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Current Neuropharmacology

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ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

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Review Article

Use of Zebrafish Genetic Models to Study Etiology of the Amyloid-Beta and Neurofibrillary Tangle Pathways in Alzheimer's Disease

Author(s): Keturah Kiper and Jennifer L. Freeman*

Volume 20, Issue 3, 2022

Published on: 07 February, 2022

Page: [524 - 539] Pages: 16

DOI: 10.2174/1570159X19666210524155944

Price: $65

Abstract

The prevalence of neurodegenerative diseases is increasing globally, with an imperative need to identify and expand the availability of pharmaceutical treatment strategies. Alzheimer's disease is the most common neurodegenerative disease for which there is no cure and limited treatments. Rodent models are primarily used in Alzheimer's disease research to investigate causes, pathology, molecular mechanisms, and pharmaceutical therapies. However, there is a lack of a comprehensive understanding of Alzheimer's disease causes, pathogenesis, and optimal treatments due in part to some limitations of using rodents, including higher economic cost, which can influence sample size and ultimately statistical power. It is necessary to expand our animal model toolbox to provide alternative strategies in Alzheimer's disease research. The zebrafish application in neurodegenerative disease research and neuropharmacology is greatly expanding due to several vital strengths spanning lower economic costs, the smaller size of the organism, a sequenced characterized genome, and well described anatomical structures. These characteristics are coupled to the conserved molecular function and disease pathways in humans. The existence of orthologs for genes associated with Alzheimer's disease in zebrafish is also confirmed. While wild-type zebrafish appear to lack some of the neuropathological features of Alzheimer's disease, the advent of genetic editing technologies has expanded the evaluation of the amyloid and neurofibrillary tangle hypotheses using the zebrafish and exploration of pharmaceutical molecular targets. An overview of how genetic editing technologies are being used on the zebrafish to create models to investigate the causes, pathology, molecular mechanisms, and pharmaceutical targets of Alzheimer's disease is detailed.

Keywords: Alzheimer's disease, amyloid, brain, drug discovery, genetic models, neurofibrillary, tau, zebrafish.

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[1]
Mohandas, E.; Rajmohan, V.; Raghunath, B. Neurobiology of Alzheimer’s disease. Indian J. Psychiatry, 2009, 51(1), 55-61.
[http://dx.doi.org/10.4103/0019-5545.44908] [PMID: 19742193]
[2]
Raudino, F. Involvement of the spinal cord in the Alzheimer’s disease: A literature review. Arch. Neurosci., 2016, 3(4)
[http://dx.doi.org/10.5812/archneurosci.33834]]
[3]
Dugger, B.N.; Hidalgo, J.A.; Chiarolanza, G.; Mariner, M.; Henry-Watson, J.; Sue, L.I.; Beach, T.G. The distribution of phosphorylated tau in spinal cords of Alzheimer’s disease and non-demented individuals. J. Alzheimers Dis., 2013, 34(2), 529-536.
[http://dx.doi.org/10.3233/JAD-121864] [PMID: 23246918]
[4]
Saito, Y.; Murayama, S. Expression of tau immunoreactivity in the spinal motor neurons of Alzheimer’s disease. Neurology, 2000, 55(11), 1727-1729.
[http://dx.doi.org/10.1212/WNL.55.11.1727] [PMID: 11113231]
[5]
Yeh, T.S.; Ho, Y.C.; Hsu, C.L.; Pan, S.L. Spinal cord injury and Alzheimer’s disease risk: a population-based, retrospective cohort study. Spinal Cord, 2018, 56(2), 151-157.
[http://dx.doi.org/10.1038/s41393-017-0009-3] [PMID: 29057990]
[6]
Lorenzi, R.M.; Palesi, F.; Castellazzi, G.; Vitali, P.; Anzalone, N.; Bernini, S.; Cotta Ramusino, M.; Sinforiani, E.; Micieli, G.; Costa, A.; D’Angelo, E.; Gandini Wheeler-Kingshott, C.A.M. Unsuspected involvement of spinal cord in Alzheimer disease. Front. Cell. Neurosci., 2020, 14, 6.
[http://dx.doi.org/10.3389/fncel.2020.00006] [PMID: 32082122]
[7]
Lee, J.H.; Ryan, J.; Andreescu, C.; Aizenstein, H.; Lim, H.K. Brainstem morphological changes in Alzheimer’s disease. Neuroreport, 2015, 26(7), 411-415.
[http://dx.doi.org/10.1097/WNR.0000000000000362] [PMID: 25830491]
[8]
Grinberg, L.T.; Rueb, U.; Heinsen, H. Brainstem: neglected locus in neurodegenerative diseases. Front. Neurol., 2011, 2, 42.
[http://dx.doi.org/10.3389/fneur.2011.00042] [PMID: 21808630]
[9]
Vajn, K.; Plunkett, J.A.; Tapanes-Castillo, A.; Oudega, M. Axonal regeneration after spinal cord injury in zebrafish and mammals: differences, similarities, translation. Neurosci. Bull., 2013, 29(4), 402-410.
[http://dx.doi.org/10.1007/s12264-013-1361-8] [PMID: 23893428]
[10]
Fakhoury, M. Microglia and astrocytes in Alzheimer’s disease: implications for therapy. Curr. Neuropharmacol., 2018, 16(5), 508-518.
[http://dx.doi.org/10.2174/1570159X15666170720095240] [PMID: 28730967]
[11]
Frost, G.R.; Li, Y.M. The role of astrocytes in amyloid production and Alzheimer’s disease. Open Biol., 2017, 7(12)170228
[http://dx.doi.org/10.1098/rsob.170228] [PMID: 29237809]
[12]
Hansen, D.V.; Hanson, J.E.; Sheng, M. Microglia in Alzheimer’s Disease. J. Cell Biol; Rockefeller University Press, 2018, pp. 459-472.
[http://dx.doi.org/10.1083/jcb.201709069]
[13]
Raikwar, S. P.; Bhagavan, S. M.; Beladakere Ramaswamy, S.; Thangavel, R.; Dubova, I.; Pushpavathi Selvakumar, G.; Ejaz Ahmed, M.; Kempuraj, D.; Iyer, S.; Zaheer, S.; Zaheer, A. Are Tanycytes the Missing Link between Type 2 Diabetes and Alzheimer’s Disease?
[http://dx.doi.org/10.1007/s12035-018-1123-8]
[14]
Babin, P.J.; Thisse, C.; Durliat, M.; Andre, M.; Akimenko, M.A.; Thisse, B. Both apolipoprotein E and A-I genes are present in a nonmammalian vertebrate and are highly expressed during embryonic development. Proc. Natl. Acad. Sci. USA, 1997, 94(16), 8622-8627.
[http://dx.doi.org/10.1073/pnas.94.16.8622] [PMID: 9238027]
[15]
Nicholls, D.G.; Budd, S.L. Mitochondria and Neuronal Survival. Physiological Reviews; American Physiological Society, 2000, pp. 315-360.
[http://dx.doi.org/10.1152/physrev.2000.80.1.315]
[16]
Carrano, A.; Hoozemans, J.J.M.; van der Vies, S.M.; Rozemuller, A.J.M.; van Horssen, J.; de Vries, H.E. Amyloid Beta induces oxidative stress-mediated blood-brain barrier changes in capillary amyloid angiopathy. Antioxid. Redox Signal., 2011, 15(5), 1167-1178.
[http://dx.doi.org/10.1089/ars.2011.3895] [PMID: 21294650]
[17]
Erickson, M.A.; Banks, W.A. Blood-brain barrier dysfunction as a cause and consequence of Alzheimer’s disease. J. Cerebral Blood Flow Metabolism; SAGE Publications, 2013, pp. 1500-1513.
[http://dx.doi.org/10.1038/jcbfm.2013.135]
[18]
Roher, A.E.; Kuo, Y.M.; Esh, C.; Knebel, C.; Weiss, N.; Kalback, W.; Luehrs, D.C.; Childress, J.L.; Beach, T.G.; Weller, R.O.; Kokjohn, T.A. Cortical and leptomeningeal cerebrovascular amyloid and white matter pathology in Alzheimer’s disease. Mol. Med., 2003, 9(3-4), 112-122.
[http://dx.doi.org/10.1007/BF03402043] [PMID: 12865947]
[19]
Zenaro, E.; Piacentino, G.; Constantin, G. The Blood-Brain Barrier in Alzheimer’s Disease. Neurobiology of Disease; Academic Press Inc., 2017, pp. 41-56.
[http://dx.doi.org/10.1016/j.nbd.2016.07.007]
[20]
Jeong, J-Y.; Kwon, H-B.; Ahn, J-C.; Kang, D.; Kwon, S-H.; Park, J.A.; Kim, K-W. Functional and developmental analysis of the blood-brain barrier in zebrafish. Brain Res. Bull., 2008, 75(5), 619-628.
[http://dx.doi.org/10.1016/j.brainresbull.2007.10.043] [PMID: 18355638]
[21]
Verdile, G.; Fuller, S.; Atwood, C.S.; Laws, S.M.; Gandy, S.E.; Martins, R.N. The role of beta amyloid in Alzheimer’s disease: still a cause of everything or the only one who got caught? Pharmacol. Res., 2004, 50(4), 397-409.
[http://dx.doi.org/10.1016/j.phrs.2003.12.028] [PMID: 15304237]
[22]
Hardy, J.; Selkoe, D. J. ?The amyloid hypothesis of Alzheimer’s disease: Progress and problems on the road to therapeutics. Science (80-. ) 2002, 297(19), 353-356.
[23]
Newman, M.; Verdile, G.; Martins, R.N.; Lardelli, M. Zebrafish as a tool in Alzheimer’s disease research. Biochim. Biophys. Acta, 2011, 1812(3), 346-352.
[http://dx.doi.org/10.1016/j.bbadis.2010.09.012] [PMID: 20920580]
[24]
Maccioni, R.B.; Farías, G.; Morales, I.; Navarrete, L. The revitalized tau hypothesis on Alzheimer’s disease. Arch. Med. Res., 2010, 41(3), 226-231.
[http://dx.doi.org/10.1016/j.arcmed.2010.03.007] [PMID: 20682182]
[25]
Cameron, D.J.; Galvin, C.; Alkam, T.; Sidhu, H.; Ellison, J.; Luna, S.; Ethell, D.W. Alzheimer’s-related peptide amyloid-β plays a conserved role in angiogenesis. PLoS One, 2012, 7(7)e39598
[http://dx.doi.org/10.1371/journal.pone.0039598] [PMID: 22792182]
[26]
Sundvik, M.; Chen, Y.C.; Panula, P. Presenilin1 regulates histamine neuron development and behavior in zebrafish, Danio rerio. J. Neurosci., 2013, 33(4), 1589-1597.
[http://dx.doi.org/10.1523/JNEUROSCI.1802-12.2013] [PMID: 23345232]
[27]
Butt, A.M.; De La Rocha, I.C.; Rivera, A. Oligodendroglial Cells in Alzheimer’s Disease.Advances in Experimental Medicine and Biology. Springer New York LLC, 2019, Vol. 1175, 325-333.
[http://dx.doi.org/10.1007/978-981-13-9913-8_12]
[28]
Preston, M.A.; Macklin, W.B. Zebrafish as a Model to Investigate CNS Myelination.GLIA; John Wiley and Sons Inc., 2015, pp. 177-193.
[http://dx.doi.org/10.1002/glia.22755]
[29]
Brösamle, C.; Halpern, M.E. Characterization of myelination in the developing zebrafish. Glia, 2002, 39(1), 47-57.
[http://dx.doi.org/10.1002/glia.10088] [PMID: 12112375]
[30]
Groth, C.; Nornes, S.; McCarty, R.; Tamme, R.; Lardelli, M. Identification of a second presenilin gene in zebrafish with similarity to the human Alzheimer’s disease gene presenilin2. Dev. Genes Evol., 2002, 212(10), 486-490.
[http://dx.doi.org/10.1007/s00427-002-0269-5] [PMID: 12424519]
[31]
Shen, J.; Bronson, R.T.; Chen, D.F.; Xia, W.; Selkoe, D.J.; Tonegawa, S. Skeletal and CNS defects in Presenilin-1-deficient mice. Cell, 1997, 89(4), 629-639.
[http://dx.doi.org/10.1016/S0092-8674(00)80244-5] [PMID: 9160754]
[32]
Wong, P.C.; Zheng, H.; Chen, H.; Becher, M.W.; Sirinathsinghji, D.J.S.; Trumbauer, M.E.; Chen, H.Y.; Price, D.L.; Van der Ploeg, L.H.T.; Sisodia, S.S. Presenilin 1 is required for Notch1 and DII1 expression in the paraxial mesoderm. Nature, 1997, 387(6630), 288-292.
[http://dx.doi.org/10.1038/387288a0] [PMID: 9153393]
[33]
Nornes, S.; Newman, M.; Wells, S.; Verdile, G.; Martins, R.N.; Lardelli, M. Independent and cooperative action of Psen2 with Psen1 in zebrafish embryos. Exp. Cell Res., 2009, 315(16), 2791-2801.
[http://dx.doi.org/10.1016/j.yexcr.2009.06.023] [PMID: 19563801]
[34]
Herreman, A.; Hartmann, D.; Annaert, W.; Saftig, P.; Craessaerts, K.; Serneels, L.; Umans, L.; Schrijvers, V.; Checler, F.; Vanderstichele, H.; Baekelandt, V.; Dressel, R.; Cupers, P.; Huylebroeck, D.; Zwijsen, A.; Van Leuven, F.; De Strooper, B. Presenilin 2 deficiency causes a mild pulmonary phenotype and no changes in amyloid precursor protein processing but enhances the embryonic lethal phenotype of presenilin 1 deficiency. Proc. Natl. Acad. Sci. USA, 1999, 96(21), 11872-11877.
[http://dx.doi.org/10.1073/pnas.96.21.11872] [PMID: 10518543]
[35]
Xie, Q.; Zhao, W.J.; Ou, G.Y.; Xue, W.K. An overview of experimental and clinical spinal cord findings in Alzheimer’s disease. Brain Sci., 2019, 9(7)E168
[http://dx.doi.org/10.3390/brainsci9070168] [PMID: 31319495]
[36]
Musa, A.; Lehrach, H.; Russo, V.A. Distinct expression patterns of two zebrafish homologues of the human APP gene during embryonic development. Dev. Genes Evol., 2001, 211(11), 563-567.
[http://dx.doi.org/10.1007/s00427-001-0189-9] [PMID: 11862463]
[37]
Lee, J-A.; Cole, G.J. Generation of transgenic zebrafish expressing green fluorescent protein under control of zebrafish amyloid precursor protein gene regulatory elements. Zebrafish, 2007, 4(4), 277-286.
[http://dx.doi.org/10.1089/zeb.2007.0516] [PMID: 18284334]
[38]
Liao, H-K.; Wang, Y.; Noack Watt, K.E.; Wen, Q.; Breitbach, J.; Kemmet, C.K.; Clark, K.J.; Ekker, S.C.; Essner, J.J.; McGrail, M. Tol2 gene trap integrations in the zebrafish amyloid precursor protein genes appa and aplp2 reveal accumulation of secreted APP at the embryonic veins. Dev. Dyn., 2012, 241(2), 415-425.
[http://dx.doi.org/10.1002/dvdy.23725] [PMID: 22275008]
[39]
Joshi, P.; Liang, J.O.; DiMonte, K.; Sullivan, J.; Pimplikar, S.W. Amyloid precursor protein is required for convergent-extension movements during Zebrafish development. Dev. Biol., 2009, 335(1), 1-11.
[http://dx.doi.org/10.1016/j.ydbio.2009.07.041] [PMID: 19664615]
[40]
Luna, S.; Cameron, D.J.; Ethell, D.W. Amyloid-β and APP deficiencies cause severe cerebrovascular defects: important work for an old villain. PLoS One, 2013, 8(9)e75052
[http://dx.doi.org/10.1371/journal.pone.0075052] [PMID: 24040383]
[41]
Cunvong, K.; Huffmire, D.; Ethell, D.W.; Cameron, D.J. Amyloid-β increases capillary bed density in the adult zebrafish retina. Invest. Ophthalmol. Vis. Sci., 2013, 54(2), 1516-1521.
[http://dx.doi.org/10.1167/iovs.12-10821] [PMID: 23404118]
[42]
Moussavi Nik, S.H.; Wilson, L.; Newman, M.; Croft, K.; Mori, T.A.; Musgrave, I.; Lardelli, M. The BACE1-PSEN-AβPP regulatory axis has an ancient role in response to low oxygen/oxidative stress. J. Alzheimers Dis., 2012, 28(3), 515-530.
[http://dx.doi.org/10.3233/JAD-2011-110533] [PMID: 22045484]
[43]
van Bebber, F.; Hruscha, A.; Willem, M.; Schmid, B.; Haass, C. Loss of Bace2 in zebrafish affects melanocyte migration and is distinct from Bace1 knock out phenotypes. J. Neurochem., 2013, 127(4), 471-481.
[http://dx.doi.org/10.1111/jnc.12198] [PMID: 23406323]
[44]
Francis, R.; McGrath, G.; Zhang, J.; Ruddy, D.A.; Sym, M.; Apfeld, J.; Nicoll, M.; Maxwell, M.; Hai, B.; Ellis, M.C.; Parks, A.L.; Xu, W.; Li, J.; Gurney, M.; Myers, R.L.; Himes, C.S.; Hiebsch, R.; Ruble, C.; Nye, J.S.; Curtis, D. aph-1 and pen-2 are required for Notch pathway signaling, γ-secretase cleavage of betaAPP, and presenilin protein accumulation. Dev. Cell, 2002, 3(1), 85-97.
[http://dx.doi.org/10.1016/S1534-5807(02)00189-2] [PMID: 12110170]
[45]
Campbell, W.A.; Yang, H.; Zetterberg, H.; Baulac, S.; Sears, J.A.; Liu, T.; Wong, S.T.C.; Zhong, T.P.; Xia, W. Zebrafish lacking Alzheimer presenilin enhancer 2 (Pen-2) demonstrate excessive p53-dependent apoptosis and neuronal loss. J. Neurochem., 2006, 96(5), 1423-1440.
[http://dx.doi.org/10.1111/j.1471-4159.2006.03648.x] [PMID: 16464238]
[46]
Lim, A.; Moussavi Nik, S.H.; Ebrahimie, E.; Lardelli, M. Analysis of nicastrin gene phylogeny and expression in zebrafish. Dev. Genes Evol., 2015, 225(3), 171-178.
[http://dx.doi.org/10.1007/s00427-015-0500-9] [PMID: 25940938]
[47]
Leimer, U.; Lun, K.; Romig, H.; Walter, J.; Grünberg, J.; Brand, M.; Haass, C. Zebrafish (Danio rerio) presenilin promotes aberrant amyloid β-peptide production and requires a critical aspartate residue for its function in amyloidogenesis. Biochemistry, 1999, 38(41), 13602-13609.
[http://dx.doi.org/10.1021/bi991453n] [PMID: 10521267]
[48]
Durliat, M.; André, M.; Babin, P.J. Conserved protein motifs and structural organization of a fish gene homologous to mammalian apolipoprotein E. Eur. J. Biochem., 2000, 267(2), 549-559.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01033.x] [PMID: 10632725]
[49]
Lee, J.; Peterson, S.M.; Freeman, J.L. Alzheimer’s disease risk genes in wild-type adult zebrafish exhibit gender-specific expression changes during aging. Neurogenetics, 2016, 17(3), 197-199.
[http://dx.doi.org/10.1007/s10048-016-0485-1] [PMID: 27234028]
[50]
Lee, J.; Peterson, S.M.; Freeman, J.L. Sex-specific characterization and evaluation of the Alzheimer’s disease genetic risk factor sorl1 in zebrafish during aging and in the adult brain following a 100 ppb embryonic lead exposure. J. Appl. Toxicol., 2017, 37(4), 400-407.
[http://dx.doi.org/10.1002/jat.3372] [PMID: 27535807]
[51]
Coburn, C.A.; Stachel, S.J.; Li, Y.M.; Rush, D.M.; Steele, T.G.; Chen-Dodson, E.; Holloway, M.K.; Xu, M.; Huang, Q.; Lai, M.T.; DiMuzio, J.; Crouthamel, M.C.; Shi, X.P.; Sardana, V.; Chen, Z.; Munshi, S.; Kuo, L.; Makara, G.M.; Annis, D.A.; Tadikonda, P.K.; Nash, H.M.; Vacca, J.P.; Wang, T. Identification of a small molecule nonpeptide active site β-secretase inhibitor that displays a nontraditional binding mode for aspartyl proteases. J. Med. Chem., 2004, 47(25), 6117-6119.
[http://dx.doi.org/10.1021/jm049388p] [PMID: 15566281]
[52]
Dockens, R.; Wang, J-S.; Castaneda, L.; Sverdlov, O.; Huang, S-P.; Slemmon, R.; Gu, H.; Wong, O.; Li, H.; Berman, R.M.; Smith, C.; Albright, C.F.; Tong, G. A placebo-controlled, multiple ascending dose study to evaluate the safety, pharmacokinetics and pharmacodynamics of avagacestat (BMS-708163) in healthy young and elderly subjects. Clin. Pharmacokinet., 2012, 51(10), 681-693.
[http://dx.doi.org/10.1007/s40262-012-0005-x] [PMID: 23018531]
[53]
Siemers, E.R.; Quinn, J.F.; Kaye, J.; Farlow, M.R.; Porsteinsson, A.; Tariot, P.; Zoulnouni, P.; Galvin, J.E.; Holtzman, D.M.; Knopman, D.S.; Satterwhite, J.; Gonzales, C.; Dean, R.A.; May, P.C. Effects of a γ-secretase inhibitor in a randomized study of patients with Alzheimer disease. Neurology, 2006, 66(4), 602-604.
[http://dx.doi.org/10.1212/01.WNL.0000198762.41312.E1] [PMID: 16505324]
[54]
McGowan, E.; Pickford, F.; Kim, J.; Onstead, L.; Eriksen, J.; Yu, C.; Skipper, L.; Murphy, M.P.; Beard, J.; Das, P.; Jansen, K.; DeLucia, M.; Lin, W.L.; Dolios, G.; Wang, R.; Eckman, C.B.; Dickson, D.W.; Hutton, M.; Hardy, J.; Golde, T. Abeta42 is essential for parenchymal and vascular amyloid deposition in mice. Neuron, 2005, 47(2), 191-199.
[http://dx.doi.org/10.1016/j.neuron.2005.06.030] [PMID: 16039562]
[55]
Haas, H.; Panula, P. The role of histamine and the tuberomamillary nucleus in the nervous system. Nat. Rev. Neurosci., 2003, 4(2), 121-130.
[http://dx.doi.org/10.1038/nrn1034] [PMID: 12563283]
[56]
Sundvik, M.; Panula, P. Organization of the histaminergic system in adult zebrafish (Danio rerio) brain: neuron number, location, and cotransmitters. J. Comp. Neurol., 2012, 520(17), 3827-3845.
[http://dx.doi.org/10.1002/cne.23126] [PMID: 22522821]
[57]
Suster, M.L.; Abe, G.; Schouw, A.; Kawakami, K. Transposon-mediated BAC transgenesis in zebrafish. Nat. Protoc., 2011, 6(12), 1998-2021.
[http://dx.doi.org/10.1038/nprot.2011.416] [PMID: 22134125]
[58]
Bedell, V.M.; Ekker, S.C. Using engineered endonucleases to create knockout and knockin Zebrafi Sh models.Methods in Molecular Biology; Pruett-Miller, S.M., Ed.;; , 2015, Vol. 1239, pp. 291-305.
[http://dx.doi.org/10.1007/978-1-4939-1862-1_17]
[59]
Irion, U.; Krauss, J.; Nüsslein-Volhard, C. Precise and efficient genome editing in zebrafish using the CRISPR/Cas9 system. Development, 2014, 141(24), 4827-4830.
[http://dx.doi.org/10.1242/dev.115584] [PMID: 25411213]
[60]
Saleem, S.; Kannan, R.R. Zebrafish: an emerging real-time model system to study Alzheimer’s disease and neurospecific drug discovery. Cell Death Discov., 2018, 4(45), 45.
[http://dx.doi.org/10.1038/s41420-018-0109-7] [PMID: 30302279]
[61]
Ring, S.; Weyer, S.W.; Kilian, S.B.; Waldron, E.; Pietrzik, C.U.; Filippov, M.A.; Herms, J.; Buchholz, C.; Eckman, C.B.; Korte, M.; Wolfer, D.P.; Müller, U.C. The secreted β-amyloid precursor protein ectodomain APPs α is sufficient to rescue the anatomical, behavioral, and electrophysiological abnormalities of APP-deficient mice. J. Neurosci., 2007, 27(29), 7817-7826.
[http://dx.doi.org/10.1523/JNEUROSCI.1026-07.2007] [PMID: 17634375]
[62]
Banote, R.K.; Chebli, J.; Şatır, T.M.; Varshney, G.K.; Camacho, R.; Ledin, J.; Burgess, S.M.; Abramsson, A.; Zetterberg, H. Amyloid precursor protein-b facilitates cell adhesion during early development in zebrafish. Sci. Rep., 2020, 10(1), 10127.
[http://dx.doi.org/10.1038/s41598-020-66584-8] [PMID: 32576936]
[63]
Pu, Y-Z.; Liang, L.; Fu, A-L.; Liu, Y.; Sun, L.; Li, Q.; Wu, D.; Sun, M-J.; Zhang, Y-G.; Zhao, B-Q. Generation of Alzheimer’s disease transgenic zebrafish expressing human APP mutation under control of zebrafish appb promotor. Curr. Alzheimer Res., 2017, 14(6), 668-679.
[http://dx.doi.org/10.2174/1567205013666161201202000] [PMID: 27978793]
[64]
Meyer, E.P.; Ulmann-Schuler, A.; Staufenbiel, M.; Krucker, T. Altered morphology and 3D architecture of brain vasculature in a mouse model for Alzheimer’s disease. Proc. Natl. Acad. Sci. USA, 2008, 105(9), 3587-3592.
[http://dx.doi.org/10.1073/pnas.0709788105] [PMID: 18305170]
[65]
Soontornniyomkij, V.; Lynch, M.D.; Mermash, S.; Pomakian, J.; Badkoobehi, H.; Clare, R.; Vinters, H.V. Cerebral microinfarcts associated with severe cerebral β-amyloid angiopathy. Brain Pathol., 2010, 20(2), 459-467.
[http://dx.doi.org/10.1111/j.1750-3639.2009.00322.x] [PMID: 19725828]
[66]
Barthelson, K.; Pederson, S.M.; Newman, M.; Lardelli, M. Brain transcriptome analysis reveals subtle effects on mitochondrial function and iron homeostasis of mutations in the SORL1 gene implicated in early onset familial Alzheimer’s disease. Mol. Brain, 2020, 13(1), 142.
[http://dx.doi.org/10.1186/s13041-020-00681-7] [PMID: 33076949]
[67]
Tomasiewicz, H.G.; Flaherty, D.B.; Soria, J.P.; Wood, J.G. Transgenic zebrafish model of neurodegeneration. J. Neurosci. Res., 2002, 70(6), 734-745.
[http://dx.doi.org/10.1002/jnr.10451] [PMID: 12444595]
[68]
Wu, B.K.; Yuan, R.Y.; Lien, H.W.; Hung, C.C.; Hwang, P.P.; Chen, R.P.Y.; Chang, C.C.; Liao, Y.F.; Huang, C.J. Multiple signaling factors and drugs alleviate neuronal death induced by expression of human and zebrafish tau proteins in vivo. J. Biomed. Sci., 2016, 23(1), 25.
[http://dx.doi.org/10.1186/s12929-016-0237-4] [PMID: 26852117]
[69]
Bai, Q.; Garver, J.A.; Hukriede, N.A.; Burton, E.A. Generation of a transgenic zebrafish model of Tauopathy using a novel promoter element derived from the zebrafish eno2 gene. Nucleic Acids Res., 2007, 35(19), 6501-6516.
[http://dx.doi.org/10.1093/nar/gkm608] [PMID: 17897967]
[70]
Paquet, D.; Bhat, R.; Sydow, A.; Mandelkow, E.M.; Berg, S.; Hellberg, S.; Fälting, J.; Distel, M.; Köster, R.W.; Schmid, B.; Haass, C. A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation. J. Clin. Invest., 2009, 119(5), 1382-1395.
[http://dx.doi.org/10.1172/JCI37537] [PMID: 19363289]
[71]
Cosacak, M.I.; Bhattarai, P.; Bocova, L.; Dzewas, T.; Mashkaryan, V.; Papadimitriou, C.; Brandt, K.; Hollak, H.; Antos, C.L.; Kizil, C. Human TAUP301L overexpression results in TAU hyperphosphorylation without neurofibrillary tangles in adult zebrafish brain. Sci. Rep., 2017, 7(1), 12959.
[http://dx.doi.org/10.1038/s41598-017-13311-5] [PMID: 29021554]
[72]
De Strooper, B.; Saftig, P.; Craessaerts, K.; Vanderstichele, H.; Guhde, G.; Annaert, W.; Von Figura, K.; Van Leuven, F. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature, 1998, 391(6665), 387-390.
[http://dx.doi.org/10.1038/34910] [PMID: 9450754]
[73]
De Strooper, B.; Iwatsubo, T.; Wolfe, M.S. Presenilins and γ-secretase: structure, function, and role in Alzheimer Disease. Cold Spring Harb. Perspect. Med., 2012, 2(1)a006304
[http://dx.doi.org/10.1101/cshperspect.a006304] [PMID: 22315713]
[74]
Takashima, A.; Murayama, M.; Murayama, O.; Kohno, T.; Honda, T.; Yasutake, K.; Nihonmatsu, N.; Mercken, M.; Yamaguchi, H.; Sugihara, S.; Wolozin, B. Presenilin 1 associates with glycogen synthase kinase-3β and its substrate tau. Proc. Natl. Acad. Sci. USA, 1998, 95(16), 9637-9641.
[http://dx.doi.org/10.1073/pnas.95.16.9637] [PMID: 9689133]
[75]
Nornes, S.; Groth, C.; Camp, E.; Ey, P.; Lardelli, M. Developmental control of Presenilin1 expression, endoproteolysis, and interaction in zebrafish embryos. Exp. Cell Res., 2003, 289(1), 124-132.
[http://dx.doi.org/10.1016/S0014-4827(03)00257-X] [PMID: 12941610]
[76]
“PSEN-1 | ALZFORUM.” Available from: . https://www.alzforum. org/mutations/psen-1(accessed Jan. 22, 2021).
[77]
Ochalek, A.; Mihalik, B.; Avci, H.X.; Chandrasekaran, A.; Téglási, A.; Bock, I.; Giudice, M.L.; Táncos, Z.; Molnár, K.; László, L.; Nielsen, J.E.; Holst, B.; Freude, K.; Hyttel, P.; Kobolák, J.; Dinnyés, A. Neurons derived from sporadic Alzheimer’s disease iPSCs reveal elevated TAU hyperphosphorylation, increased amyloid levels, and GSK3B activation. Alzheimers Res. Ther., 2017, 9(1), 90.
[http://dx.doi.org/10.1186/s13195-017-0317-z] [PMID: 29191219]
[78]
Hin, N.; Newman, M.; Kaslin, J.; Douek, A.M.; Lumsden, A.; Zhou, X-F.; Ludington, A.; Adelson, D.L.; Pederson, S.; Lardelli, M. Accelerated Brain Aging towards Transcriptional Inversion in a Zebrafish Model of Familial Alzheimer’s Disease. PLoS One,
[http://dx.doi.org/10.1101/262162]]
[79]
Pigino, G.; Pelsman, A.; Mori, H.; Busciglio, J. Presenilin-1 mutations reduce cytoskeletal association, deregulate neurite growth, and potentiate neuronal dystrophy and tau phosphorylation. J. Neurosci., 2001, 21(3), 834-842.
[http://dx.doi.org/10.1523/JNEUROSCI.21-03-00834.2001] [PMID: 11157069]
[80]
Zon, L.I.; Peterson, R.T. In vivo drug discovery in the zebrafish. Nat. Rev. Drug Discov., 2005, 4(1), 35-44.
[http://dx.doi.org/10.1038/nrd1606] [PMID: 15688071]
[81]
"FDA-approved treatments for Alzheimer's," Aug. 2019. Accessed: Jan. 22, 2021. Available from: . https://www.alz.org/media/documents/fda-approved-treatments-alzheimers-ts.pdf
[82]
Weller, J.; Budson, A. Current Understanding of Alzheimer’s Disease Diagnosis and Treatment.F1000Research; F1000 Research Ltd, 2018.
[http://dx.doi.org/10.12688/f1000research.14506.1]
[83]
Elmaleh, D. R. Combination Therapies for the Treatment of Alzheimer’s Disease and Related Disorders - Google Patents. 412 WO2014066318A1,. 2021.
[84]
Kocis, P.; Tolar, M.; Yu, J.; Sinko, W.; Ray, S.; Blennow, K.; Fillit, H.; Hey, J.A. Elucidating the Aβ42 Anti-Aggregation Mechanism of Action of Tramiprosate in Alzheimer’s Disease: Integrating Molecular Analytical Methods, Pharmacokinetic and Clinical Data. CNS Drugs, 2017, 31(6), 495-509.
[http://dx.doi.org/10.1007/s40263-017-0434-z] [PMID: 28435985]
[85]
Hey, J.A.; Yu, J.Y.; Versavel, M.; Abushakra, S.; Kocis, P.; Power, A.; Kaplan, P.L.; Amedio, J.; Tolar, M. Clinical pharmacokinetics and safety of ALZ-801, a novel prodrug of tramiprosate in development for the treatment of Alzheimer’s disease. Clin. Pharmacokinet., 2018, 57(3), 315-333.
[http://dx.doi.org/10.1007/s40262-017-0608-3] [PMID: 29063518]
[86]
Cirrito, J. R.; Wallace, C. E.; Yan, P.; Davis, T. A.; Gardiner, W. D.; Doherty, B. M.; King, D.; Yuede, C. M.; Lee, J.-M.; Sheline, Y. I. Effect of Escitalopram on Aβ Levels and Plaque Load in an Alzheimer Mouse Model., 2020.
[http://dx.doi.org/10.1212/WNL.0000000000010733]
[87]
Buttini, M.; Masliah, E.; Barbour, R.; Grajeda, H.; Motter, R.; Johnson-Wood, K.; Khan, K.; Seubert, P.; Freedman, S.; Schenk, D.; Games, D. β-amyloid immunotherapy prevents synaptic degeneration in a mouse model of Alzheimer’s disease. J. Neurosci., 2005, 25(40), 9096-9101.
[http://dx.doi.org/10.1523/JNEUROSCI.1697-05.2005] [PMID: 16207868]
[88]
Bard, F.; Cannon, C.; Barbour, R.; Burke, R.L.; Games, D.; Grajeda, H.; Guido, T.; Hu, K.; Huang, J.; Johnson-Wood, K.; Khan, K.; Kholodenko, D.; Lee, M.; Lieberburg, I.; Motter, R.; Nguyen, M.; Soriano, F.; Vasquez, N.; Weiss, K.; Welch, B.; Seubert, P.; Schenk, D.; Yednock, T. Peripherally administered antibodies against amyloid β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med., 2000, 6(8), 916-919.
[http://dx.doi.org/10.1038/78682] [PMID: 10932230]
[89]
Farlow, M.R.; Andreasen, N.; Riviere, M.E.; Vostiar, I.; Vitaliti, A.; Sovago, J.; Caputo, A.; Winblad, B.; Graf, A. Long-term treatment with active Aβ immunotherapy with CAD106 in mild Alzheimer’s disease. Alzheimers Res. Ther., 2015, 7(1), 23.
[http://dx.doi.org/10.1186/s13195-015-0108-3] [PMID: 25918556]
[90]
Winblad, B.; Andreasen, N.; Minthon, L.; Floesser, A.; Imbert, G.; Dumortier, T.; Maguire, R.P.; Blennow, K.; Lundmark, J.; Staufenbiel, M.; Orgogozo, J.M.; Graf, A. Safety, tolerability, and antibody response of active Aβ immunotherapy with CAD106 in patients with Alzheimer’s disease: randomised, double-blind, placebo-controlled, first-in-human study. Lancet Neurol., 2012, 11(7), 597-604.
[http://dx.doi.org/10.1016/S1474-4422(12)70140-0] [PMID: 22677258]
[91]
] Novartis Pharmaceuticals. A Randomized, Double-blind, Placebocontrolled, Two-cohort, Parallel Group Study to Evaluate the Efficacy of CAD106 and CNP520 in Participants at Risk for the Onset 464 of Clinical Symptoms of Alzheimer’s Disease. Available from:. https://clinicaltrials.gov/ct2/show/NCT02565511(accessed Jan 25, 2021)
[92]
Donanemab ALZFORUM." Available from:. https://www. alzforum.org/therapeuticsdonanemab(accessed Jan. 25, 2021)/
[93]
.“UB-311 | ALZFORUM.” Available from: https://www. alzforum. org/therapeutics/ub-311(accessed Jan. 25, 2021)
[94]
Lacosta, A.M.; Pascual-Lucas, M.; Pesini, P.; Casabona, D.; Pérez-Grijalba, V.; Marcos-Campos, I.; Sarasa, L.; Canudas, J.; Badi, H.; Monleón, I.; San-José, I.; Munuera, J.; Rodríguez-Gómez, O.; Abdelnour, C.; Lafuente, A.; Buendía, M.; Boada, M.; Tárraga, L.; Ruiz, A.; Sarasa, M. Safety, tolerability and immunogenicity of an active anti-Aβ40 vaccine (ABvac40) in patients with Alzheimer’s disease: a randomised, double-blind, placebo-controlled, phase I trial. Alzheimers Res. Ther., 2018, 10(1), 12.
[http://dx.doi.org/10.1186/s13195-018-0340-8] [PMID: 29378651]
[95]
Fabre, C.; Gobbi, M.; Ezzili, C.; Zoubir, M.; Sablin, M.P.; Small, K. Im, E.; Shinwari, N.; Zhang, D.; Zhou, H.; Le Tourneau, C. Clinical Study of the Novel Cyclin-Dependent Kinase Inhibitor Dinaciclib in Combination with Rituximab in Relapsed/Refractory Chronic Lymphocytic Leukemia Patients. Cancer Chemother. Pharmacol., 2014, 74(5), 1057-1064.
[http://dx.doi.org/10.1007/s00280-014-2583-9] [PMID: 25217392]
[96]
Kumar, S.K.; LaPlant, B.; Chng, W.J.; Zonder, J.; Callander, N.; Fonseca, R.; Fruth, B.; Roy, V.; Erlichman, C.; Stewart, A.K. Dinaciclib, a novel CDK inhibitor, demonstrates encouraging single-agent activity in patients with relapsed multiple myeloma. Blood, 2015, 125(3), 443-448.
[http://dx.doi.org/10.1182/blood-2014-05-573741] [PMID: 25395429]
[97]
Novak, P.; Schmidt, R.; Kontsekova, E.; Kovacech, B.; Smolek, T.; Katina, S.; Fialova, L.; Prcina, M.; Parrak, V.; Dal-Bianco, P.; Brunner, M.; Staffen, W.; Rainer, M.; Ondrus, M.; Ropele, S.; Smisek, M.; Sivak, R.; Zilka, N.; Winblad, B.; Novak, M. FUNDAMANT: an interventional 72-week phase 1 follow-up study of AADvac1, an active immunotherapy against tau protein pathology in Alzheimer’s disease. Alzheimers Res. Ther., 2018, 10(1), 108.
[http://dx.doi.org/10.1186/s13195-018-0436-1] [PMID: 30355322]
[98]
Theunis, C.; Crespo-Biel, N.; Gafner, V.; Pihlgren, M.; López-Deber, M.P.; Reis, P.; Hickman, D.T.; Adolfsson, O.; Chuard, N.; Ndao, D.M.; Borghgraef, P.; Devijver, H.; Van Leuven, F.; Pfeifer, A.; Muhs, A. Efficacy and safety of a liposome-based vaccine against protein Tau, assessed in tau.P301L mice that model tauopathy. PLoS One, 2013, 8(8)e72301
[http://dx.doi.org/10.1371/journal.pone.0072301] [PMID: 23977276]
[99]
Nobuhara, C.K.; DeVos, S.L.; Commins, C.; Wegmann, S.; Moore, B.D.; Roe, A.D.; Costantino, I.; Frosch, M.P.; Pitstick, R.; Carlson, G.A.; Hock, C.; Nitsch, R.M.; Montrasio, F.; Grimm, J.; Cheung, A.E.; Dunah, A.W.; Wittmann, M.; Bussiere, T.; Weinreb, P.H.; Hyman, B.T.; Takeda, S. Tau Antibody Targeting Pathological Species Blocks Neuronal Uptake and Interneuron Propagation of Tau in Vitro. Am. J. Pathol., 2017, 187(6), 1399-1412.
[http://dx.doi.org/10.1016/j.ajpath.2017.01.022] [PMID: 28408124]
[100]
“JNJ-63733657 ALZFORUM.” Available from: . https://www. alzforum.org/therapeutics/jnj-63733657accessed Jan. 26, 2021].
[101]
"Gosuranemab ALZFORUM." Available from:. https://www. alzforum.org/therapeutics/gosuranemab[accessed Jan. 26, 2021]
[102]
Zambusi, A.; Ninkovic, J. Regeneration of the Central Nervous System-Principles from Brain Regeneration in Adult Zebrafish. World J. Stem Cells; Baishideng Publishing Group Co, 2020, pp. 8-24.
[http://dx.doi.org/10.4252/wjsc.v12.i1.8]
[103]
Naini, S.M.A.; Yanicostas, C.; Hassan-Abdi, R.; Blondeel, S.; Bennis, M.; Weiss, R.J.; Tor, Y.; Esko, J.D.; Soussi-Yanicostas, N. Surfen and Oxalyl Surfen Decrease Tau Hyperphosphorylation and Mitigate Neuron Deficits in vivo in a Zebrafish Model of Tauopathy. Transl. Neurodegener., 2018, 7(6)
[http://dx.doi.org/10.1186/s40035-018-0111-2] [PMID: 33342432]
[104]
Spilman, P.; Podlutskaya, N.; Hart, M.J.; Debnath, J.; Gorostiza, O.; Bredesen, D.; Richardson, A.; Strong, R.; Galvan, V. Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-β levels in a mouse model of Alzheimer’s disease. PLoS One, 2010, 5(4)e9979
[http://dx.doi.org/10.1371/journal.pone.0009979] [PMID: 20376313]
[105]
Mattson, M.P.; Moehl, K.; Ghena, N.; Schmaedick, M.; Cheng, A. Intermittent Metabolic Switching, Neuroplasticity and Brain Health; Nature Rev. Neurosci. Nature Publishing Group, 2018, pp. 81-94.
[http://dx.doi.org/10.1038/nrn.2017.156]
[106]
Deering Brose, R.; Lehrmann, E.; Zhang, Y.; Reeves, R. H.; Smith, K. D.; Mattson, M. P. Hydroxyurea attenuates oxidative, metabolic, and excitotoxic stress in rat hippocampal neurons and improves spatial memory in a mouse model of Alzheimer’s disease., 2018.
[http://dx.doi.org/10.1016/j.neurobiolaging.2018.08.021]
[107]
Koehler, D.; Shah, Z.A.; Hensley, K.; Williams, F.E. Lanthionine ketimine-5-ethyl ester provides neuroprotection in a zebrafish model of okadaic acid-induced Alzheimer’s disease. Neurochem. Int., 2018, 115, 61-68.
[http://dx.doi.org/10.1016/j.neuint.2018.02.002] [PMID: 29475037]
[108]
Nery, L.R.; Eltz, N.S.; Hackman, C.; Fonseca, R.; Altenhofen, S.; Guerra, H.N.; Freitas, V.M.; Bonan, C.D.; Vianna, M.R.M.R. Brain intraventricular injection of amyloid-β in zebrafish embryo impairs cognition and increases tau phosphorylation, effects reversed by lithium. PLoS One, 2014, 9(9)e105862
[http://dx.doi.org/10.1371/journal.pone.0105862] [PMID: 25187954]
[109]
Javed, I.; Peng, G.; Xing, Y.; Yu, T.; Zhao, M.; Kakinen, A.; Faridi, A.; Parish, C.L.; Ding, F.; Davis, T.P.; Ke, P.C.; Lin, S. Inhibition of amyloid beta toxicity in zebrafish with a chaperone-gold nanoparticle dual strategy. Nat. Commun., 2019, 10(1), 3780.
[http://dx.doi.org/10.1038/s41467-019-11762-0] [PMID: 31439844]

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