Towards developing a rhesus monkey model of early Alzheimer's disease focusing on women's health.
Alzheimer's disease
AβOs
NHPs
female
microglia
synapses
Journal
American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
revised:
11
05
2021
received:
10
03
2021
accepted:
16
05
2021
pubmed:
1
6
2021
medline:
25
11
2021
entrez:
31
5
2021
Statut:
ppublish
Résumé
Alzheimer's disease (AD) is the most common cause of elderly dementia, affecting nearly 50 million people worldwide, with two-thirds of the cases in the USA in women. Despite considerable investment, this prevalence is expected to increase further in the coming decades, based on the projected demographics of the population. Currently, most of the preclinical AD studies rely on transgenic mice carrying mutations associated with the early onset familiar form of AD, although the vast majority of cases are sporadic. A prevailing current hypothesis is that the cascade of events leading to AD starts with the accumulation of small soluble oligomers of the Aβ peptide (AβOs) that target and disrupt synapses. Taking advantage of the high translational power of rhesus monkeys due to their physiological and genetic similarities to humans, we recently developed a female rhesus monkey model of early AD pathogenesis based on exogenous administration AβOs. Here we review and discuss how soluble oligomers of Aβ can target vulnerable spines in the neocortex and hippocampus of female middle-aged monkeys and induce neuroinflammatory responses, similar to what is known to occur in the human brain. Developing a rhesus monkey model of early AD focusing on women's health is critical for the understanding of how hormonal changes during menopause transition affect brain health and ultimately may contribute to AD neurodegeneration.
Substances chimiques
Amyloid beta-Peptides
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23289Subventions
Organisme : NIH HHS
ID : PO1-AG016765
Pays : United States
Organisme : NIH HHS
ID : R37-AG06647
Pays : United States
Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
2020 Alzheimer's disease facts and figures. (2020). 2020 Alzheimer's disease facts and figures. Alzheimer's & Dementia, 16(3), 391-460.
Arnsten, A. F. T., Datta, D., Leslie, S., Yang, S. T., Wang, M., & Nairn, A. C. (2019). Alzheimer's-like pathology in aging rhesus macaques: Unique opportunity to study the etiology and treatment of Alzheimer's disease. Proceedings of the National Academy of Sciences of the United States of America, 116, 26230-26238.
Baldereschi, M., Di Carlo, A., Lepore, V., Bracco, L., Maggi, S., Grigoletto, F., Scarlato, G., & Amaducci, L. (1998). Estrogen-replacement therapy and Alzheimer's disease in the Italian longitudinal study on aging. Neurology, 50, 996-1002.
Beckman, D., Ott, S., Donis-Cox, K., Janssen, W. G., Bliss-Moreau, E., Rudebeck, P. H., Baxter, M. G., & Morrison, J. H. (2019). Oligomeric Aβ in the monkey brain impacts synaptic integrity and induces accelerated cortical aging. Proceedings of the National Academy of Sciences of the United States of America. https://doi.org/10.1073/pnas.1902301116
Crimins, J. L., Hara, Y., & Morrison, J. H. (2020). Estrogenic regulation of synaptic health and cognition in aging Rhesus monkeys, Estrogens and Memory (pp. 303-334.Oxford University Press. https://doi.org/10.1093/oso/9780190645908.003.0018
Dumitriu, D., Hao, J., Hara, Y., Kaufmann, J., Janssen, W. G. M., Lou, W., Rapp, P. R., & Morrison, J. H. (2010). Selective Changes in Thin Spine Density and Morphology in Monkey Prefrontal Cortex Correlate with Aging-Related Cognitive Impairment. Journal of Neuroscience, 30(22), 7507-7515.
Dumitriu, D., Rapp, P. R., McEwen, B. S., & Morrison, J. H. (2010). Estrogen and the aging brain: An elixir for the weary cortical network. Annals of the New York Academy of Sciences, 1204, 104-112.
Edler, M. K., Sherwood, C. C., Meindl, R. S., Hopkins, W. D., Ely, J. J., Erwin, J. M., Mufson, E. J., Hof, P. R., & Raghanti, M. A. (2017). Aged chimpanzees exhibit pathologic hallmarks of Alzheimer's disease. Neurobiology of Aging, 59, 107-120.
Van Essen, D. C., Donahue, C. J., Coalson, T. S., Kennedy, H., Hayashi, T., & Glasser, M. F. (2019). Cerebral cortical folding, parcellation, and connectivity in humans, nonhuman primates, and mice. Proceedings of the National Academy of Sciences of the United States of America. https://doi.org/10.1073/pnas.1902299116
Van Essen, D. C., Donahue, C. J., & Glasser, M. F. (2018). Development and evolution of cerebral and cerebellar cortex. Brain, Behavior and Evolution, 91, 158-169.
Forny-Germano, L., Lyra e Silva, N. M., Batista, A. F., Brito-Moreira, J., Gralle, M., Boehnke, S. E., Coe, B. C., Lablans, A., Marques, S. A., Martinez, A. M., Klein, W. L., Houzel, J. C., Ferreira, S. T., Munoz, D. P., & De Felice, F. G. (2014). Alzheimer's disease-like pathology induced by amyloid-β oligomers in nonhuman primates. Journal of Neuroscience, 34(41), 13629-13643.
Hara, Y., Rapp, P. R., & Morrison, J. H. (2012). Neuronal and morphological bases of cognitive decline in aged rhesus monkeys. In Age, 34(Issue 5), 1051-1073.
Hara, Y., Waters, E. M., McEwen, B. S., & Morrison, J. H. (2015). Estrogen effects on cognitive and synaptic health over the lifecourse. Physiological Reviews, 95, 785-807.
Heikkinen, T., Puoliväli, J., & Tanila, H. (2004). Effects of long-term ovariectomy and estrogen treatment on maze learning in aged mice. Experimental Gerontology, 39(9), 1277-1283.
Hong, S., Beja-Glasser, V. F., Nfonoyim, B. M., Frouin, A., Li, S., Ramakrishnan, S., Merry, K. M., Shi, Q., Rosenthal, A., Barres, B. A., Lemere, C. A., Selkoe, D. J., & Stevens, B. (2016). Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science, 352(6286), 712-716.
Johann, S., & Beyer, C. (2013). Neuroprotection by gonadal steroid hormones in acute brain damage requires cooperation with astroglia and microglia. In Journal of Steroid Biochemistry and Molecular Biology, 137, 71-81.
Kantarci, K., Lowe, V. J., Lesnick, T. G., Tosakulwong, N., Bailey, K. R., Fields, J. A., Shuster, L. T., Zuk, S. M., Senjem, M. L., Mielke, M. M., Gleason, C., Jack, C. R., Rocca, W. A., & Miller, V. M. (2016). Early Postmenopausal Transdermal 17β-Estradiol Therapy and Amyloid-β Deposition. Journal of Alzheimer's Disease, 53(2), 547-556.
Latimer, C. S., Shively, C. A., Keene, C. D., Jorgensen, M. J., Andrews, R. N., Register, T. C., Montine, T. J., Wilson, A. M., Neth, B. J., Mintz, A., Maldjian, J. A., Whitlow, C. T., Kaplan, J. R., & Craft, S. (2019). A nonhuman primate model of early Alzheimer's disease pathologic change: Implications for disease pathogenesis. Alzheimer's and Dementia, 15, 93-105.
Li, K., Li, J., Zheng, J., & Qin, S. (2019). Reactive astrocytes in neurodegenerative diseases. Aging and Disease. https://doi.org/10.14336/ad.2018.0720
Liddelow, S. A., & Barres, B. A. (2017). Reactive astrocytes: Production, function, and therapeutic potential. In Immunity, 46, 957-967.
Mackenzie, I. R. A., Hao, C., & Munoz, D. G. (1995). Role of microglia in senile plaque formation. Neurobiology of Aging, 16(5), 797-804.
Mattson, M. P., & Magnus, T. (2006). Ageing and neuronal vulnerability. Nature Reviews Neuroscience, 7(4), 278-294. https://doi.org/10.1038/nrn1886
McDowell, I., Hill, G., Lindsay, J., Helliwell, B., Costa, L., Beattie, B. L., Tuokko, H., Hertzman, C., Gutman, G., Parhad, I., Parboosingh, J., Bland, R., Newman, S., Dobbs, A., Hazlett, C., Rule, B., D'Arcy, C., Segall, A., & Chappell, N. (1994). Canadian Study of Health and Aging: Study methods and prevalence of dementia. Canadian Medical Association Journal/Journal de l'Association Medicale Canadienne, 150, 899-913.
Mishra, A., & Brinton, R. D. (2018). Inflammation: Bridging age, menopause and APOEε4 genotype to Alzheimer's Disease. Frontiers in Aging Neuroscience, 10, 312.
Morrison, J. H., & Baxter, M. G. (2012). The ageing cortical synapse: Hallmarks and implications for cognitive decline. In Nature Reviews Neuroscience, 13(Issue 4), 240-250.
Morrison, J. H., Brinton, R. D., Schmidt, P. J., & Gore, A. C. (2006). Estrogen, menopause, and the aging brain: How basic neuroscience can inform hormone therapy in women. Journal of Neuroscience, 26, 10332-10348.
Nebel, R. A., Aggarwal, N. T., Barnes, L. L., Gallagher, A., Goldstein, J. M., Kantarci, K., Mallampalli, M. P., Mormino, E. C., Scott, L., Yu, W. H., Maki, P. M., & Mielke, M. M. (2018). Understanding the impact of sex and gender in Alzheimer's disease: A call to action. Alzheimer's and Dementia, 14, 1171-1183.
Paspalas, C. D., Carlyle, B. C., Leslie, S., Preuss, T. M., Crimins, J. L., Huttner, A. J., van Dyck, C. H., Rosene, D. L., Nairn, A. C., & Arnsten, A. F. T. (2018). The aged rhesus macaque manifests Braak stage III/IV Alzheimer's-like pathology. Alzheimer's and Dementia, 680-691, 14, 680-691.
Rocca, W. A., Mielke, M. M., Vemuri, P., & Miller, V. M. (2014). Sex and gender differences in the causes of dementia: A narrative review. In Maturitas, 79, 196-201.
Selkoe, D. J. (2002). Alzheimer's disease is a synaptic failure. Science (New York, N.Y.), 298(5594), 789-791.
Selkoe, D. J., & Hardy, J. (2016). The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Molecular Medicine, 8, 595-608.
Sheng, M., Sabatini, B. L., & Südhof, T. C. (2012). Synapses and Alzheimer's disease. Cold Spring Harbor Perspectives in Biology, 4, a005777.
Stephan, A. H., Madison, D. V., Mateos, J. M., Fraser, D. A., Lovelett, E. A., Coutellier, L., Kim, L., Tsai, H.-H., Huang, E. J., Rowitch, D. H., Berns, D. S., Tenner, A. J., Shamloo, M., & Barres, B. A. (2013). A Dramatic Increase of C1q Protein in the CNS during Normal Aging. Journal of Neuroscience, 33(33), 13460-13474.
Tanzi, R. E. (2012). The genetics of Alzheimer Disease. Cold Spring Harbor Perspectives in Medicine, 2(10), a006296.
Verkhratsky, A., Olabarria, M., Noristani, H. N., Yeh, C. Y., & Rodriguez, J. J. (2010). Astrocytes in Alzheimer's Disease. Neurotherapeutics, 7, 399-412.
Villa, A., Vegeto, E., Poletti, A., & Maggi, A. (2016). Estrogens, neuroinflammation, and neurodegeneration. In Endocrine Reviews, 37, 372-402.
Viola, K. L., & Klein, W. L. (2015). Amyloid β oligomers in Alzheimer's disease pathogenesis, treatment, and diagnosis. In. Acta Neuropathologica, 129(Issue 2), 183-206.
Walker, L. C., & Jucker, M. (2017). The exceptional vulnerability of humans to Alzheimer's Disease. In. Trends in Molecular Medicine, 23, 534-545.
Wilcock, D. M. (2012). A changing perspective on the role of neuroinflammation in Alzheimer's disease. In International Journal of Alzheimer's Disease, 2012, 1-7.
Wyss-Coray, T., & Rogers, J. (2012). Inflammation in Alzheimer's disease-A brief review of the basic science and clinical literature. Cold Spring Harbor Perspectives in Medicine, 2, 006346.
Yue, X., Lu, M., Lancaster, T., Cao, P., Honda, S. I., Staufenbiel, M., Harada, N., Zhong, Z., Shen, Y., & Li, R. (2005). Brain estrogen deficiency accelerates Aβ plaque formation in an Alzheimer's disease animal model. Proceedings of the National Academy of Sciences of the United States of America, 102, 19198-19203.
Zhao, L., Mao, Z., Woody, S. K., & Brinton, R. D. (2016). Sex differences in metabolic aging of the brain: Insights into female susceptibility to Alzheimer's disease. Neurobiology of Aging, 42, 69-79.