Synthetic, Cell-Derived, Brain-Derived, and Recombinant β-Amyloid: Modelling Alzheimer’s Disease for Research and Drug Development
Abstract
:1. Introduction
2. Structure of Aβ Aggregates
2.1. Synthetic and Brain-Derived Aβ Oligomers and Fibrils
2.2. Synthetic and Cell-Derived Aβ Aggregates
2.3. Synthetic and Recombinant Aβ Aggregates
3. Biological Effects of Aβ In Vitro and In Vivo
3.1. Synthetic and Brain-Derived Aβ Effects in Cultured Cells
3.1.1. Tau Phosphorylation and Cytoskeletal Disruption
3.1.2. Receptor Interaction
3.1.3. Ion Channel Modulation and Neuronal Survival
3.2. Synthetic and Natural Aβ in Animal Models of Alzheimer’s Disease
3.2.1. Cerebral Amyloidosis
3.2.2. Tau Phosphorylation and Cytoskeletal Disruption In Vivo
3.2.3. Receptor Interaction In Vivo
3.2.4. Memory and Cognition
3.3. Studies of Aβ in the Acute Slice Model
3.3.1. Effects of Aβ on LTP and LTD
3.3.2. Aβ-Induced Tau Abnormalities in Acute Slices
4. Factors behind the Different Properties of Brain-Derived, Cell-Derived, and Synthetic Aβ
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Anand, R.; Gill, K.D.; Mahdi, A.A. Therapeutics of Alzheimer’s disease: Past, present and future. Neuropharmacology 2014, 76 (Pt A), 27–50. [Google Scholar] [CrossRef] [PubMed]
- Chen, G.-F.; Xu, T.-H.; Yan, Y.; Zhou, Y.-R.; Jiang, Y.; Melcher, K.; Xu, H.E. Amyloid beta: Structure, biology and structure-based therapeutic development. Acta Pharmacol. Sin. 2017, 38, 1205–1235. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lublin, A.L.; Gandy, S. Amyloid-β Oligomers: Possible Roles as Key Neurotoxins in Alzheimer’s Disease. Mt. Sinai J. Med. N. Y. 2010, 77, 43–49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kayed, R.; Lasagna-Reeves, C.A. Molecular Mechanisms of Amyloid Oligomers Toxicity. J. Alzheimers Dis. 2013, 33, S67–S78. [Google Scholar] [CrossRef] [Green Version]
- Bloom, G.S. Amyloid-β and tau: The trigger and bullet in Alzheimer disease pathogenesis. JAMA Neurol. 2014, 71, 505–508. [Google Scholar] [CrossRef] [Green Version]
- Musiek, E.S.; Holtzman, D.M. Three dimensions of the amyloid hypothesis: Time, space and “wingmen”. Nat. Neurosci. 2015, 18, 800–806. [Google Scholar] [CrossRef] [Green Version]
- Doens, D.; Fernández, P.L. Microglia receptors and their implications in the response to amyloid β for Alzheimer’s disease pathogenesis. J. Neuroinflamm. 2014, 11, 48. [Google Scholar] [CrossRef] [Green Version]
- Ranjan, V.D.; Qiu, L.; Tan, E.K.; Zeng, L.; Zhang, Y. Modelling Alzheimer’s disease: Insights from in vivo to in vitro three-dimensional culture platforms. J. Tissue Eng. Regen. Med. 2018, 12, 1944–1958. [Google Scholar] [CrossRef]
- Saraceno, C.; Musardo, S.; Marcello, E.; Pelucchi, S.; Diluca, M. Modeling Alzheimer’s disease: From past to future. Front. Pharmacol. 2013, 4, 77. [Google Scholar] [CrossRef] [Green Version]
- Cho, S.; Wood, A.; Bowlby, M.R. Brain Slices as Models for Neurodegenerative Disease and Screening Platforms to Identify Novel Therapeutics. Curr. Neuropharmacol. 2007, 5, 19–33. [Google Scholar] [CrossRef]
- Gerakis, Y.; Hetz, C. Brain organoids: A next step for humanized Alzheimer’s disease models? Mol. Psychiatry 2019, 24, 474–478. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, X.; Crick, S.L.; Bu, G.; Frieden, C.; Pappu, R.V.; Lee, J.-M. Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc. Natl. Acad. Sci. USA 2009, 106, 20324–20329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seubert, P.; Vigo-Pelfrey, C.; Esch, F.; Lee, M.; Dovey, H.; Davis, D.; Sinha, S.; Schiossmacher, M.; Whaley, J.; Swindlehurst, C.; et al. Isolation and quantification of soluble Alzheimer’s β-peptide from biological fluids. Nature 1992, 359, 325–327. [Google Scholar] [CrossRef] [PubMed]
- Chaney, M.O.; Stine, W.B.; Kokjohn, T.A.; Kuo, Y.-M.; Esh, C.; Rahman, A.; Luehrs, D.C.; Schmidt, A.M.; Stern, D.; Yan, S.D.; et al. RAGE and amyloid beta interactions: Atomic force microscopy and molecular modeling. Biochim. Biophys. Acta BBA-Mol. Basis Dis. 2005, 1741, 199–205. [Google Scholar] [CrossRef] [Green Version]
- Gong, Y.; Chang, L.; Viola, K.L.; Lacor, P.N.; Lambert, M.P.; Finch, C.E.; Krafft, G.A.; Klein, W.L. Alzheimer’s disease-affected brain: Presence of oligomeric Aβ ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc. Natl. Acad. Sci. USA 2003, 100, 10417–10422. [Google Scholar] [CrossRef] [Green Version]
- Wickramasinghe, A.; Xiao, Y.; Kobayashi, N.; Wang, S.; Scherpelz, K.P.; Yamazaki, T.; Meredith, S.C.; Ishii, Y. Sensitivity-Enhanced Solid-State NMR Detection of Structural Differences and Unique Polymorphs in Pico- to Nanomolar Amounts of Brain-Derived and Synthetic 42-Residue Amyloid-β Fibrils. J. Am. Chem. Soc. 2021, 143, 11462–11472. [Google Scholar] [CrossRef]
- Moore, B.D.; Rangachari, V.; Tay, W.M.; Milkovic, N.M.; Rosenberry, T.L. Biophysical Analyses of Synthetic Amyloid-β(1−42) Aggregates before and after Covalent Cross-Linking. Implications for Deducing the Structure of Endogenous Amyloid-β Oligomers. Biochemistry 2009, 48, 11796–11806. [Google Scholar] [CrossRef]
- Kollmer, M.; Close, W.; Funk, L.; Rasmussen, J.; Bsoul, A.; Schierhorn, A.; Schmidt, M.; Sigurdson, C.J.; Jucker, M.; Fändrich, M. Cryo-EM structure and polymorphism of Aβ amyloid fibrils purified from Alzheimer’s brain tissue. Nat. Commun. 2019, 10, 4760. [Google Scholar] [CrossRef] [Green Version]
- Romano, A.; Serafino, A.; Krasnowska, E.; Ciotti, M.T.; Calissano, P.; Ruberti, F.; Galli, C. Neuronal fibrillogenesis: Amyloid fibrils from primary neuronal cultures impair long-term memory in the crab Chasmagnathus. Behav. Brain Res. 2003, 147, 73–82. [Google Scholar] [CrossRef]
- Podlisny, M.B.; Ostaszewski, B.L.; Squazzo, S.L.; Koo, E.H.; Rydell, R.E.; Teplow, D.B.; Selkoe, D.J. Aggregation of Secreted Amyloid β-Protein into Sodium Dodecyl Sulfate-stable Oligomers in Cell Culture (∗). J. Biol. Chem. 1995, 270, 9564–9570. [Google Scholar] [CrossRef]
- Podlisny, M.B.; Walsh, D.M.; Amarante, P.; Ostaszewski, B.L.; Stimson, E.R.; Maggio, J.E.; Teplow, D.B.; Selkoe, D.J. Oligomerization of endogenous and synthetic amyloid beta-protein at nanomolar levels in cell culture and stabilization of monomer by Congo red. Biochemistry 1998, 37, 3602–3611. [Google Scholar] [CrossRef] [PubMed]
- Walsh, D.M.; Klyubin, I.; Fadeeva, J.V.; Cullen, W.K.; Anwyl, R.; Wolfe, M.S.; Rowan, M.J.; Selkoe, D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416, 535–539. [Google Scholar] [CrossRef] [PubMed]
- Adams, D.J.; Nemkov, T.G.; Mayer, J.P.; Old, W.M.; Stowell, M.H.B. Identification of the primary peptide contaminant that inhibits fibrillation and toxicity in synthetic amyloid-β42. PLoS ONE 2017, 12, e0182804. [Google Scholar] [CrossRef] [Green Version]
- Finder, V.H.; Vodopivec, I.; Nitsch, R.M.; Glockshuber, R. The Recombinant Amyloid-β Peptide Aβ1–42 Aggregates Faster and Is More Neurotoxic than Synthetic Aβ1–42. J. Mol. Biol. 2010, 396, 9–18. [Google Scholar] [CrossRef]
- Hartley, D.M.; Walsh, D.M.; Ye, C.P.; Diehl, T.; Vasquez, S.; Vassilev, P.M.; Teplow, D.B.; Selkoe, D.J. Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J. Neurosci. 1999, 19, 8876–8884. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pike, C.J.; Cummings, B.J.; Cotman, C.W. beta-Amyloid induces neuritic dystrophy in vitro: Similarities with Alzheimer pathology. Neuroreport 1992, 3, 769–772. [Google Scholar] [CrossRef]
- Li, X.; Uemura, K.; Hashimoto, T.; Nasser-Ghodsi, N.; Arimon, M.; Lill, C.M.; Palazzolo, I.; Krainc, D.; Hyman, B.T.; Berezovska, O. Neuronal activity and secreted amyloid β lead to altered amyloid β precursor protein and presenilin 1 interactions. Neurobiol. Dis. 2013, 50, 127–134. [Google Scholar] [CrossRef] [Green Version]
- Zimbone, S.; Monaco, I.; Gianì, F.; Pandini, G.; Copani, A.G.; Giuffrida, M.L.; Rizzarelli, E. Amyloid Beta monomers regulate cyclic adenosine monophosphate response element binding protein functions by activating type-1 insulin-like growth factor receptors in neuronal cells. Aging Cell 2018, 17, e12684. [Google Scholar] [CrossRef]
- Wang, Z.-F.; Li, H.-L.; Li, X.-C.; Zhang, Q.; Tian, Q.; Wang, Q.; Xu, H.; Wang, J.-Z. Effects of endogenous β-amyloid overproduction on tau phosphorylation in cell culture. J. Neurochem. 2006, 98, 1167–1175. [Google Scholar] [CrossRef]
- Takashima, A.; Noguchi, K.; Michel, G.; Mercken, M.; Hoshi, M.; Ishiguro, K.; Imahori, K. Exposure of rat hippocampal neurons to amyloid β peptide (25–35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3β. Neurosci. Lett. 1996, 203, 33–36. [Google Scholar] [CrossRef]
- Takashima, A.; Honda, T.; Yasutake, K.; Michel, G.; Murayama, O.; Murayama, M.; Ishiguro, K.; Yamaguchi, H. Activation of tau protein kinase I/glycogen synthase kinase-3β by amyloid β peptide (25–35) enhances phosphorylation of tau in hippocampal neurons. Neurosci. Res. 1998, 31, 317–323. [Google Scholar] [CrossRef] [PubMed]
- Hoshi, M.; Sato, M.; Matsumoto, S.; Noguchi, A.; Yasutake, K.; Yoshida, N.; Sato, K. Spherical aggregates of β-amyloid (amylospheroid) show high neurotoxicity and activate tau protein kinase I/glycogen synthase kinase-3β. Proc. Natl. Acad. Sci. USA 2003, 100, 6370–6375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jin, M.; Shepardson, N.; Yang, T.; Chen, G.; Walsh, D.; Selkoe, D.J. Soluble amyloid β-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc. Natl. Acad. Sci. USA 2011, 108, 5819–5824. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Park, J.; Wetzel, I.; Marriott, I.; Dréau, D.; D’Avanzo, C.; Kim, D.Y.; Tanzi, R.E.; Cho, H. A 3D human triculture system modeling neurodegeneration and neuroinflammation in Alzheimer’s disease. Nat. Neurosci. 2018, 21, 941–951. [Google Scholar] [CrossRef] [PubMed]
- Zhang, D.; Pekkanen-Mattila, M.; Shahsavani, M.; Falk, A.; Teixeira, A.I.; Herland, A. A 3D Alzheimer’s disease culture model and the induction of P21-activated kinase mediated sensing in iPSC derived neurons. Biomaterials 2014, 35, 1420–1428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ishizuka, Y.; Hanamura, K. Drebrin in Alzheimer’s Disease. Adv. Exp. Med. Biol. 2017, 1006, 203–223. [Google Scholar] [CrossRef] [PubMed]
- Wiatrak, B.; Piasny, J.; Kuźniarski, A.; Gąsiorowski, K. Interactions of Amyloid-β with Membrane Proteins. Int. J. Mol. Sci. 2021, 22, 6075. [Google Scholar] [CrossRef] [PubMed]
- Dewachter, I.; Filipkowski, R.K.; Priller, C.; Ris, L.; Neyton, J.; Croes, S.; Terwel, D.; Gysemans, M.; Devijver, H.; Borghgraef, P.; et al. Deregulation of NMDA-receptor function and down-stream signaling in APP[V717I] transgenic mice. Neurobiol. Aging 2009, 30, 241–256. [Google Scholar] [CrossRef] [PubMed]
- Cascella, R.; Evangelisti, E.; Bigi, A.; Becatti, M.; Fiorillo, C.; Stefani, M.; Chiti, F.; Cecchi, C. Soluble Oligomers Require a Ganglioside to Trigger Neuronal Calcium Overload. J. Alzheimers Dis. JAD 2017, 60, 923–938. [Google Scholar] [CrossRef]
- Liu, J.; Chang, L.; Roselli, F.; Almeida, O.F.X.; Gao, X.; Wang, X.; Yew, D.T.; Wu, Y. Amyloid-β Induces Caspase-Dependent Loss of PSD-95 and Synaptophysin Through NMDA Receptors. J. Alzheimers Dis. 2010, 22, 541–556. [Google Scholar] [CrossRef]
- De Felice, F.G.; Velasco, P.T.; Lambert, M.P.; Viola, K.; Fernandez, S.J.; Ferreira, S.T.; Klein, W.L. Abeta oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J. Biol. Chem. 2007, 282, 11590–11601. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Almeida, C.G.; Tampellini, D.; Takahashi, R.H.; Greengard, P.; Lin, M.T.; Snyder, E.M.; Gouras, G.K. Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol. Dis. 2005, 20, 187–198. [Google Scholar] [CrossRef] [PubMed]
- Jämsä, A.; Belda, O.; Edlund, M.; Lindström, E. BACE-1 inhibition prevents the γ-secretase inhibitor evoked Aβ rise in human neuroblastoma SH-SY5Y cells. J. Biomed. Sci. 2011, 18, 76. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lilja, A.M.; Porras, O.; Storelli, E.; Nordberg, A.; Marutle, A. Functional interactions of fibrillar and oligomeric amyloid-β with alpha7 nicotinic receptors in Alzheimer’s disease. J. Alzheimers Dis. JAD 2011, 23, 335–347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kamynina, A.V.; Holmström, K.M.; Koroev, D.O.; Volpina, O.M.; Abramov, A.Y. Acetylcholine and antibodies against the acetylcholine receptor protect neurons and astrocytes against beta-amyloid toxicity. Int. J. Biochem. Cell Biol. 2013, 45, 899–907. [Google Scholar] [CrossRef] [Green Version]
- Calabrese, B.; Shaked, G.M.; Tabarean, I.V.; Braga, J.; Koo, E.H.; Halpain, S. Rapid, concurrent alterations in pre- and postsynaptic structure induced by naturally-secreted amyloid-β protein. Mol. Cell. Neurosci. 2007, 35, 183–193. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giuffrida, M.L.; Caraci, F.; De Bona, P.; Pappalardo, G.; Nicoletti, F.; Rizzarelli, E.; Copani, A. The monomer state of beta-amyloid: Where the Alzheimer’s disease protein meets physiology. Rev. Neurosci. 2010, 21, 83–93. [Google Scholar] [CrossRef] [PubMed]
- Plant, L.D.; Boyle, J.P.; Smith, I.F.; Peers, C.; Pearson, H.A. The Production of Amyloid β Peptide Is a Critical Requirement for the Viability of Central Neurons. J. Neurosci. 2003, 23, 5531–5535. [Google Scholar] [CrossRef] [Green Version]
- Plant, L.D.; Webster, N.J.; Boyle, J.P.; Ramsden, M.; Freir, D.B.; Peers, C.; Pearson, H.A. Amyloid β peptide as a physiological modulator of neuronal ‘A’-type K+ current. Neurobiol. Aging 2006, 27, 1673–1683. [Google Scholar] [CrossRef]
- Mehta, P.D.; Pirttilä, T.; Mehta, S.P.; Sersen, E.A.; Aisen, P.S.; Wisniewski, H.M. Plasma and Cerebrospinal Fluid Levels of Amyloid β Proteins 1-40 and 1-42 in Alzheimer Disease. Arch. Neurol. 2000, 57, 100–105. [Google Scholar] [CrossRef]
- Fagan, A.M.; Roe, C.M.; Xiong, C.; Mintun, M.A.; Morris, J.C.; Holtzman, D.M. Cerebrospinal fluid tau/beta-amyloid(42) ratio as a prediction of cognitive decline in nondemented older adults. Arch. Neurol. 2007, 64, 343–349. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ondrejcak, T.; Klyubin, I.; Corbett, G.T.; Fraser, G.; Hong, W.; Mably, A.J.; Gardener, M.; Hammersley, J.; Perkinton, M.S.; Billinton, A.; et al. Cellular Prion Protein Mediates the Disruption of Hippocampal Synaptic Plasticity by Soluble Tau In Vivo. J. Neurosci. 2018, 38, 10595–10606. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giuffrida, M.L.; Caraci, F.; Pignataro, B.; Cataldo, S.; Bona, P.D.; Bruno, V.; Molinaro, G.; Pappalardo, G.; Messina, A.; Palmigiano, A.; et al. β-Amyloid Monomers Are Neuroprotective. J. Neurosci. 2009, 29, 10582–10587. [Google Scholar] [CrossRef] [Green Version]
- Bate, C.; Williams, A. Monomeric amyloid-β reduced amyloid-β oligomer-induced synapse damage in neuronal cultures. Neurobiol. Dis. 2018, 111, 48–58. [Google Scholar] [CrossRef] [Green Version]
- Kaushal, A.; Wani, W.Y.; Anand, R.; Gill, K.D. Spontaneous and induced nontransgenic animal models of AD: Modeling AD using combinatorial approach. Am. J. Alzheimers Dis. Other Demen. 2013, 28, 318–326. [Google Scholar] [CrossRef] [PubMed]
- Stéphan, A.; Phillips, A.G. A case for a non-transgenic animal model of Alzheimer’s disease. Genes Brain Behav. 2005, 4, 157–172. [Google Scholar] [CrossRef]
- Lecanu, L.; Papadopoulos, V. Modeling Alzheimer’s disease with non-transgenic rat models. Alzheimers Res. Ther. 2013, 5, 17. [Google Scholar] [CrossRef] [Green Version]
- Meyer-Luehmann, M.; Coomaraswamy, J.; Bolmont, T.; Kaeser, S.; Schaefer, C.; Kilger, E.; Neuenschwander, A.; Abramowski, D.; Frey, P.; Jaton, A.L.; et al. Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 2006, 313, 1781–1784. [Google Scholar] [CrossRef]
- Kane, M.D.; Lipinski, W.J.; Callahan, M.J.; Bian, F.; Durham, R.A.; Schwarz, R.D.; Roher, A.E.; Walker, L.C. Evidence for seeding of beta -amyloid by intracerebral infusion of Alzheimer brain extracts in beta -amyloid precursor protein-transgenic mice. J. Neurosci. 2000, 20, 3606–3611. [Google Scholar] [CrossRef] [Green Version]
- Fritschi, S.K.; Cintron, A.; Ye, L.; Mahler, J.; Bühler, A.; Baumann, F.; Neumann, M.; Nilsson, K.P.R.; Hammarström, P.; Walker, L.C.; et al. Aβ seeds resist inactivation by formaldehyde. Acta Neuropathol. 2014, 128, 477–484. [Google Scholar] [CrossRef]
- Kuo, Y.M.; Kokjohn, T.A.; Beach, T.G.; Sue, L.I.; Brune, D.; Lopez, J.C.; Kalback, W.M.; Abramowski, D.; Sturchler-Pierrat, C.; Staufenbiel, M.; et al. Comparative analysis of amyloid-beta chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer’s disease brains. J. Biol. Chem. 2001, 276, 12991–12998. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rasmussen, J.; Mahler, J.; Beschorner, N.; Kaeser, S.A.; Häsler, L.M.; Baumann, F.; Nyström, S.; Portelius, E.; Blennow, K.; Lashley, T.; et al. Amyloid polymorphisms constitute distinct clouds of conformational variants in different etiological subtypes of Alzheimer’s disease. Proc. Natl. Acad. Sci. USA 2017, 114, 13018–13023. [Google Scholar] [CrossRef] [Green Version]
- Duran-Aniotz, C.; Moreno-Gonzalez, I.; Gamez, N.; Perez-Urrutia, N.; Vegas-Gomez, L.; Soto, C.; Morales, R. Amyloid pathology arrangements in Alzheimer’s disease brains modulate in vivo seeding capability. Acta Neuropathol. Commun. 2021, 9, 56. [Google Scholar] [CrossRef] [PubMed]
- Watts, J.C.; Condello, C.; Stöhr, J.; Oehler, A.; Lee, J.; DeArmond, S.J.; Lannfelt, L.; Ingelsson, M.; Giles, K.; Prusiner, S.B. Serial propagation of distinct strains of Aβ prions from Alzheimer’s disease patients. Proc. Natl. Acad. Sci. USA 2014, 111, 10323–10328. [Google Scholar] [CrossRef] [Green Version]
- Ridley, R.M.; Baker, H.F.; Windle, C.P.; Cummings, R.M. Very long term studies of the seeding of beta-amyloidosis in primates. J. Neural Transm. 2006, 113, 1243–1251. [Google Scholar] [CrossRef]
- Stöhr, J.; Watts, J.C.; Mensinger, Z.L.; Oehler, A.; Grillo, S.K.; DeArmond, S.J.; Prusiner, S.B.; Giles, K. Purified and synthetic Alzheimer’s amyloid beta (Aβ) prions. Proc. Natl. Acad. Sci. USA 2012, 109, 11025–11030. [Google Scholar] [CrossRef] [Green Version]
- Kozin, S.A.; Cheglakov, I.B.; Ovsepyan, A.A.; Telegin, G.B.; Tsvetkov, P.O.; Lisitsa, A.V.; Makarov, A.A. Peripherally applied synthetic peptide isoAsp7-Aβ(1-42) triggers cerebral β-amyloidosis. Neurotox. Res. 2013, 24, 370–376. [Google Scholar] [CrossRef] [PubMed]
- Stancu, I.-C.; Vasconcelos, B.; Terwel, D.; Dewachter, I. Models of β-amyloid induced Tau-pathology: The long and “folded” road to understand the mechanism. Mol. Neurodegener. 2014, 9, 51. [Google Scholar] [CrossRef] [Green Version]
- Selenica, M.-L.B.; Brownlow, M.; Jimenez, J.P.; Lee, D.C.; Pena, G.; Dickey, C.A.; Gordon, M.N.; Morgan, D. Amyloid Oligomers Exacerbate Tau Pathology in a Mouse Model of Tauopathy. Neurodegener. Dis. 2013, 11, 165–181. [Google Scholar] [CrossRef] [Green Version]
- Götz, J.; Chen, F.; van Dorpe, J.; Nitsch, R.M. Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science 2001, 293, 1491–1495. [Google Scholar] [CrossRef]
- Bolmont, T.; Clavaguera, F.; Meyer-Luehmann, M.; Herzig, M.C.; Radde, R.; Staufenbiel, M.; Lewis, J.; Hutton, M.; Tolnay, M.; Jucker, M. 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. 2007, 171, 2012–2020. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Klyubin, I.; Wang, Q.; Reed, M.N.; Irving, E.A.; Upton, N.; Hofmeister, J.; Cleary, J.P.; Anwyl, R.; Rowan, M.J. Protection against Aβ-mediated rapid disruption of synaptic plasticity and memory by memantine. Neurobiol. Aging 2011, 32, 614–623. [Google Scholar] [CrossRef] [PubMed]
- Arbel-Ornath, M.; Hudry, E.; Boivin, J.R.; Hashimoto, T.; Takeda, S.; Kuchibhotla, K.V.; Hou, S.; Lattarulo, C.R.; Belcher, A.M.; Shakerdge, N.; et al. Soluble oligomeric amyloid-β induces calcium dyshomeostasis that precedes synapse loss in the living mouse brain. Mol. Neurodegener. 2017, 12, 27. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Müller, M.K.; Jacobi, E.; Sakimura, K.; Malinow, R.; von Engelhardt, J. NMDA receptors mediate synaptic depression, but not spine loss in the dentate gyrus of adult amyloid Beta (Aβ) overexpressing mice. Acta Neuropathol. Commun. 2018, 6, 110. [Google Scholar] [CrossRef] [Green Version]
- Shankar, G.M.; Li, S.; Mehta, T.H.; Garcia-Munoz, A.; Shepardson, N.E.; Smith, I.; Brett, F.M.; Farrell, M.A.; Rowan, M.J.; Lemere, C.A.; et al. Amyloid-β protein dimers isolated directly from Alzheimer’s brains impair synaptic plasticity and memory. Nat. Med. 2008, 14, 837–842. [Google Scholar] [CrossRef] [Green Version]
- Reed, M.N.; Hofmeister, J.J.; Jungbauer, L.; Welzel, A.T.; Yu, C.; Sherman, M.A.; Lesné, S.; LaDu, M.J.; Walsh, D.M.; Ashe, K.H.; et al. Cognitive effects of cell-derived and synthetically-derived Aβ oligomers. Neurobiol. Aging 2011, 32, 1784–1794. [Google Scholar] [CrossRef] [Green Version]
- Hu, N.-W.; Nicoll, A.J.; Zhang, D.; Mably, A.J.; O’Malley, T.; Purro, S.A.; Terry, C.; Collinge, J.; Walsh, D.M.; Rowan, M.J. mGlu5 receptors and cellular prion protein mediate amyloid-β-facilitated synaptic long-term depression in vivo. Nat. Commun. 2014, 5, 3374. [Google Scholar] [CrossRef] [Green Version]
- Barry, A.E.; Klyubin, I.; Mc Donald, J.M.; Mably, A.J.; Farrell, M.A.; Scott, M.; Walsh, D.M.; Rowan, M.J. Alzheimer’s disease brain-derived amyloid-β-mediated inhibition of LTP in vivo is prevented by immunotargeting cellular prion protein. J. Neurosci. 2011, 31, 7259–7263. [Google Scholar] [CrossRef] [Green Version]
- Klyubin, I.; Betts, V.; Welzel, A.T.; Blennow, K.; Zetterberg, H.; Wallin, A.; Lemere, C.A.; Cullen, W.K.; Peng, Y.; Wisniewski, T.; et al. Amyloid beta protein dimer-containing human CSF disrupts synaptic plasticity: Prevention by systemic passive immunization. J. Neurosci. 2008, 28, 4231–4237. [Google Scholar] [CrossRef] [Green Version]
- Puzzo, D.; Privitera, L.; Leznik, E.; Fà, M.; Staniszewski, A.; Palmeri, A.; Arancio, O. Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci. 2008, 28, 14537–14545. [Google Scholar] [CrossRef] [Green Version]
- Qi, Y.; Shang, L.; Liao, Z.; Su, H.; Jing, H.; Wu, B.; Bi, K.; Jia, Y. Intracerebroventricular injection of resveratrol ameliorated Aβ-induced learning and cognitive decline in mice. Metab. Brain Dis. 2019, 34, 257–266. [Google Scholar] [CrossRef] [PubMed]
- Sharma, S.; Verma, S.; Kapoor, M.; Saini, A.; Nehru, B. Alzheimer’s disease like pathology induced six weeks after aggregated amyloid-beta injection in rats: Increased oxidative stress and impaired long-term memory with anxiety-like behavior. Neurol. Res. 2016, 38, 838–850. [Google Scholar] [CrossRef] [PubMed]
- Wong, R.S.; Cechetto, D.F.; Whitehead, S.N. Assessing the Effects of Acute Amyloid β Oligomer Exposure in the Rat. Int. J. Mol. Sci. 2016, 17, 1390. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nakamura, S.; Murayama, N.; Noshita, T.; Annoura, H.; Ohno, T. Progressive brain dysfunction following intracerebroventricular infusion of beta(1-42)-amyloid peptide. Brain Res. 2001, 912, 128–136. [Google Scholar] [CrossRef]
- Park, S.; Huh, J.-W.; Eom, T.; Na, N.; Lee, Y.; Kim, J.-S.; Kim, S.-U.; Shim, I.; Lee, S.-R.; Kim, E. Effects of Newly Synthesized Recombinant Human Amyloid-β Complexes and Poly-Amyloid-β Fibers on Cell Apoptosis and Cognitive Decline. J. Microbiol. Biotechnol. 2017, 27, 2044–2051. [Google Scholar] [CrossRef] [Green Version]
- Baerends, E.; Soud, K.; Folke, J.; Pedersen, A.-K.; Henmar, S.; Konrad, L.; Lycas, M.D.; Mori, Y.; Pakkenberg, B.; Woldbye, D.P.D.; et al. Modeling the early stages of Alzheimer’s disease by administering intracerebroventricular injections of human native Aβ oligomers to rats. Acta Neuropathol. Commun. 2022, 10, 113. [Google Scholar] [CrossRef]
- Poling, A.; Morgan-Paisley, K.; Panos, J.J.; Kim, E.-M.; O’Hare, E.; Cleary, J.P.; Lesné, S.; Ashe, K.H.; Porritt, M.; Baker, L.E. Oligomers of the amyloid-beta protein disrupt working memory: Confirmation with two behavioral procedures. Behav. Brain Res. 2008, 193, 230–234. [Google Scholar] [CrossRef] [Green Version]
- Dao, A.T.; Zagaar, M.A.; Levine, A.T.; Salim, S.; Eriksen, J.L.; Alkadhi, K.A. Treadmill exercise prevents learning and memory impairment in Alzheimer’s disease-like pathology. Curr. Alzheimer Res. 2013, 10, 507–515. [Google Scholar] [CrossRef]
- Puzzo, D.; Privitera, L.; Fa’, M.; Staniszewski, A.; Hashimoto, G.; Aziz, F.; Sakurai, M.; Ribe, E.M.; Troy, C.M.; Mercken, M.; et al. Endogenous amyloid-β is necessary for hippocampal synaptic plasticity and memory. Ann. Neurol. 2011, 69, 819–830. [Google Scholar] [CrossRef] [Green Version]
- Gulisano, W.; Melone, M.; Ripoli, C.; Tropea, M.R.; Li Puma, D.D.; Giunta, S.; Cocco, S.; Marcotulli, D.; Origlia, N.; Palmeri, A.; et al. Neuromodulatory Action of Picomolar Extracellular Aβ42 Oligomers on Presynaptic and Postsynaptic Mechanisms Underlying Synaptic Function and Memory. J. Neurosci. 2019, 39, 5986–6000. [Google Scholar] [CrossRef]
- Li, S.; Jin, M.; Koeglsperger, T.; Shepardson, N.E.; Shankar, G.M.; Selkoe, D.J. Soluble Aβ oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J. Neurosci. 2011, 31, 6627–6638. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, S.; Hong, S.; Shepardson, N.E.; Walsh, D.M.; Shankar, G.M.; Selkoe, D. Soluble oligomers of amyloid β-protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009, 62, 788–801. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Q.; Walsh, D.M.; Rowan, M.J.; Selkoe, D.J.; Anwyl, R. Block of long-term potentiation by naturally secreted and synthetic amyloid beta-peptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase, cyclin-dependent kinase 5, and p38 mitogen-activated protein kinase as well as metabotropic glutamate receptor type 5. J. Neurosci. 2004, 24, 3370–3378. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, Q.-S.; Wei, W.-Z.; Shimahara, T.; Xie, C.-W. Alzheimer amyloid beta-peptide inhibits the late phase of long-term potentiation through calcineurin-dependent mechanisms in the hippocampal dentate gyrus. Neurobiol. Learn. Mem. 2002, 77, 354–371. [Google Scholar] [CrossRef] [Green Version]
- Lambert, M.P.; Barlow, A.K.; Chromy, B.A.; Edwards, C.; Freed, R.; Liosatos, M.; Morgan, T.E.; Rozovsky, I.; Trommer, B.; Viola, K.L.; et al. Diffusible, nonfibrillar ligands derived from Aβ1–42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA 1998, 95, 6448–6453. [Google Scholar] [CrossRef] [Green Version]
- Townsend, M.; Shankar, G.M.; Mehta, T.; Walsh, D.M.; Selkoe, D.J. Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: A potent role for trimers. J. Physiol. 2006, 572, 477–492. [Google Scholar] [CrossRef]
- Shipton, O.A.; Leitz, J.R.; Dworzak, J.; Acton, C.E.J.; Tunbridge, E.M.; Denk, F.; Dawson, H.N.; Vitek, M.P.; Wade-Martins, R.; Paulsen, O.; et al. Tau Protein Is Required for Amyloid β-Induced Impairment of Hippocampal Long-Term Potentiation. J. Neurosci. 2011, 31, 1688–1692. [Google Scholar] [CrossRef] [Green Version]
- Taylor, H.B.C.; Emptage, N.J.; Jeans, A.F. Long-term depression links amyloid-β to the pathological hyperphosphorylation of tau. Cell Rep. 2021, 36, 109638. [Google Scholar] [CrossRef]
- Mendes, N.D.; Fernandes, A.; Almeida, G.M.; Santos, L.E.; Selles, M.C.; Lyra e Silva, N.M.; Machado, C.M.; Horta-Júnior, J.A.C.; Louzada, P.R.; De Felice, F.G.; et al. Free-floating adult human brain-derived slice cultures as a model to study the neuronal impact of Alzheimer’s disease-associated Aβ oligomers. J. Neurosci. Methods 2018, 307, 203–209. [Google Scholar] [CrossRef] [Green Version]
- Novotny, R.; Langer, F.; Mahler, J.; Skodras, A.; Vlachos, A.; Wegenast-Braun, B.M.; Kaeser, S.A.; Neher, J.J.; Eisele, Y.S.; Pietrowski, M.J.; et al. Conversion of Synthetic Aβ to In Vivo Active Seeds and Amyloid Plaque Formation in a Hippocampal Slice Culture Model. J. Neurosci. 2016, 36, 5084–5093. [Google Scholar] [CrossRef]
- Shankar, G.M.; Bloodgood, B.L.; Townsend, M.; Walsh, D.M.; Selkoe, D.J.; Sabatini, B.L. Natural Oligomers of the Alzheimer Amyloid-β Protein Induce Reversible Synapse Loss by Modulating an NMDA-Type Glutamate Receptor-Dependent Signaling Pathway. J. Neurosci. 2007, 27, 2866–2875. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Teplow, D.B. Preparation of amyloid beta-protein for structural and functional studies. Methods Enzymol. 2006, 413, 20–33. [Google Scholar] [CrossRef] [PubMed]
- Howlett, D.R.; Jennings, K.H.; Lee, D.C.; Clark, M.S.; Brown, F.; Wetzel, R.; Wood, S.J.; Camilleri, P.; Roberts, G.W. Aggregation state and neurotoxic properties of Alzheimer beta-amyloid peptide. Neurodegener. Neuroregeneration 1995, 4, 23–32. [Google Scholar] [CrossRef] [PubMed]
- Simmons, L.K.; May, P.C.; Tomaselli, K.J.; Rydel, R.E.; Fuson, K.S.; Brigham, E.F.; Wright, S.; Lieberburg, I.; Becker, G.W.; Brems, D.N. Secondary structure of amyloid beta peptide correlates with neurotoxic activity in vitro. Mol. Pharmacol. 1994, 45, 373–379. [Google Scholar]
- Bitan, G.; Tarus, B.; Vollers, S.S.; Lashuel, H.A.; Condron, M.M.; Straub, J.E.; Teplow, D.B. A molecular switch in amyloid assembly: Met35 and amyloid beta-protein oligomerization. J. Am. Chem. Soc. 2003, 125, 15359–15365. [Google Scholar] [CrossRef] [Green Version]
- Dahlgren, K.N.; Manelli, A.M.; Stine, W.B.; Baker, L.K.; Krafft, G.A.; LaDu, M.J. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 2002, 277, 32046–32053. [Google Scholar] [CrossRef] [Green Version]
- Stelmashook, E.V.; Isaev, N.K.; Genrikhs, E.E.; Amelkina, G.A.; Khaspekov, L.G.; Skrebitsky, V.G.; Illarioshkin, S.N. Role of zinc and copper ions in the pathogenetic mechanisms of Alzheimer’s and Parkinson’s diseases. Biochem. Biokhimiia 2014, 79, 391–396. [Google Scholar] [CrossRef]
- Atwood, C.S.; Scarpa, R.C.; Huang, X.; Moir, R.D.; Jones, W.D.; Fairlie, D.P.; Tanzi, R.E.; Bush, A.I. Characterization of copper interactions with alzheimer amyloid beta peptides: Identification of an attomolar-affinity copper binding site on amyloid beta1-42. J. Neurochem. 2000, 75, 1219–1233. [Google Scholar] [CrossRef]
- Cherny, R.A.; Legg, J.T.; McLean, C.A.; Fairlie, D.P.; Huang, X.; Atwood, C.S.; Beyreuther, K.; Tanzi, R.E.; Masters, C.L.; Bush, A.I. Aqueous dissolution of Alzheimer’s disease Abeta amyloid deposits by biometal depletion. J. Biol. Chem. 1999, 274, 23223–23228. [Google Scholar] [CrossRef] [Green Version]
- Williamson, R.; Usardi, A.; Hanger, D.P.; Anderton, B.H. Membrane-bound beta-amyloid oligomers are recruited into lipid rafts by a fyn-dependent mechanism. FASEB J. 2008, 22, 1552–1559. [Google Scholar] [CrossRef]
- Ahyayauch, H.; Masserini, M.; Goñi, F.M.; Alonso, A. The interaction of Aβ42 peptide in monomer, oligomer or fibril forms with sphingomyelin/cholesterol/ganglioside bilayers. Int. J. Biol. Macromol. 2021, 168, 611–619. [Google Scholar] [CrossRef] [PubMed]
- Kozin, S.A.; Barykin, E.P.; Mitkevich, V.A.; Makarov, A.A. Anti-amyloid Therapy of Alzheimer’s Disease: Current State and Prospects. Biochem. Biokhimiia 2018, 83, 1057–1067. [Google Scholar] [CrossRef] [PubMed]
- Willem, M.; Tahirovic, S.; Busche, M.A.; Ovsepian, S.V.; Chafai, M.; Kootar, S.; Hornburg, D.; Evans, L.D.B.; Moore, S.; Daria, A.; et al. η-Secretase processing of APP inhibits neuronal activity in the hippocampus. Nature 2015, 526, 443–447. [Google Scholar] [CrossRef] [PubMed]
- Welzel, A.T.; Maggio, J.E.; Shankar, G.M.; Walker, D.E.; Ostaszewski, B.L.; Li, S.; Klyubin, I.; Rowan, M.J.; Seubert, P.; Walsh, D.M.; et al. Secreted Amyloid β-Proteins in a Cell Culture Model Include N-Terminally Extended Peptides That Impair Synaptic Plasticity. Biochemistry 2014, 53, 3908–3921. [Google Scholar] [CrossRef]
- Bugrova, A.E.; Strelnikova, P.A.; Indeykina, M.I.; Kononikhin, A.S.; Zakharova, N.V.; Brzhozovskiy, A.G.; Barykin, E.P.; Pekov, S.I.; Gavrish, M.S.; Babaev, A.A.; et al. The Dynamics of β-Amyloid Proteoforms Accumulation in the Brain of a 5xFAD Mouse Model of Alzheimer’s Disease. Int. J. Mol. Sci. 2021, 23, 27. [Google Scholar] [CrossRef]
- Wildburger, N.C.; Esparza, T.J.; LeDuc, R.D.; Fellers, R.T.; Thomas, P.M.; Cairns, N.J.; Kelleher, N.L.; Bateman, R.J.; Brody, D.L. Diversity of Amyloid-beta Proteoforms in the Alzheimer’s Disease Brain. Sci. Rep. 2017, 7, 9520. [Google Scholar] [CrossRef] [Green Version]
- Medvedev, A.E.; Radko, S.P.; Yurinskaya, M.M.; Vinokurov, M.G.; Buneeva, O.A.; Kopylov, A.T.; Kozin, S.A.; Mitkevich, V.A.; Makarov, A.A. Neurotoxic Effects of Aβ 6-42 Peptides Mimicking Putative Products Formed by the Angiotensin Converting Enzyme. J. Alzheimers Dis. 2018, 66, 263–270. [Google Scholar] [CrossRef]
- Rudinskiy, N.; Fuerer, C.; Demurtas, D.; Zamorano, S.; De Piano, C.; Herrmann, A.G.; Spires-Jones, T.L.; Oeckl, P.; Otto, M.; Frosch, M.P.; et al. Amyloid-beta oligomerization is associated with the generation of a typical peptide fragment fingerprint. Alzheimers Dement. 2016, 12, 996–1013. [Google Scholar] [CrossRef] [Green Version]
- Wang, R.; Sweeney, D.; Gandy, S.E.; Sisodia, S.S. The profile of soluble amyloid beta protein in cultured cell media. Detection and quantification of amyloid beta protein and variants by immunoprecipitation-mass spectrometry. J. Biol. Chem. 1996, 271, 31894–31902. [Google Scholar] [CrossRef] [Green Version]
- Barykin, E.P.; Mitkevich, V.A.; Kozin, S.A.; Makarov, A.A. Amyloid β Modification: A Key to the Sporadic Alzheimer’s Disease? Front. Genet. 2017, 8, 58. [Google Scholar] [CrossRef] [Green Version]
- Kolmogorov, V.S.; Erofeev, A.S.; Barykin, E.P.; Timoshenko, R.V.; Lopatukhina, E.V.; Kozin, S.A.; Salikhov, S.V.; Klyachko, N.L.; Mitkevich, V.A.; Edwards, C.R.W.; et al. Scanning ion-conductance microscopy for studying β-amyloid aggregate formation on living cell surface. bioRxiv 2022. [Google Scholar] [CrossRef]
- Toropygin, I.Y.; Kugaevskaya, E.V.; Mirgorodskaya, O.A.; Elisseeva, Y.E.; Kozmin, Y.P.; Popov, I.A.; Nikolaev, E.N.; Makarov, A.A.; Kozin, S.A. The N-domain of angiotensin-converting enzyme specifically hydrolyzes the Arg-5-His-6 bond of Alzheimer’s Aβ-(1-16) peptide and its isoAsp-7 analogue with different efficiency as evidenced by quantitative matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 2008, 22, 231–239. [Google Scholar] [CrossRef]
- Mitkevich, V.A.; Petrushanko, I.Y.; Yegorov, Y.E.; Simonenko, O.V.; Vishnyakova, K.S.; Kulikova, A.A.; Tsvetkov, P.O.; Makarov, A.A.; Kozin, S.A. Isomerization of Asp7 leads to increased toxic effect of amyloid-β42 on human neuronal cells. Cell Death Dis. 2013, 4, e939. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gunn, A.P.; Wong, B.X.; Johanssen, T.; Griffith, J.C.; Masters, C.L.; Bush, A.I.; Barnham, K.J.; Duce, J.A.; Cherny, R.A. Amyloid-β Peptide Aβ3pE-42 Induces Lipid Peroxidation, Membrane Permeabilization, and Calcium Influx in Neurons. J. Biol. Chem. 2016, 291, 6134–6145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Russo, C.; Violani, E.; Salis, S.; Venezia, V.; Dolcini, V.; Damonte, G.; Benatti, U.; D’Arrigo, C.; Patrone, E.; Carlo, P.; et al. Pyroglutamate-modified amyloid beta-peptides--AbetaN3(pE)--strongly affect cultured neuron and astrocyte survival. J. Neurochem. 2002, 82, 1480–1489. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barnham, K.J.; Haeffner, F.; Ciccotosto, G.D.; Curtain, C.C.; Tew, D.; Mavros, C.; Beyreuther, K.; Carrington, D.; Masters, C.L.; Cherny, R.A.; et al. Tyrosine gated electron transfer is key to the toxic mechanism of Alzheimer’s disease beta-amyloid. FASEB J. 2004, 18, 1427–1429. [Google Scholar] [CrossRef] [PubMed]
- Al-Hilaly, Y.K.; Williams, T.L.; Stewart-Parker, M.; Ford, L.; Skaria, E.; Cole, M.; Bucher, W.G.; Morris, K.L.; Sada, A.A.; Thorpe, J.R.; et al. A central role for dityrosine crosslinking of Amyloid-β in Alzheimer’s disease. Acta Neuropathol. Commun. 2013, 1, 83. [Google Scholar] [CrossRef] [Green Version]
- Barykin, E.P.; Petrushanko, I.Y.; Kozin, S.A.; Telegin, G.B.; Chernov, A.S.; Lopina, O.D.; Radko, S.P.; Mitkevich, V.A.; Makarov, A.A. Phosphorylation of the Amyloid-Beta Peptide Inhibits Zinc-Dependent Aggregation, Prevents Na,K-ATPase Inhibition, and Reduces Cerebral Plaque Deposition. Front. Mol. Neurosci. 2018, 11, 302. [Google Scholar] [CrossRef] [Green Version]
- Kozin, S.A.; Barykin, E.P.; Telegin, G.B.; Chernov, A.S.; Adzhubei, A.A.; Radko, S.P.; Mitkevich, V.A.; Makarov, A.A. Intravenously Injected Amyloid-β Peptide With Isomerized Asp7 and Phosphorylated Ser8 Residues Inhibits Cerebral β-Amyloidosis in AβPP/PS1 Transgenic Mice Model of Alzheimer’s Disease. Front. Neurosci. 2018, 12, 518. [Google Scholar] [CrossRef] [Green Version]
- Lindberg, D.J.; Wranne, M.S.; Gilbert Gatty, M.; Westerlund, F.; Esbjörner, E.K. Steady-state and time-resolved Thioflavin-T fluorescence can report on morphological differences in amyloid fibrils formed by Aβ(1-40) and Aβ(1-42). Biochem. Biophys. Res. Commun. 2015, 458, 418–423. [Google Scholar] [CrossRef] [Green Version]
- Triguero, L.; Singh, R.; Prabhakar, R. Comparative Molecular Dynamics Studies of Wild-Type and Oxidized Forms of Full-Length Alzheimer Amyloid β-Peptides Aβ(1−40) and Aβ(1−42). J. Phys. Chem. B 2008, 112, 7123–7131. [Google Scholar] [CrossRef]
- Lim, K.H.; Collver, H.H.; Le, Y.T.H.; Nagchowdhuri, P.; Kenney, J.M. Characterizations of distinct amyloidogenic conformations of the Aβ (1–40) and (1–42) peptides. Biochem. Biophys. Res. Commun. 2007, 353, 443–449. [Google Scholar] [CrossRef] [PubMed]
- Olofsson, A.; Lindhagen-Persson, M.; Sauer-Eriksson, A.E.; Öhman, A. Amide solvent protection analysis demonstrates that amyloid-β(1–40) and amyloid-β(1–42) form different fibrillar structures under identical conditions. Biochem. J. 2007, 404, 63–70. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barykin, E.P.; Garifulina, A.I.; Kruykova, E.V.; Spirova, E.N.; Anashkina, A.A.; Adzhubei, A.A.; Shelukhina, I.V.; Kasheverov, I.E.; Mitkevich, V.A.; Kozin, S.A.; et al. Isomerization of Asp7 in Beta-Amyloid Enhances Inhibition of the α7 Nicotinic Receptor and Promotes Neurotoxicity. Cells 2019, 8, 771. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Warmack, R.A.; Boyer, D.R.; Zee, C.-T.; Richards, L.S.; Sawaya, M.R.; Cascio, D.; Gonen, T.; Eisenberg, D.S.; Clarke, S.G. Structure of amyloid-β (20-34) with Alzheimer’s-associated isomerization at Asp23 reveals a distinct protofilament interface. Nat. Commun. 2019, 10, 3357. [Google Scholar] [CrossRef] [Green Version]
- Goldblatt, G.; Matos, J.O.; Gornto, J.; Tatulian, S.A. Isotope-edited FTIR reveals distinct aggregation and structural behaviors of unmodified and pyroglutamylated amyloid β peptides. Phys. Chem. Chem. Phys. 2015, 17, 32149–32160. [Google Scholar] [CrossRef] [Green Version]
- Hassan, R.; Abedin, F.; Tatulian, S.A. Structure of unmodified and pyroglutamylated amyloid beta peptides in lipid membranes. Biophys. J. 2022, 121, 328a. [Google Scholar] [CrossRef]
- Rezaei-Ghaleh, N.; Kumar, S.; Walter, J.; Zweckstetter, M. Phosphorylation Interferes with Maturation of Amyloid-β Fibrillar Structure in the N-terminus. J. Biol. Chem. 2016, 291, 16059–16067. [Google Scholar] [CrossRef] [Green Version]
- Hu, Z.-W.; Vugmeyster, L.; Au, D.F.; Ostrovsky, D.; Sun, Y.; Qiang, W. Molecular structure of an N-terminal phosphorylated β-amyloid fibril. Proc. Natl. Acad. Sci. 2019, 116, 11253–11258. [Google Scholar] [CrossRef] [Green Version]
- Hou, L.; Shao, H.; Zhang, Y.; Li, H.; Menon, N.K.; Neuhaus, E.B.; Brewer, J.M.; Byeon, I.-J.L.; Ray, D.G.; Vitek, M.P.; et al. Solution NMR Studies of the Aβ(1−40) and Aβ(1−42) Peptides Establish that the Met35 Oxidation State Affects the Mechanism of Amyloid Formation. J. Am. Chem. Soc. 2004, 126, 1992–2005. [Google Scholar] [CrossRef]
- Hou, L.; Lee, H.; Han, F.; Tedesco, J.M.; Perry, G.; Smith, M.A.; Zagorski, M.G. Modification of Amyloid-β 1-42 Fibril Structure by Methionine-35 Oxidation. J. Alzheimers Dis. 2013, 37, 9–18. [Google Scholar] [CrossRef] [PubMed]
- Medvedev, A.E.; Buneeva, O.A.; Kopylov, A.T.; Mitkevich, V.A.; Kozin, S.A.; Zgoda, V.G.; Makarov, A.A. Chemical modifications of amyloid-β(1-42) have a significant impact on the repertoire of brain amyloid-β(1-42) binding proteins. Biochimie 2016, 128–129, 55–58. [Google Scholar] [CrossRef] [PubMed]
- Tolstova, A.P.; Adzhubei, A.A.; Mitkevich, V.A.; Petrushanko, I.Y.; Makarov, A.A. Docking and Molecular Dynamics-Based Identification of Interaction between Various Beta-Amyloid Isoforms and RAGE Receptor. Int. J. Mol. Sci. 2022, 23, 11816. [Google Scholar] [CrossRef] [PubMed]
- Suvorina, M.Y.; Selivanova, O.M.; Grigorashvili, E.I.; Nikulin, A.D.; Marchenkov, V.V.; Surin, A.K.; Galzitskaya, O.V. Studies of Polymorphism of Amyloid-β 42 Peptide from Different Suppliers. J. Alzheimers Dis. 2015, 47, 583–593. [Google Scholar] [CrossRef] [PubMed]
- Roberts, B.R.; Lind, M.; Wagen, A.Z.; Rembach, A.; Frugier, T.; Li, Q.-X.; Ryan, T.M.; McLean, C.A.; Doecke, J.D.; Rowe, C.C.; et al. Biochemically-defined pools of amyloid-β in sporadic Alzheimer’s disease: Correlation with amyloid PET. Brain 2017, 140, 1486–1498. [Google Scholar] [CrossRef] [Green Version]
- Wang, Z.; Jackson, R.J.; Hong, W.; Taylor, W.M.; Corbett, G.T.; Moreno, A.; Liu, W.; Li, S.; Frosch, M.P.; Slutsky, I.; et al. Human Brain-Derived Aβ Oligomers Bind to Synapses and Disrupt Synaptic Activity in a Manner That Requires APP. J. Neurosci. 2017, 37, 11947–11966. [Google Scholar] [CrossRef] [Green Version]
- Yang, T.; Li, S.; Xu, H.; Walsh, D.M.; Selkoe, D.J. Large Soluble Oligomers of Amyloid β-Protein from Alzheimer Brain Are Far Less Neuroactive Than the Smaller Oligomers to Which They Dissociate. J. Neurosci. 2017, 37, 152–163. [Google Scholar] [CrossRef] [Green Version]
- Tiiman, A.; Krishtal, J.; Palumaa, P.; Tõugu, V. In vitro fibrillization of Alzheimer’s amyloid-β peptide (1-42). AIP Adv. 2015, 5, 092401. [Google Scholar] [CrossRef] [Green Version]
- Zurdo, J.; Guijarro, J.I.; Dobson, C.M. Preparation and Characterization of Purified Amyloid Fibrils. J. Am. Chem. Soc. 2001, 123, 8141–8142. [Google Scholar] [CrossRef]
- Benseny-Cases, N.; Klementieva, O.; Cladera, J. In vitro oligomerization and fibrillogenesis of amyloid-beta peptides. Subcell. Biochem. 2012, 65, 53–74. [Google Scholar] [CrossRef]
Effect | Source of Aβ | Models | ||
---|---|---|---|---|
Cells | In Vivo | Slices | ||
Tau phosphorylation and cytoskeletal disruption | Synthetic Aβ | + (100–500 nM) [31,33,35] | + (100 µM, single injection or prolonged infusion) [69,70] | + (100–500 nM) [97,98,99] |
Cell-derived Aβ | ++ (0.2–0.5 nM) [29,34] | nd | nd | |
Brain-derived Aβ | ++ (0.2–0.5 nM) [33] | ++ (nM, single injection) [71] | +/− (1 nM, only in combination with sAβ) [100] | |
Receptor interaction (NMDAR, AMPAR, nAChR) | Synthetic Aβ | + (300–500 nM–10 µM) [38,39,40,41,44,45] | + [72] | + [91,92] |
Cell-derived Aβ | ++ (subnanomolar concentrations) [42,46] | ++ (pM) [73] | + [91,92,101] | |
Brain-derived Aβ | nd | + (transgenic animals) [38,74] | + [91,92] | |
Cognitive dysfunction/inhibition of LTP | Synthetic Aβ | n/a | + (µM) [76,77,80] | + (200–500 nM) [72,91,92,93,94,95] |
Cell-derived Aβ | n/a | ++ (pM) [76,79] | ++ (100–300 pM–1 nM) [91,92,93,96] | |
Brain-derived Aβ | n/a | + (micromolar concentrations) [75,76,77,78] | + [75,91,92] | |
Physiological role: plasticity, survival | Synthetic Aβ | ++ (nM) [48,49,53] | ++ (pM) [80,90] | ++ (pM) [80,90] |
Cell-derived Aβ | +/− (endogenous only) [48,49] | nd | nd | |
Brain-derived Aβ | ++ (1 nM) [54] | ++ (pM, endogenous) [89] | ++ (pM, endogenous) [89] |
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Varshavskaya, K.B.; Mitkevich, V.A.; Makarov, A.A.; Barykin, E.P. Synthetic, Cell-Derived, Brain-Derived, and Recombinant β-Amyloid: Modelling Alzheimer’s Disease for Research and Drug Development. Int. J. Mol. Sci. 2022, 23, 15036. https://doi.org/10.3390/ijms232315036
Varshavskaya KB, Mitkevich VA, Makarov AA, Barykin EP. Synthetic, Cell-Derived, Brain-Derived, and Recombinant β-Amyloid: Modelling Alzheimer’s Disease for Research and Drug Development. International Journal of Molecular Sciences. 2022; 23(23):15036. https://doi.org/10.3390/ijms232315036
Chicago/Turabian StyleVarshavskaya, Kseniya B., Vladimir A. Mitkevich, Alexander A. Makarov, and Evgeny P. Barykin. 2022. "Synthetic, Cell-Derived, Brain-Derived, and Recombinant β-Amyloid: Modelling Alzheimer’s Disease for Research and Drug Development" International Journal of Molecular Sciences 23, no. 23: 15036. https://doi.org/10.3390/ijms232315036
APA StyleVarshavskaya, K. B., Mitkevich, V. A., Makarov, A. A., & Barykin, E. P. (2022). Synthetic, Cell-Derived, Brain-Derived, and Recombinant β-Amyloid: Modelling Alzheimer’s Disease for Research and Drug Development. International Journal of Molecular Sciences, 23(23), 15036. https://doi.org/10.3390/ijms232315036