Login Register Cart 0
Generic placeholder image

Current Alzheimer Research

Editor-in-Chief

ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

The Prion-like Properties of Amyloid-beta Peptide and Tau: Is there Any Risk of Transmitting Alzheimer's Disease During Neurosurgical Interventions?

Author(s): Huber S. Padilla-Zambrano, Ezequiel García-Ballestas, Gabriel A. Quiñones-Ossa, Andrés E. Sibaja-Perez, Amit Agrawal, Luis R. Moscote-Salazar and Manuel Menéndez-González*

Volume 17, Issue 9, 2020

Page: [781 - 789] Pages: 9

DOI: 10.2174/1567205017666201204164220

Price: $65

Abstract

Recent studies have recognized similarities between the peptides involved in the neuropathology of Alzheimer’s disease and prions. The Tau protein and the Amyloid β peptide represent the theoretical pillars of Alzheimer’s disease development. It is probable that there is a shared mechanism for the transmission of these substances and the prion diseases development; this presumption is based on the presentation of several cases of individuals without risk factors who developed dementia decades after a neurosurgical procedure.

This article aims to present the role of Aβ and Tau, which underlie the pathophysiologic mechanisms involved in the AD and their similarities with the prion diseases infective mechanisms by means of the presentation of the available evidence at molecular (in-vitro), animal, and human levels that support the controversy on whether these diseases might be transmitted in neurosurgical interventions, which may constitute a wide public health issue.

Keywords: Transmission, prion diseases, amyloid-β, Aβ, neurosurgery, cerebral amyloid angiopathy, tau proteins, Alzheimer disease.

Next »
[1]
Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991; 82(4): 239-59.
[http://dx.doi.org/10.1007/BF00308809] [PMID: 1759558]
[2]
Fenyi A, Coens A, Bellande T, Melki R, Bousset L. Assessment of the efficacy of different procedures that remove and disassemble alpha-synuclein, tau and A-beta fibrils from laboratory material and surfaces. Sci Rep 2018; 8(1): 10788.
[http://dx.doi.org/10.1038/s41598-018-28856-2] [PMID: 30018327]
[3]
Ugalde CL, Finkelstein DI, Lawson VA, Hill AF. Pathogenic mechanisms of prion protein, amyloid-β and α-synuclein misfolding: The prion concept and neurotoxicity of protein oligomers. J Neurochem 2016; 139(2): 162-80.
[http://dx.doi.org/10.1111/jnc.13772] [PMID: 27529376]
[4]
Goedert M. Alzheimer’s and Parkinson’s diseases: The prion concept in relation to assembled Aβ, tau, and α-synuclein. Science 2015; 349: 6248.
[http://dx.doi.org/10.1126/science.1255555]
[5]
Jaunmuktane Z, Mead S, Ellis M, et al. Evidence for human transmission of amyloid-β pathology and cerebral amyloid angiopathy. Nature 2015; 525(7568): 247-50.
[http://dx.doi.org/10.1038/nature15369] [PMID: 26354483]
[6]
Lahiri DK. Prions: A piece of the puzzle? Science 2012; 337(6099): 1172.
[http://dx.doi.org/10.1126/science.337.6099.1172-a] [PMID: 22955815]
[7]
Prusiner SB. Cell biology. A unifying role for prions in neurodegenerative diseases. Science 2012; 336(6088): 1511-3.
[http://dx.doi.org/10.1126/science.1222951] [PMID: 22723400]
[8]
Aoyagi A, Condello C, Stöhr J, et al. Aβ and tau prion-like activities decline with longevity in the Alzheimer’s disease human brain. Sci Transl Med 2019; 11(490)eaat8462
[http://dx.doi.org/10.1126/scitranslmed.aat8462] [PMID: 31043574]
[9]
Selkoe DJ. Resolving controversies on the path to Alzheimer’s therapeutics. Nat Med 2011; 17(9): 1060-5.
[http://dx.doi.org/10.1038/nm.2460] [PMID: 21900936]
[10]
Goedert M, Spillantini MG. A century of Alzheimer’s disease. Science 2006; 314(5800): 777-81.
[http://dx.doi.org/10.1126/science.1132814] [PMID: 17082447]
[11]
Selkoe DJ, Podlisny MB, Joachim CL, et al. Beta-amyloid precursor protein of Alzheimer disease occurs as 110- to 135-kilodalton membrane-associated proteins in neural and nonneural tissues. Proc Natl Acad Sci USA 1988; 85(19): 7341-5.
[http://dx.doi.org/10.1073/pnas.85.19.7341] [PMID: 3140239]
[12]
Prusiner S, Miller B. Prion diseases Harrison’s Principles of Internal Medicine. 19th ed. New York: McGraw-Hill Education 2015.
[13]
Seeley W, Miller B. Alzheimer’s disease and other dementias Harrison’s principles of internal medicine. 19th ed. New York: McGraw-Hill Education 2015.
[14]
Yin YI, Bassit B, Zhu L, Yang X, Wang C, Li Y-M. γ-Secretase substrate concentration modulates the Aβ42/Aβ40 ratio. J Biol Chem 2007; 282(32): 23639-44.
[http://dx.doi.org/10.1074/jbc.M704601200] [PMID: 17556361]
[15]
Wilkins HM, Swerdlow RH. Amyloid precursor protein processing and bioenergetics. Brain Res Bull 2017; 133: 71-9.
[http://dx.doi.org/10.1016/j.brainresbull.2016.08.009] [PMID: 27545490]
[16]
Hartmann T, Bieger SC, Brühl B, et al. Distinct sites of intracellular production for Alzheimer’s disease A β40/42 amyloid peptides. Nat Med 1997; 3(9): 1016-20.
[http://dx.doi.org/10.1038/nm0997-1016] [PMID: 9288729]
[17]
Olsson F, Schmidt S, Althoff V, et al. Characterization of intermediate steps in amyloid beta (Aβ) production under near-native conditions. J Biol Chem 2014; 289(3): 1540-50.
[http://dx.doi.org/10.1074/jbc.M113.498246] [PMID: 24225948]
[18]
Silva-Lucero M, Cortes-Ortiz M, Jimnez-Ramos B, et al. Physiological role of amyloid beta in neural cells: The cellular trophic activity neurochemistry. Rijeka: IntechOpen 2014.
[19]
Vivekanandan S, Brender JR, Lee SY, Ramamoorthy A. A partially folded structure of amyloid-beta (1-40) in an aqueous environment. Biochem Biophys Res Commun 2011; 411(2): 312-6.
[http://dx.doi.org/10.1016/j.bbrc.2011.06.133] [PMID: 21726530]
[20]
Zhang S, Iwata K, Lachenmann MJ, et al. The Alzheimer’s peptide A β adopts a collapsed coil structure in water. J Struct Biol 2000; 130(2-3): 130-41.
[http://dx.doi.org/10.1006/jsbi.2000.4288] [PMID: 10940221]
[21]
Sgourakis NG, Yan Y, McCallum SA, Wang C, Garcia AE. The Alzheimer’s peptides Abeta40 and 42 adopt distinct conformations in water: A combined MD/NMR study. J Mol Biol 2007; 368(5): 1448-57.
[http://dx.doi.org/10.1016/j.jmb.2007.02.093] [PMID: 17397862]
[22]
Yang M, Teplow DB. Amyloid beta-protein monomer folding: Free-energy surfaces reveal alloform-specific differences. J Mol Biol 2008; 384(2): 450-64.
[http://dx.doi.org/10.1016/j.jmb.2008.09.039] [PMID: 18835397]
[23]
Selkoe DJ. Alzheimer’s disease: Genes, proteins, and therapy. Physiol Rev 2001; 81(2): 741-66.
[http://dx.doi.org/10.1152/physrev.2001.81.2.741] [PMID: 11274343]
[24]
Forloni G. beta-Amyloid neurotoxicity. Funct Neurol 1993; 8(3): 211-25.
[PMID: 8406141]
[25]
Clarris HJ, Cappai R, Heffernan D, Beyreuther K, Masters CL, Small DH. Identification of heparin-binding domains in the amyloid precursor protein of Alzheimer’s disease by deletion mutagenesis and peptide mapping. J Neurochem 1997; 68(3): 1164-72.
[http://dx.doi.org/10.1046/j.1471-4159.1997.68031164.x] [PMID: 9048763]
[26]
Maas T, Eidenmüller J, Brandt R. Interaction of tau with the neural membrane cortex is regulated by phosphorylation at sites that are modified in paired helical filaments. J Biol Chem 2000; 275(21): 15733-40.
[http://dx.doi.org/10.1074/jbc.M000389200] [PMID: 10747907]
[27]
Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW. A protein factor essential for microtubule assembly. Proc Natl Acad Sci USA 1975; 72(5): 1858-62.
[http://dx.doi.org/10.1073/pnas.72.5.1858] [PMID: 1057175]
[28]
Avila J, Jiménez JS, Sayas CL, et al. Tau structures. Front Aging Neurosci 2016; 8: 262.
[http://dx.doi.org/10.3389/fnagi.2016.00262] [PMID: 27877124]
[29]
Micheli F, Martín AN, Aconapé JJ, Pardal M, Biller J. Tratado de neurología clínica. Médica Panamericana 2002.
[30]
Goedert M, Spillantini MG, Potier MC, Ulrich J, Crowther RA. Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: Differential expression of tau protein mRNAs in human brain. EMBO J 1989; 8(2): 393-9.
[http://dx.doi.org/10.1002/j.1460-2075.1989.tb03390.x] [PMID: 2498079]
[31]
Buée L, Bussière T, Buée-Scherrer V, Delacourte A, Hof PR. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 2000; 33(1): 95-130.
[http://dx.doi.org/10.1016/S0165-0173(00)00019-9] [PMID: 10967355]
[32]
Hasegawa M. Molecular mechanisms in the pathogenesis of Alzheimer’s disease and tauopathies-prion-like seeded aggregation and phosphorylation. Biomolecules 2016; 6(2): 24.
[33]
Gamblin TC, Berry RW, Binder LI. Modeling tau polymerization in vitro: A review and synthesis. Biochemistry 2003; 42(51): 15009-17.
[http://dx.doi.org/10.1021/bi035722s] [PMID: 14690409]
[34]
Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA. Multiple isoforms of human microtubule-associated protein tau: Sequences and localization in neurofibrillary tangles of Alzheimer’s disease. Neuron 1989; 3(4): 519-26.
[http://dx.doi.org/10.1016/0896-6273(89)90210-9] [PMID: 2484340]
[35]
Couchie D, Mavilia C, Georgieff IS, Liem RK, Shelanski ML, Nunez J. Primary structure of high molecular weight tau present in the peripheral nervous system. Proc Natl Acad Sci USA 1992; 89(10): 4378-81.
[http://dx.doi.org/10.1073/pnas.89.10.4378] [PMID: 1374898]
[36]
Yoshida H, Goedert M. Molecular cloning and functional characterization of chicken brain tau: Isoforms with up to five tandem repeats. Biochemistry 2002; 41(51): 15203-11.
[http://dx.doi.org/10.1021/bi026464m] [PMID: 12484758]
[37]
D’Souza I, Schellenberg GD. Tau Exon 10 expression involves a bipartite intron 10 regulatory sequence and weak 5′ and 3′ splice sites. J Biol Chem 2002; 277(29): 26587-99.
[http://dx.doi.org/10.1074/jbc.M203794200] [PMID: 12000767]
[38]
D’Souza I, Schellenberg GD. Determinants of 4-repeat tau expression. Coordination between enhancing and inhibitory splicing sequences for exon 10 inclusion. J Biol Chem 2000; 275(23): 17700-9.
[http://dx.doi.org/10.1074/jbc.M909470199] [PMID: 10748133]
[39]
Grover A, Houlden H, Baker M, et al. 5′ splice site mutations in tau associated with the inherited dementia FTDP-17 affect a stem-loop structure that regulates alternative splicing of exon 10. J Biol Chem 1999; 274(21): 15134-43.
[http://dx.doi.org/10.1074/jbc.274.21.15134] [PMID: 10329720]
[40]
Heutink P. Untangling tau-related dementia. Hum Mol Genet 2000; 9(6): 979-86.
[http://dx.doi.org/10.1093/hmg/9.6.979] [PMID: 10767321]
[41]
Hernández F, Pérez M, Lucas JJ, Mata AM, Bhat R, Avila J. Glycogen synthase kinase-3 plays a crucial role in tau exon 10 splicing and intranuclear distribution of SC35. Implications for Alzheimer’s disease. J Biol Chem 2004; 279(5): 3801-6.
[http://dx.doi.org/10.1074/jbc.M311512200] [PMID: 14602710]
[42]
Correas I, Díaz-Nido J, Avila J. Microtubule-associated protein tau is phosphorylated by protein kinase C on its tubulin binding domain. J Biol Chem 1992; 267(22): 15721-8.
[PMID: 1639808]
[43]
Arnold CS, Johnson GV, Cole RN, Dong DL, Lee M, Hart GW. The microtubule-associated protein tau is extensively modified with O-linked N-acetylglucosamine. J Biol Chem 1996; 271(46): 28741-4.
[http://dx.doi.org/10.1074/jbc.271.46.28741] [PMID: 8910513]
[44]
Balin BJ, Hudson AP. Etiology and pathogenesis of late-onset Alzheimer’s disease. Curr Allergy Asthma Rep 2014; 14(3): 417.
[http://dx.doi.org/10.1007/s11882-013-0417-1] [PMID: 24429902]
[45]
Bonda DJ, Manjila S, Mehndiratta P, et al. Human prion diseases: Surgical lessons learned from iatrogenic prion transmission. Neurosurg Focus 2016; 41(1)E10
[http://dx.doi.org/10.3171/2016.5.FOCUS15126] [PMID: 27364252]
[46]
O’Brien RJ, Wong PC. Amyloid precursor protein processing and Alzheimer’s disease. Annu Rev Neurosci 2011; 34(1): 185-204.
[http://dx.doi.org/10.1146/annurev-neuro-061010-113613] [PMID: 21456963]
[47]
Pimplikar SW. Reassessing the amyloid cascade hypothesis of Alzheimer’s disease. Int J Biochem Cell Biol 2009; 41(6): 1261-8.
[http://dx.doi.org/10.1016/j.biocel.2008.12.015] [PMID: 19124085]
[48]
Kane MD, Lipinski WJ, Callahan MJ, et al. Evidence for seeding of beta -amyloid by intracerebral infusion of Alzheimer brain extracts in beta -amyloid precursor protein-transgenic mice. J Neurosci 2000; 20(10): 3606-11.
[http://dx.doi.org/10.1523/JNEUROSCI.20-10-03606.2000] [PMID: 10804202]
[49]
Eisele YS, Obermüller U, Heilbronner G, Baumann F. Peripherally applied Aβ-containing inoculates induce cerebral β-amyloidosis Science (80- ) 2011; 330(6006): 980-2.
[50]
Stöhr J, Watts JC, Mensinger ZL, et al. Purified and synthetic Alzheimer’s amyloid beta (Aβ) prions. Proc Natl Acad Sci USA 2012; 109(27): 11025-30.
[http://dx.doi.org/10.1073/pnas.1206555109] [PMID: 22711819]
[51]
Kayed R, Canto I, Breydo L, et al. Conformation dependent monoclonal antibodies distinguish different replicating strains or conformers of prefibrillar Aβ oligomers. Mol Neurodegener 2010; 5(1): 57.
[http://dx.doi.org/10.1186/1750-1326-5-57] [PMID: 21144050]
[52]
Gunther EC, Smith LM, Kostylev MA, et al. Rescue of transgenic Alzheimer’s pathophysiology by polymeric cellular prion protein antagonists. Cell Rep 2019; 26(1): 145-158.e8.
[http://dx.doi.org/10.1016/j.celrep.2018.12.021] [PMID: 30605671]
[53]
Bate C, Williams A. Amyloid-β-induced synapse damage is mediated via cross-linkage of cellular prion proteins. J Biol Chem 2011; 286(44): 37955-63.
[http://dx.doi.org/10.1074/jbc.M111.248724] [PMID: 21900234]
[54]
Liberski PP. Prion, prionoids and infectious amyloid. Parkinsonism Relat Disord 2014; 20(1): S80-4.
[http://dx.doi.org/10.1016/S1353-8020(13)70021-X] [PMID: 24262195]
[55]
Griffiths HH, Whitehouse IJ, Hooper NM. Regulation of amyloid-β production by the prion protein. Prion 2012; 6(3): 217-22.
[http://dx.doi.org/10.4161/pri.18988] [PMID: 22449984]
[56]
Walker LC, Schelle J, Jucker M. The prion-like properties of amyloid-β assemblies: Implications for Alzheimer’s disease. Cold Spring Harb Perspect Med 2016; 6(7)a024398
[http://dx.doi.org/10.1101/cshperspect.a024398] [PMID: 27270558]
[57]
Tatarnikova OG, Orlov MA, Bobkova NV. Beta-Amyloid and tau-protein: Structure, interaction, and prion-like properties. Biochemistry (Mosc) 2015; 80(13): 1800-19.
[http://dx.doi.org/10.1134/S000629791513012X] [PMID: 26878581]
[58]
Mengel D, Hong W, Corbett GT, et al. PrP-grafted antibodies bind certain amyloid β-protein aggregates, but do not prevent toxicity. Brain Res 2019; 1710: 125-35.
[http://dx.doi.org/10.1016/j.brainres.2018.12.038] [PMID: 30593771]
[59]
Braak H, Del Tredici K. Alzheimer’s pathogenesis: Is there neuron-to-neuron propagation? Acta Neuropathol 2011; 121(5): 589-95.
[http://dx.doi.org/10.1007/s00401-011-0825-z] [PMID: 21516512]
[60]
Nussbaum JM, Seward ME, Bloom GS. Alzheimer disease: A tale of two prions. Prion 2013; 7(1): 14-9.
[http://dx.doi.org/10.4161/pri.22118] [PMID: 22965142]
[61]
Frost B, Jacks RL, Diamond MI. Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 2009; 284(19): 12845-52.
[http://dx.doi.org/10.1074/jbc.M808759200] [PMID: 19282288]
[62]
Clavaguera F, Bolmont T, Crowther RA, et al. UKPMC Funders Group Transmission and spreading of tauopathy in transgenic mouse brain. Cell 2010; 11(7): 909-13.
[63]
Lasagna-Reeves CA, Castillo-Carranza DL, Guerrero-Muoz MJ, Jackson GR, Kayed R. Preparation and characterization of neurotoxic tau oligomers. Biochemistry 2010; 49(47): 10039-41.
[http://dx.doi.org/10.1021/bi1016233] [PMID: 21047142]
[64]
Jucker M, Walker LC. Neurodegeneration: Amyloid-β pathology induced in humans. Nature 2015; 525(7568): 193-4.
[http://dx.doi.org/10.1038/525193a] [PMID: 26354478]
[65]
Eisele YS, Bolmont T, Heikenwalder M, et al. Induction of cerebral beta-amyloidosis: Intracerebral versus systemic Abeta inoculation. Proc Natl Acad Sci USA 2009; 106(31): 12926-31.
[http://dx.doi.org/10.1073/pnas.0903200106] [PMID: 19622727]
[66]
Jaunmuktane Z, Quaegebeur A, Taipa R, et al. Evidence of amyloid-β cerebral amyloid angiopathy transmission through neurosurgery. Acta Neuropathol 2018; 135(5): 671-9.
[http://dx.doi.org/10.1007/s00401-018-1822-2] [PMID: 29450646]

Rights & Permissions Print Cite
Article Metrics
11
© 2024 Bentham Science Publishers | Privacy Policy