Alzheimer’s Disease: A Search for the Best Experimental Models for the Decoding of the Cellular and Molecular Mechanisms of the Development of the Diease

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Abstract

Alzheimer’s disease is the most common type of dementia associated with cognitive decline, such as memory and visuospatial skills. Insufficiently effective treatments have prompted the creation of experimental animal models capable of reproducing the pathology of Alzheimer’s disease, especially at the presymptomatic stage, in order to develop and study preventive and therapeutic strategies. To date, none of the developed animal models fully reflects the entire spectrum of neuropathological and cognitive impairments observed in the development of Alzheimer’s disease in humans. However, each model created allows, to one degree or another, to study various aspects of the pathogenesis of the disease, providing an important understanding of the key pathological changes that may occur during its development. In this review, we present a summary of the neuropathological features of Alzheimer’s disease and their relationship to cognitive impairment in the animal models currently in use. We also present in a comparative aspect the features of the development of Alzheimer’s type neurodegeneration using the example of 2 models – genetic and injection, which will make it possible to determine optimal approach when choosing a model for implementing research tasks.

About the authors

Y. V. Gorina

Laboratory of Molecular Neurodegeneration, the St. Petersburg Polytechnic University
of Peter the Great; Research Institute of Molecular Medicine and Pathobiochemistry,
Professor Voino-Yasenetsky Krasnoyarsk State Medical University

Author for correspondence.
Email: yana_20@bk.ru
Russia, St. Petersburg; Russia, Krasnoyarsk

O. L. Vlasova

Laboratory of Molecular Neurodegeneration, the St. Petersburg Polytechnic University
of Peter the Great

Email: yana_20@bk.ru
Russia, St. Petersburg

A. V. Bolshakova

Laboratory of Molecular Neurodegeneration, the St. Petersburg Polytechnic University
of Peter the Great

Email: yana_20@bk.ru
Russia, St. Petersburg

A. B. Salmina

Laboratory of Molecular Neurodegeneration, the St. Petersburg Polytechnic University
of Peter the Great; Research Institute of Molecular Medicine and Pathobiochemistry,
Professor Voino-Yasenetsky Krasnoyarsk State Medical University; Laboratory of Neurobiology and Tissue Engineering, Brain Institute,
Research Center of Neurology

Email: yana_20@bk.ru
Russia, St. Petersburg; Russia, Krasnoyarsk; Russia, Moscow

References

  1. Sanchez-Varo R, Mejias-Ortega M, Fernandez-Valenzuela JJ, Nuñez-Diaz C, Caceres-Palomo L, Vegas-Gomez L, Sanchez-Mejias E, Trujillo-Estrada L, Garcia-Leon JA, Moreno-Gonzalez I, Vizuete M, Vitorica J, Baglietto-Vargas D, Gutierrez A (2022) Transgenic Mouse Models of Alzheimer’s Disease: An Integrative Analysis. Int J Mol Sci 23: 5404. https://doi.org/10.3390/ijms23105404.:45-54
  2. Lithner CU, Hedberg MM, Nordberg A (2011) Transgenic mice as a model for Alzheimer’s disease. Curr Alzheimer Res 8: 818–831. https://doi.org/10.2174/156720511798192736
  3. Иптышев АМ, Горина ЯВ, Лопатина ОЛ, Комлева ЮК, Салмина АБ (2016) Экспериментальные модели болезни Альцгеймера: преимущества и недостатки. Сибирск мед обозр 4: 5–21. [Iptyshev AM, Gorina YAV, Lopatina OL, Komleva YUK, Salmina AB (2016) Experimental models of Alzheimer’s disease: advantages and disadvantages. Siber Med Rev 4: 5–21. (In Russ)].
  4. Cruchaga C, Del-Aguila JL, Saef B, Black K, Fernandez MV, Budde J, Ibanez L, Deming Y, Kapoor M, Tosto G, Mayeux RP, Holtzman DM, Fagan AM, Morris JC, Bateman RJ, Goate AM, Dominantly Inherited Alzheimer Network (DIAN), Disease Neuroimaging Initiative (ADNI), NIA-LOAD family study, Harari O (2018) Polygenic risk score of sporadic late-onset Alzheimer’s disease reveals a shared architecture with the familial and early-onset forms. Alzheimer’s & Dementia 14: 205–214. https://doi.org/10.1016/j.jalz.2017.08.013
  5. Giau VV, Bagyinszky E, Youn YC, An SSA, Kim SY (2019) APP, PSEN1, and PSEN2 Mutations in Asian Patients with Early-Onset Alzheimer Disease. Int J Mol Sci 20: 4757. https://doi.org/10.3390/ijms20194757
  6. Geijselaers SLC, Aalten P, Ramakers IHGB, De Deyn PP, Heijboer AC, Koek HL, OldeRikkert MGM, Papma JM, Reesink FE, Smits LL, Stehouwer CDA, Teunissen CE, Verhey FRJ, van der Flier WM, Biessels GJ, Parelsnoer Institute Neurodegenerative Diseases study group (2017) Association of Cerebrospinal Fluid (CSF) Insulin with Cognitive Performance and CSF Biomarkers of Alzheimer’s Disease. J Alzheimer’s Disease 61: 309–320. https://doi.org/10.3233/JAD-170522
  7. Zhang F, Wei J, Li X, Ma C, Gao Y (2018) Early Candidate Urine Biomarkers for Detecting Alzheimer’s Disease Before Amyloid-β Plaque Deposition in an APP (swe)/PSEN1dE9 Transgenic Mouse Model. J Alzheimer’s Disease 66: 613–637. https://doi.org/10.3233/JAD-180412
  8. Forrest SL, Kril JJ, Stevens CH, Kwok JB, Hallupp M, Kim WS, Huang Y, McGinley CV, Werka H, Kiernan MC, Götz J, Spillantini MG, Hodges JR, Ittner LM, Halliday GM (2018) Retiring the term FTDP-17 as MAPT mutations are genetic forms of sporadic frontotemporal tauopathies. Brain 141: 521–534. https://doi.org/10.1093/brain/awx328
  9. Adams SJ, Crook RJP, Deture M, Randle SJ, Innes AE, Yu XZ, Lin WL, Dugger BN, McBride M, Hutton M, Dickson DW, McGowan E (2009) Overexpression of Wild-Type Murine Tau Results in Progressive Tauopathy and Neurodegeneration. Am J Pathol 175: 1598–1609. https://doi.org/10.2353/ajpath.2009.090462
  10. Johnson ECB, Ho K, Yu GQ, Das M, Sanchez PE, Djukic B, Lopez I, Yu X, Gill M, Zhang W, Paz JT, Palop JJ, Mucke L (2020) Behavioral and neural network abnormalities in human APP transgenic mice resemble those of App knock-in mice and are modulated by familial Alzheimer’s disease mutations but not by inhibition of BACE1. Mol Neurodegenerat 15: 53. https://doi.org/10.1186/s13024-020-00393-5
  11. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative Memory Deficits, A Elevation, and Amyloid Plaques in Transgenic Mice. Science 274: 99–103. https://doi.org/10.1126/science.274.5284.99
  12. Oulès B, Del Prete D, Greco B, Zhang X, Lauritzen I, Sevalle J, Moreno S, Paterlini-Bréchot P, Trebak M, Checler F, Benfenati F, Chami M (2012) Ryanodine Receptor Blockade Reduces Amyloid- Load and Memory Impairments in Tg2576 Mouse Model of Alzheimer Disease. J Neurosci 32: 11820–11834. https://doi.org/10.1523/JNEUROSCI.0875-12.2012
  13. Westerman MA, Cooper-Blacketer D, Mariash A, Kotilinek L, Kawarabayashi T, Younkin LH, Carlson GA, Younkin SG, Ashe KH (2002) The Relationship between Aβ and Memory in the Tg2576 Mouse Model of Alzheimer’s Disease. J Neurosci 22: 1858–1867. https://doi.org/10.1523/JNEUROSCI.22-05-01858.2002
  14. Lefterov I, Fitz NF, Cronican A, Lefterov P, Staufenbiel M, Koldamova R (2009) Memory deficits in APP23/Abca1+/- mice correlate with the level of Aβ oligomers. ASN Neuro 1: e00006. https://doi.org/10.1042/AN20090015
  15. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Bürki K, Frey P, Paganetti PA, Waridel C, Calhoun ME, Jucker M, Probst A, Staufenbiel M, Sommer B (1997) Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci USA 94: 13287–13292. https://doi.org/10.1073/pnas.94.24.13287
  16. Van Dam D, D’Hooge R, Staufenbiel M, Van Ginneken C, Van Meir F, De Deyn PP (2003) Age-dependent cognitive decline in the APP23 model precedes amyloid deposition: Behavioral testing of the APP23 model. Eur J Neurosci 17: 388–396. https://doi.org/10.1046/j.1460-9568.2003.02444.x
  17. Chen G, Chen KS, Knox J, Inglis J, Bernard A, Martin SJ, Justice A, McConlogue L, Games D, Freedman SB, Morris RG (2000) A learning deficit related to age and β-amyloid plaques in a mouse model of Alzheimer’s disease. Nature 408: 975–979. https://doi.org/10.1038/35050103
  18. Games D, Adams D, Alessandrini R, Barbour R, Borthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, Guido T, Hagopian S, Johnson-Wood K, Khan K, Lee M, Leibowitz P, Lieberburg I, Little S, Masliah E, McConlogue L, Montoya-Zavala M, Mucke L, Paganini L, Penniman E, Power M, Schenk D, Seubert P, Snyder B, Soriano F, Tan H, Vitale J, Wadsworth S, Wolozin B, Zhao J (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373: 523–527. https://doi.org/10.1038/373523a0
  19. Ameen-Ali KE, Wharton SB, Simpson JE, Heath PR, Sharp P, Berwick J (2017) Review: Neuropathology and behavioural features of transgenic murine models of Alzheimer’s disease. Neuropathol Appl Neurobiol 43: 553–570. https://doi.org/10.1111/nan.12440
  20. Escribano L, Simón AM, Pérez-Mediavilla A, Salazar-Colocho P, Del Río J, Frechilla D (2009) Rosiglitazone reverses memory decline and hippocampal glucocorticoid receptor down-regulation in an Alzheimer’s disease mouse model. Biochem Biophys Res Commun 379: 406–410. https://doi.org/10.1016/j.bbrc.2008.12.071
  21. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L (2000) High-Level Neuronal Expression of Aβ 1-42 in Wild-Type Human Amyloid Protein Precursor Transgenic Mice: Synaptotoxicity without Plaque Formation. J Neurosci 20: 4050–4058. https://doi.org/10.1523/JNEUROSCI.20-11-04050.2000
  22. Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J, Masliah E, Mucke L (2003) Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer’s disease-related cognitive deficits. Proc Natl Acad Sci U S A 100: 9572–9577. https://doi.org/10.1073/pnas.1133381100
  23. Ambrée O, Richter H, Sachser N, Lewejohann L, Dere E, de Souza Silva MA, Herring A, Keyvani K, Paulus W, Schäbitz WR (2009) Levodopa ameliorates learning and memory deficits in a murine model of Alzheimer’s disease. Neurobiol Aging 30: 1192–1204. https://doi.org/10.1016/j.neurobiolaging.2007.11.010
  24. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, Strome R, Zuker N, Loukides J, French J, Turner S, Lozza G, Grilli M, Kunicki S, Morissette C, Paquette J, Gervais F, Bergeron C, Fraser PE, Carlson GA, George-Hyslop PS, Westaway D (2001) Early-onset Amyloid Deposition and Cognitive Deficits in Transgenic Mice Expressing a Double Mutant Form of Amyloid Precursor Protein 695. J Biol Chem 276: 21562–21570. https://doi.org/10.1074/jbc.M100710200
  25. Kobayashi DT, Chen KS (2005) Behavioral phenotypes of amyloid-based genetically modified mouse models of Alzheimer’s disease. Genes, Brain and Behav 4: 173–196. https://doi.org/10.1111/j.1601-183X.2005.00124
  26. Kosel F, Torres Munoz P, Yang JR, Wong AA, Franklin TB (2019) Age-related changes in social behaviours in the 5xFAD mouse model of Alzheimer’s disease. Behav Brain Res 362: 160–172. https://doi.org/10.1016/j.bbr.2019.01.029
  27. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R (2006) Intraneuronal beta-Amyloid Aggregates, Neurodegeneration, and Neuron Loss in Transgenic Mice with Five Familial Alzheimer’s Disease Mutations: Potential Factors in Amyloid Plaque Formation. J Neurosci 26: 10129–10140. https://doi.org/10.1523/JNEUROSCI.1202-06.2006
  28. Ohno M, Chang L, Tseng W, Oakley H, Citron M, Klein WL, Vassar R, Disterhoft JF (2006) Temporal memory deficits in Alzheimer’s mouse models: rescue by genetic deletion of BACE1. Eur J Neurosci 23: 251–260. https://doi.org/10.1111/j.1460-9568.2005.04551.x
  29. Saito T, Suemoto T, Brouwers N, Sleegers K, Funamoto S, Mihira N, Matsuba Y, Yamada K, Nilsson P, Takano J, Nishimura M, Iwata N, Van Broeckhoven C, Ihara Y, Saido TC (2011) Potent amyloidogenicity and pathogenicity of Aβ43. Nature Neurosci 14: 1023–1032. https://doi.org/10.1038/nn.2858
  30. Lee CYD, Daggett A, Gu X, Jiang LL, Langfelder P, Li X, Wang N, Zhao Y, Park CS, Cooper Y, Ferando I, Mody I, Coppola G, Xu H, Yang XW (2018) Elevated TREM2 Gene Dosage Reprograms Microglia Responsivity and Ameliorates Pathological Phenotypes in Alzheimer’s Disease Models. Neuron 97: 1032–1048.e5. https://doi.org/10.1016/j.neuron.2018.02.002
  31. Belfiore R, Rodin A, Ferreira E, Velazquez R, Branca C, Caccamo A, Oddo S (2019) Temporal and regional progression of Alzheimer’s disease-like pathology in 3xTg-AD mice. Aging Cell 18: e12873. https://doi.org/10.1111/acel.12873
  32. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM (2005) Affiliations expand Intraneuronal Aβ Causes the Onset of Early Alzheimer’s Disease-Related Cognitive Deficits in Transgenic Mice. Neuron 45: 675–688. https://doi.org/10.1016/j.neuron.2005.01.040
  33. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-Transgenic Model of Alzheimer’s Disease with Plaques and Tangles. Neuron 39: 409–421. https://doi.org/10.1016/s0896-6273(03)00434-3
  34. Volloch V, Olsen B, Rits S (2019) Alzheimer’s Disease is Driven by Intraneuronally Retained Beta-Amyloid Produced in the AD-Specific, βAPP-Independent Pathway: Current Perspective and Experimental Models for Tomorrow. Ann Integrat Mol Med 2: 90–114. https://doi.org/10.33597/aimm.02-1007
  35. Creighton SD, Mendell AL, Palmer D, Kalisch BE, MacLusky NJ, Prado VF, Prado MAM, Winters BD (2019) Dissociable cognitive impairments in two strains of transgenic Alzheimer’s disease mice revealed by a battery of object-based tests. Sci Rep 9: 57. https://doi.org/10.1038/s41598-018-37312-0
  36. Kitazawa M, Medeiros R, LaFerla FM (2012) Transgenic Mouse Models of Alzheimer Disease: Developing a Better Model as a Tool for Therapeutic Interventions. Current Pharm Design 18: 1131–1147. https://doi.org/10.2174/138161212799315786
  37. Poon CH, Wang Y, Fung ML, Zhang C, Lim LW (2020) Rodent Models of Amyloid-Beta Feature of Alzheimer’s Disease: Development and Potential Treatment Implications. Aging and Disease 11: 1235–1259. https://doi.org/10.14336/AD.2019.1026
  38. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, Strome R, Zuker N, Loukides J, French J, Turner S, Lozza G, Grilli M, Kunicki S, Morissette C, Paquette J, Gervais F, Bergeron C, Fraser PE, Carlson GA, George-Hyslop PS, Westaway D (2001) Early-onset Amyloid Deposition and Cognitive Deficits in Transgenic Mice Expressing a Double Mutant Form of Amyloid Precursor Protein 695. J Biol Chem 276: 21562–21570. https://doi.org/10.1074/jbc.M100710200
  39. Bagyinszky E, Park SA, Kim HJ, Choi SH, An SS, Kim SY (2016) PSEN1 L226F mutation in a patient with early-onset Alzheimer’s disease in Korea. Clin Intervent Aging 11: 1433–1440. https://doi.org/10.2147/CIA.S111821
  40. Otvos LJ, Szendrei GI, Lee VM, Mantsch HH (1993) Human and rodent Alzheimer beta-amyloid peptides acquire distinct conformations in membrane-mimicking solvents. Eur J Biochem 211: 249–257. https://doi.org/10.1111/j.1432-1033.1993.tb19893.x
  41. Jaffar S, Counts SE, Ma SY, Dadko E, Gordon MN, Morgan D, Mufson EJ (2001) Neuropathology of Mice Carrying Mutant APPswe and/or PS1M146L Transgenes: Alterations in the p75NTR Cholinergic Basal Forebrain Septohippocampal Pathway. Exp Neurol 170: 227–243. https://doi.org/10.1006/exnr.2001.7710
  42. Li XY, Men WW, Zhu H, Lei JF, Zuo FX, Wang ZJ, Zhu ZH, Bao XJ, Wang RZ (2016) Age- and Brain Region-Specific Changes of Glucose Metabolic Disorder, Learning, and Memory Dysfunction in Early Alzheimer’s Disease Assessed in APP/PS1 Transgenic Mice Using 18F-FDG-PET. Int J Mol Sci 17: 1707. https://doi.org/10.3390/ijms17101707
  43. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O’Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nature Med 4: 97–100. https://doi.org/10.1038/nm0198-097
  44. Eimer WA., Vassar R (2013) Neuron loss in the 5XFAD mouse model of Alzheimer’s disease correlates with intraneuronal Aβ42 accumulation and Caspase-3 activation. Mol Neurodegen 8: 2. https://doi.org/10.1186/1750-1326-8-2
  45. Xiao NA, Zhang J, Zhou M, Wei Z, Wu XL, Dai XM, Zhu YG, Chen XC (2015) Reduction of Glucose Metabolism in Olfactory Bulb is an Earlier Alzheimer’s Disease-related Biomarker in 5XFAD Mice. Chin Med J 128: 2220–2227. https://doi.org/10.4103/0366-6999.162507
  46. Wirths O, Zampar S (2020) Neuron Loss in Alzheimer’s Disease: Translation in Transgenic Mouse Models. Int J Mol Sci 21: 8144. https://doi.org/10.3390/ijms21218144
  47. Héraud C, Goufak D, Ando K, Leroy K, Suain V, Yilmaz Z, De Decker R, Authelet M, Laporte V, Octave JN, Brion JP (2014) Increased misfolding and truncation of tau in APP/PS1/tau transgenic mice compared to mutant tau mice. Neurobiol Disease 62: 100–112. https://doi.org/10.1016/j.nbd.2013.09.010
  48. DeBay DR, Reid GA, Macdonald IR, Mawko G, Burrell S, Martin E, Bowen CV, Darvesh S (2017) Butyrylcholinesterase-knockout reduces fibrillar β-amyloid and conserves 18FDG retention in 5XFAD mouse model of Alzheimer’s disease. Brain Res 1671: 102–110. https://doi.org/10.1016/j.brainres.2017.07.009
  49. Hüttenrauch M, Baches S, Gerth J, Bayer TA, Weggen S, Wirths O (2015) Neprilysin Deficiency Alters the Neuropathological and Behavioral Phenotype in the 5XFAD Mouse Model of Alzheimer’s Disease. J Alzheimer’s Disease 44: 1291–1302. https://doi.org/10.3233/JAD-142463
  50. Jafari Z, Okuma M, Karem H, Mehla J, Kolb BE, Mohajerani MH (2019) Prenatal noise stress aggravates cognitive decline and the onset and progression of beta amyloid pathology in a mouse model of Alzheimer’s disease. Neurobiol Aging 77: 66–86. https://doi.org/10.1016/j.neurobiolaging.2019.01.019
  51. Kelley BJ, Petersen RC (2007) Alzheimer’s Disease and Mild Cognitive Impairment. Neurol Clin 25: 577–609. https://doi.org/10.1016/j.ncl.2007.03.008
  52. Schliebs R, Arendt T (2011). The cholinergic system in aging and neuronal degeneration. Behav Brain Res 221: 555–563. https://doi.org/10.1016/j.bbr.2010.11.058
  53. Selkoe DJ, Hardy J (2016) The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol Med 8: 595–608. https://doi.org/10.15252/emmm.201606210
  54. Chen Z, Zhong C (2013) Decoding Alzheimer’s disease from perturbed cerebral glucose metabolism: Implications for diagnostic and therapeutic strategies. Progr Neurobiol 108: 21–43. https://doi.org/10.1016/j.pneurobio.2013.06.004
  55. Bezprozvanny I (2022) Alzheimer’s disease – Where do we go from here? Biochem Biophys Res Commun 633:72–76. https://doi.org/10.1016/j.bbrc.2022.08.075
  56. Levy E, Carman MD, Fernandez-Madrid IJ, Power MD, Lieberburg I, van Duinen SG, Bots GT, Luyendijk W, Frangione B (1990) Mutation of the Alzheimer’s Disease Amyloid Gene in Hereditary Cerebral Hemorrhage, Dutch Type. Science 248: 1124–1126. https://doi.org/10.1126/science.2111584
  57. Zhang X, Fu Z, Meng L, He M, Zhang Z (2018) The Early Events That Initiate β-Amyloid Aggregation in Alzheimer’s Disease. Front Aging Neurosci 10: 359. https://doi.org/10.3389/fnagi.2018.00359
  58. Puzzo D, Gulisano W, Palmeri A, Arancio O (2015) Rodent models for Alzheimer’s disease drug discovery. Expert Opin Drug Discov 10: 703–711. https://doi.org/10.1517/17460441.2015.1041913
  59. LaFerla FM, Green KN (2012) Animal Models of Alzheimer Disease. Cold Spring Harbor Perspect Med 2: a006320. https://doi.org/10.1101/cshperspect.a006320
  60. Drummond E, Wisniewski T (2017) Alzheimer’s disease: experimental models and reality. Acta Neuropathol 133: 155–175. https://doi.org/10.1007/s00401-016-1662-x
  61. Esquerda-Canals G, Montoliu-Gaya L, Güell-Bosch J, Villegas S (2017) Mouse Models of Alzheimer’s Disease. J Alzheimer’s Disease 57: 1171–1183. https://doi.org/10.3233/JAD-170045
  62. Jawhar S, Trawicka A, Jenneckens C, Bayer TA, Wirths O (2012) Motor deficits, neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal Aβ aggregation in the 5XFAD mouse model of Alzheimer’s disease. Neurobiol Aging 33: 196.e29. https://doi.org/10.1016/j.neurobiolaging.2010.05.027
  63. Jean YY, Baleriola J, Fà M, Hengst U, Troy CM (2015) Stereotaxic Infusion of Oligomeric Amyloid-beta into the Mouse Hippocampus. J Visual Experim 100: e52805. https://doi.org/10.3791/52805
  64. Frautschy SA., Yang F, Calderón L, Cole GM (1996) Rodent models of Alzheimer’s disease: Rat aβ infusion approaches to amyloid deposits. Neurobiol Aging 17: 311–332. https://doi.org/10.1016/0197-4580(95)02073-X
  65. O'Hare E, Weldon DT, Mantyh PW, Ghilardi JR, Finke MP, Kuskowski MA, Maggio JE, Shephard RA, Cleary J (1999) Delayed behavioral effects following intrahippocampal injection of aggregated Aβ(1-42). Brain Res 815: 1–10. https://doi.org/10.1016/s0006-8993(98)01002-6
  66. Scuderi C, Stecca C, Valenza M, Ratano P, Bronzuoli MR, Bartoli S, Steardo L, Pompili E, Fumagalli L, Campolongo P, Steardo L (2014) Palmitoylethanolamide controls reactive gliosis and exerts neuroprotective functions in a rat model of Alzheimer’s disease. Cell Death & Disease 5: e1419. https://doi.org/10.1038/cddis.2014.376
  67. Bolmont T, Clavaguera F, Meyer-Luehmann M, Herzig MC, Radde R, Staufenbiel M, Lewis J, Hutton M, Tolnay M, Jucker M (2007) Induction of Tau Pathology by Intracerebral Infusion of Amyloid-β-Containing Brain Extract and by Amyloid-β Deposition in APP × Tau Transgenic Mice. Am J Pathol 171: 2012–2020. https://doi.org/10.2353/ajpath.2007.070403
  68. Denny CA, Burghardt NS, Schachter DM, Hen R, Drew MR (2012) 4- to 6-week-old adult-born hippocampal neurons influence novelty-evoked exploration and contextual fear conditioning. Hippocampus 22: 1188–1201. https://doi.org/10.1002/hipo.20964
  69. Ohm TG (2007) The dentate gyrus in Alzheimer’s disease. Progr Brain Res 163: 723–740. https://doi.org/10.1016/S0079-6123(07)63039-8
  70. Baleriola J, Walker CA, Jean YY, Crary JF, Troy CM, Nagy PL, Hengst U (2014) Axonally Synthesized ATF4 Transmits a Neurodegenerative Signal across Brain Regions. Cell 158: 1159–1172. https://doi.org/10.1016/j.cell.2014.07.001
  71. Jean YY, Ribe EM, Pero ME, Moskalenko M, Iqbal Z, Marks LJ, Greene LA, Troy CM (2013) Caspase-2 is essential for c-Jun transcriptional activation and Bim induction in neuron death. Biochem J 455: 15–25. https://doi.org/10.1042/BJ20130556
  72. Sotthibundhu A, Sykes AM, Fox B, Underwood CK, Thangnipon W, Coulson EJ (2008) Beta-amyloid(1-42) Induces Neuronal Death through the p75 Neurotrophin Receptor. J Neurosci 28: 3941–3946. https://doi.org/10.1523/JNEUROSCI.0350-08.2008
  73. Jhoo JH, Kim HC, Nabeshima T, Yamada K, Shin EJ, Jhoo WK, Kim W, Kang KS, Jo SA, Woo JI (2004) β-Amyloid (1-42)-induced learning and memory deficits in mice: involvement of oxidative burdens in the hippocampus and cerebral cortex. Behav Brain Res 155: 185–196. https://doi.org/10.1016/j.bbr.2004.04.012
  74. Prediger RD, Franco JL, Pandolfo P, Medeiros R, Duarte FS, Di Giunta G, Figueiredo CP, Farina M, Calixto JB, Takahashi RN, Dafre AL (2007) Differential susceptibility following β-amyloid peptide-(1–40) administration in C57BL/6 and Swiss albino mice: Evidence for a dissociation between cognitive deficits and the glutathione system response. Behav Brain Res 177: 205–213. https://doi.org/10.1016/j.bbr.2006.11.032
  75. Yamada K, Tanaka T, Mamiya T, Shiotani T, Kameyama T, Nabeshima T (1999) Improvement by nefiracetam of β -amyloid-(1-42)-induced learning and memory impairments in rats: Nefiracetam and β -amyloid-induced memory deficits. Br J Pharmacol 126: 235–244. https://doi.org/10.1038/sj.bjp.0702309
  76. Yamaguchi Y, Miyashita H, Tsunekawa H, Mouri A, Kim HC, Saito K, Matsuno T, Kawashima S, Nabeshima T (2006) Effects of a Novel Cognitive Enhancer, Spiro[imidazo-[1,2-a]pyridine-3,2-indan]-2(3 H) -one (ZSET1446), on Learning Impairments Induced by Amyloid-β 1–40 in the Rat. J Pharmacol Exp Ther 317: 1079–1087. https://doi.org/10.1124/jpet.105.098640
  77. Yan JJ, Cho JY, Kim HS, Kim KL, Jung JS, Huh SO, Suh HW, Kim YH, Song DK (2001) Protection against β-amyloid peptide toxicity in vivo with long-term administration of ferulic acid: In vivo protection against b-amyloid toxicity with ferulic acid. Br J Pharmacol 133: 89–96. https://doi.org/10.1038/sj.bjp.0704047
  78. Figueiredo CP, Bicca MA, Latini A, Prediger RD, Medeiros R, Calixto JB (2011) Folic Acid Plus α-Tocopherol Mitigates Amyloid-β-Induced Neurotoxicity through Modulation of Mitochondrial Complexes Activity. J Alzheimer’s Disease 24: 61–75. https://doi.org/10.3233/JAD-2010-101320
  79. Piermartiri TCB, Figueiredo CP, Rial D, Duarte FS, Bezerra SC, Mancini G, de Bem AF, Prediger RDS, Tasca CI (2010) Atorvastatin prevents hippocampal cell death, neuroinflammation and oxidative stress following amyloid-β1-40 administration in mice: Evidence for dissociation between cognitive deficits and neuronal damage. Exp Neurol 226: 274–284. https://doi.org/10.1016/j.expneurol.2021.113840
  80. Santos DB, Peres KC, Ribeiro RP, Colle D, dos Santos AA, Moreira EL, Souza DO, Figueiredo CP, Farina M (2012) Probucol, a lipid-lowering drug, prevents cognitive and hippocampal synaptic impairments induced by amyloid β peptide in mice. Exp Neurol 233: 767–775. https://doi.org/10.1016/j.expneurol.2011.11.036
  81. Minogue AM, Schmid AW, Fogarty MP, Moore AC, Campbell VA, Herron CE, Lynch MA (2003) Activation of the c-Jun N-terminal Kinase Signaling Cascade Mediates the Effect of Amyloid-β on Long Term Potentiation and Cell Death in Hippocampus. J Biol Chem 278: 27971–27980. https://doi.org/10.1074/jbc.M302530200
  82. Figueiredo CP, Clarke JR, Ledo JH, Ribeiro FC, Costa CV, Melo HM, Mota-Sales AP, Saraiva LM, Klein WL, Sebollela A, De Felice FG, Ferreira ST (2013) Memantine Rescues Transient Cognitive Impairment Caused by High-Molecular-Weight A Oligomers But Not the Persistent Impairment Induced by Low-Molecular-Weight Oligomers. J Neurosci 33: 9626–9634. https://doi.org/10.1523/JNEUROSCI.0482-13.2013
  83. Ledo JH, Azevedo EP, Clarke JR, Ribeiro FC, Figueiredo CP, Foguel D, De Felice FG, Ferreira ST (2013) Amyloid-β oligomers link depressive-like behavior and cognitive deficits in mice. Mol Psychiatry 18: 1053–1054. https://doi.org/10.1038/mp.2012.168
  84. Elder GA, Gama Sosa MA, De Gasperi R (2010) Transgenic Mouse Models of Alzheimer’s Disease. Mount Sinai J Med 77(1): 69–81. https://doi.org/10.1002/msj.20159
  85. Kim HY, Lee DK, Chung BR, Kim HV, Kim Y (2016) Intracerebroventricular Injection of Amyloid-β Peptides in Normal Mice to Acutely Induce Alzheimer-like Cognitive Deficits. J Visual Experim 109: 53308. https://doi.org/10.3791/53308

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