47:365-368.
60. Grimaldi LM, Casadei VM, Ferri C, Veglia F, Licastro F, Annoni G, Biunno I, De Bellis G, Sorbi S, Mariani C, Canal N, Griffin WS, Franceschi M: Association of early-onset Alzheimer's disease with an interleukin-1alpha gene polymorphism. Ann Neurol 2000;47:361-365.
61. Tseng BP, Kitazawa M, LaFerla FM: Amyloid B-peptide: the inside story. Curr Alzheimer Res 2004;1:231-239.
62. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, et al: Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 1999;400:173-177.
63. Lemere CA, Spooner ET, LaFrancois J, et al: Evidence for peripheral clearance of cerebral Aβ protein following chronic, active Aβ immunization in PSAPP mice. Neurobiol Disease 2003;14:10-18.
64. DiCarlo G, Wilcock D, Henderson D, Gordon M, Morgan D: Intrahippocampal LPS injections reduce Aβ load in APP and PS1 transgenic mice. Neurobiol Aging 2001;22:1007-1012.
65. Quinn J, Montine T, Morrow J, Woodward WR, Kulhanek D, Eckenstein F: Inflammation and cerebral amyloidosis are disconnected in an animal model of Alzheimer's disease. J Neuroimmunol 2003;137:32-41.
66. Linton PJ, Dorshkind K: Age-related changes in lymphocyte development and function. Nat Immunol 2004;5:133-139.
67. Pawelec G, Ouyang Q, Colonna-Romano G, Candore G, Lio D, Caruso C: Is human immunosenescence clinically relevant? Looking for 'immunological risk phenotypes'. Trends Immunol 2002;23:330-332.
68. Lloberas J, Celada A: Effect of aging on macrophage function. Exp Gerontol 2002;37:1325-1331.
69. De la Fuente M: Effects of antioxidants on immune system ageing. Eur J Clin Nutr 2002;56:S5-S8.
70. De la Fuente M, Hernanz A, Guayerbas N, Victor VM, Arnalich F: Vitamin E ingestion improves several immune functions in elderly men and women. Free Radic Res 2008;42:272-280.
71. Medina S, Del Rio M, Victor VM, Hernanz A, De la Fuente, M: Changes with ageing in the modulation of murine lymphocyte chemotaxis by CCK-8s, GRP and NPY. Mech Ageing Dev 1998;102:249-261.
72. Ferrández MD, Correa R, Del Rio M, De la Fuente M: Effects in vitro of several antioxidants on the natural killer function of aging mice. Exp Gerontol 1999;34:675-685.
73. Wayne SL, Rhyne RL, Garry PJ, Goodwin JS: Cell-mediated immunity as a predictor of morbility and mortality in subjects over 60. J Gerontol 1990;45:M45-M48.
74. Guayerbas N, Puerto M, Victor VM, Miquel J, De la Fuente M: Leukocyte function and life span in a murine model of premature immunosenescence. Exp Gerontol 2002;37:249-256.
75. Guayerbas N, De La Fuente M: An impairment of phagocytic function is linked to a shorter life span in two strains of prematurely aging mice. Dev Comp Immunol 2003;27:339-350.
76. Bonotis K, Krikki E, Holeva V, Aggouridaki C, Costa V, Baloyannis S: Systemic immune aberrations in Alzheimer's disease patients. J Neuroimmunol 2008;193:183-187.
77. Liu H, Harrell LE, Shenvi S, Hagen T, Liu LM: Gender differences in glutathione metabolism in Alzheimer's disease. J Neurosci Res 2005;79:861-867.
78. Alvarado C, Alvarez P, Puerto M, Gausserés N, Jimenez L, De la Fuente M: Dietary supplementation with antioxidants improves functions and decreases oxidative stress of leukocytes from prematurely aging mice. Nutrition 2006;22:767-777.
79. Viveros MP, Arranz L, Hernanz A, Miquel J, De la Fuente M: A model of premature ageing in mice based on altered stress-related behavioural response and immunosenescence. Neuroimmunomodulation 2007;14:157-162.
80. Hartmamm A, Veldhuis JD, Deuschle M, Standhardt H, Heurser I: Twenty-four hour cortisol release profiles in patients with Alzheimer's and Parkinson's disease compared to normal controls: ultradian secretory pulsatility and diurnal variation. Neurobiol Aging 1997;18:285-289.
81. Woiciechowsky C, Schoning B, Lanksch WR, Volk H-D, Docke W-D: Mechanisms of brain-mediated systemic anti-inflammatory syndrome causing immunodepression. J Mol Med 1999;77:769-780.
82. Sapolsky RM, Krey LC, McEwen BS: The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr Rev 1986;75:284-301.
83. Selye H: The stress of life: revised edition. New York, McGraw Hill Book Co., 1975.
84. Maeda K, Tanimoto K, Terada T, Shintani T, Kakigi T: Elevated urinary free cortisol in patients with dementia. Neurobiol Aging 1991;12:161-163.
85. Hatzinger M, Z'Brun A, Hemmeter U, Seifritz E, Baumann F, Holsboer-Tachsler E, Heuser IJ: Hypotaholamic-pituitary-adrenal system function inpatients with Alzheimer's disease. Neurobiol Aging 1995;16:205-209.
86. Touma C, Ambree O, Gortz N, Keyvani K, Lewejohann L, Palme R, Paulus W, Schwarze-Eicker K, Sachser N: Age- and sex-dependent development of adrenocortical hyperactivity in a transgenic mouse model of Alzheimer's disease. Neurobiol Aging 2004;25:893-904.
87. Pedersen WA, Culmsee C, Ziegler D, Herman JP, Mattson MP: Aberrant stress response associated with severe hypoglycemia in a transgenic mouse model of Alzheimer's disease. J Mol Neurosci 1999;13:159-165.
88. Gimenez-Llort L, Blázquez G, Canete T, Rosa R, Vivo M, Oddo S, Navarro X, Lamerla FM, Johansson B, Tobena A, Fernandez-Teruel A: Modeling neuropsychiatric symptoms of Alzheimer's dementia in 3 x Tg-AD mice; in Iqbal K, Winblad B, Avila J (eds): Alzheimer's Disease:New Advances. Bologna, Medimond S.r.l., 2006, pp 513-516.
89. Rasmuson S, Näsman B, Carlström K, Olsson T: Increased levels of adrenocortical and gonadal hormones in mild to moderate Alzheimer's disease. Dement Geriatr Cogn Disord 2002;13:74-79.
90. Clinton LK, Billings LM, Green KN, Caccamo A, Ngo J, Oddo S, McGaugh JL, LaFerla FM: Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice. Neurobiol Dis 2007;28:76-82.