Login Register Cart 0
Generic placeholder image

Current Reviews in Clinical and Experimental Pharmacology

Editor-in-Chief

ISSN (Print): 2772-4328
ISSN (Online): 2772-4336

Back
Journal Home About Journal Editorial Board Current Issue Volumes/Issues
Subscribe
Mini-Review Article

Zebrafish Experimental Animal Models for AD: A Comprehensive Review

Author(s): Ruksar Sande, Angel Godad and Gaurav Doshi*

Volume 19, Issue 4, 2024

Published on: 26 January, 2024

Page: [295 - 311] Pages: 17

DOI: 10.2174/0127724328279684240104094257

Price: $65

Abstract

AD disease (AD) is a multifaceted and intricate neurodegenerative disorder characterized by intracellular neurofibrillary tangle (NFT) formation and the excessive production and deposition of Aβ senile plaques. While transgenic AD models have been found instrumental in unravelling AD pathogenesis, they involve cost and time constraints during the preclinical phase. Zebrafish, owing to their simplicity, well-defined behavioural patterns, and relevance to neurodegenerative research, have emerged as a promising complementary model. Zebrafish possess glutaminergic and cholinergic pathways implicated in learning and memory, actively contributing to our understanding of neural transmission processes. This review sheds light on the molecular mechanisms by which various neurotoxic agents, including okadaic acid (OKA), cigarette smoke extract, metals, and transgenic zebrafish models with genetic similarities to AD patients, induce cognitive impairments and neuronal degeneration in mammalian systems. These insights may facilitate the identification of effective neurotoxic agents for replicating AD pathogenesis in the zebrafish brain. In this comprehensive review, the pivotal role of zebrafish models in advancing our comprehension of AD is emphasized. These models hold immense potential for shaping future research directions and clinical interventions, ultimately contributing to the development of novel AD therapies.

Keywords: AD, neurodegeneration, neurofibrillary tangles, amyloid β plaques, cognitive impairment agents, transgenic models.

Next »
Graphical Abstract

[1]
Scheltens P, Blennow K, Breteler MMB, et al. Alzheimer’s disease. Lancet 2016; 388(10043): 505-17.
[http://dx.doi.org/10.1016/S0140-6736(15)01124-1] [PMID: 26921134]
[2]
Lleó A, Greenberg SM, Growdon JH. Current pharmacotherapy for Alzheimer’s disease. Annu Rev Med 2006; 57(1): 513-33.
[http://dx.doi.org/10.1146/annurev.med.57.121304.131442] [PMID: 16409164]
[3]
Graham WV, Bonito-Oliva A, Sakmar TP. Update on Alzheimer’s Disease therapy and prevention strategies. Annu Rev Med 2017; 68: 413-30.
[http://dx.doi.org/10.1146/annurev-med-042915-103753]
[4]
Bhattacharjee S, Zhao Y, Hill JM, Percy ME, Lukiw WJ. Aluminum and its potential contribution to Alzheimer’s disease (AD). Front Aging Neurosci 2014; 6: 62.
[http://dx.doi.org/10.3389/fnagi.2014.00062] [PMID: 24782759]
[5]
Wu L, Rosa-Neto P, Hsiung GYR, et al. Early-onset familial Alzheimer’s disease (EOFAD). Can J Neurol Sci 2012; 39(4): 436-45.
[http://dx.doi.org/10.1017/S0317167100013949] [PMID: 22728850]
[6]
Crews L, Masliah E. Molecular mechanisms of neurodegeneration in Alzheimer’s disease. Hum Mol Genet 2010; 19(R1): R12-20.
[http://dx.doi.org/10.1093/hmg/ddq160] [PMID: 20413653]
[7]
Arnsten AFT, Datta D, Del Tredici K, Braak H. Hypothesis: Tau pathology is an initiating factor in sporadic Alzheimer’s disease. Alzheimers Dement 2021; 17(1): 115-24.
[http://dx.doi.org/10.1002/alz.12192] [PMID: 33075193]
[8]
Tcw J, Goate AM. Genetics of β-amyloid precursor protein in alzheimer’s disease. Cold Spring Harb Perspect Med 2017; 7(6): a024539.
[http://dx.doi.org/10.1101/cshperspect.a024539]
[9]
Pogue AI, Lukiw WJ. Aluminum, the genetic apparatus of the human CNS and Alzheimer’s disease (AD). Morphologie 2016; 100(329): 56-64.
[http://dx.doi.org/10.1016/j.morpho.2016.01.001] [PMID: 26969391]
[10]
Aisen PS, Vellas B, Hampel H. Moving towards early clinical trials for amyloid-targeted therapy in Alzheimer’s disease. Nat Rev Drug Discov 2013; 12(4): 324.
[http://dx.doi.org/10.1038/nrd3842-c1] [PMID: 23493086]
[11]
Hampel H, Hardy J, Blennow K, et al. The amyloid-β pathway in alzheimer’s Disease. Mol Psychiatry 2021; 26(10): 5481-503.
[http://dx.doi.org/10.1038/s41380-021-01249-0] [PMID: 34456336]
[12]
Hampel H, Hardy J, Blennow K, Chen C, Perry G, Kim SH. The amyloid-β pathway in Alzheimer’s Disease. Mol Psychiatry 2021; 26(10): 5481-503.
[http://dx.doi.org/10.1038/s41380-021-01249-0]
[13]
Alavi NSM, Soussi-Yanicostas N. Tau hyperphosphorylation and oxidative stress, a critical vicious circle in neurodegenerative tauopathies? Oxid Med Cell Longev 2015; 2015: 151979.
[http://dx.doi.org/10.1155/2015/151979]
[14]
Brandt R, Léger J, Lee G. Interaction of tau with the neural plasma membrane mediated by tau’s amino-terminal projection domain. J Cell Biol 1995; 131(5): 1327-40.
[http://dx.doi.org/10.1083/jcb.131.5.1327] [PMID: 8522593]
[15]
Rösler TW, Marvian A, Brendel M, et al. Four-repeat tauopathies. Prog Neurobiol 2019; 180: 101644.
[http://dx.doi.org/10.1016/j.pneurobio.2019.101644] [PMID: 31238088]
[16]
Saha P, Sen N. Tauopathy: A common mechanism for neurodegeneration and brain aging. Mech Ageing Dev 2019; 178: 72-9.
[http://dx.doi.org/10.1016/j.mad.2019.01.007] [PMID: 30668956]
[17]
Auld DS, Kornecook TJ, Bastianetto S, Quirion R. Alzheimer’s disease and the basal forebrain cholinergic system: Relations to β-amyloid peptides, cognition, and treatment strategies. Prog Neurobiol 2002; 68(3): 209-45.
[http://dx.doi.org/10.1016/S0301-0082(02)00079-5] [PMID: 12450488]
[18]
Lindsley CW, Hooker JM. Beyond the amyloid hypothesis of alzheimer’s disease: tau pathology takes center stage. ACS Chem Neurosci 2018; 9(11): 2519.
[http://dx.doi.org/10.1021/acschemneuro.8b00610] [PMID: 30458619]
[19]
Scheuner D, Eckman C, Jensen M, et al. Secreted amyloid β–protein similar to that in the senile plaques of Alzheimer’s disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer’s disease. Nat Med 1996; 2(8): 864-70.
[http://dx.doi.org/10.1038/nm0896-864] [PMID: 8705854]
[20]
Sengupta U, Nilson AN, Kayed R. The role of amyloid-β oligomers in toxicity, propagation, and immunotherapy. EBioMedicine 2016; 6: 42-9.
[http://dx.doi.org/10.1016/j.ebiom.2016.03.035] [PMID: 27211547]
[21]
Yuan S, Huang X, Zhang L, et al. Associations of air pollution with all-cause dementia, Alzheimer’s disease, and vascular dementia: A prospective cohort study based on 437,932 participants from the UK biobank. Front Neurosci 2023; 17: 1216686.
[http://dx.doi.org/10.3389/fnins.2023.1216686] [PMID: 37600021]
[22]
Bagyinszky E, Youn YC, An SSA, Kim S. Mutations, associated with early-onset Alzheimer’s disease, discovered in Asian countries. Clin Interv Aging 2016; 11: 1467-88.
[http://dx.doi.org/10.2147/CIA.S116218] [PMID: 27799753]
[23]
Adams JD. Probable causes of Alzheimer’s disease. Sci 2021; 3(1): 16.
[http://dx.doi.org/10.3390/sci3010016]
[24]
Jiang T, Yu JT, Tian Y, Tan L. Epidemiology and etiology of Alzheimer’s disease: From genetic to non-genetic factors. Curr Alzheimer Res 2013; 10(8): 852-67.
[http://dx.doi.org/10.2174/15672050113109990155] [PMID: 23919770]
[25]
Drummond E, Wisniewski T. Alzheimer’s Disease: Experimental models and reality. Acta Neuropathol 2017; 133(2): 155.
[26]
Yokoyama M, Kobayashi H, Tatsumi L, Tomita T. Mouse models of alzheimer’s disease. Front Mol Neurosci 2022; 15: 912995.
[http://dx.doi.org/10.3389/fnmol.2022.912995] [PMID: 35799899]
[27]
Castillo-Rangel C, Marín G, Diaz-Chiguer DL, Zarate-Calderon CJ, Viveros-Martinez I, Caycho-Salazar FDMDJ. Animal models in Alzheimer’s disease: Biological plausibility and mood disorders. Neurology Perspectives 2023; 3(1): 100110.
[28]
Sasaguri H, Hashimoto S, Watamura N, et al. Recent advances in the modeling of alzheimer’s disease. Front Neurosci 2022; 16: 807473.
[http://dx.doi.org/10.3389/fnins.2022.807473] [PMID: 35431779]
[29]
Vitek MP, Araujo JA, Fossel M, et al. Translational animal models for Alzheimer’s disease: An Alzheimer’s Association Business Consortium Think Tank. Alzheimers Dement 2020; 6(1): e12114.
[http://dx.doi.org/10.1002/trc2.12114] [PMID: 33457489]
[30]
Jucker M. The benefits and limitations of animal models for translational research in neurodegenerative diseases. Nat Med 2010; 16(11): 1210-4.
[http://dx.doi.org/10.1038/nm.2224]
[31]
Xu QQ, Yang W, Zhong M, Lin ZX, Gray NE, Xian YF. Animal models of Alzheimer’s disease: preclinical insights and challenges. Acta Materia Medica 2023; 2(2): 192-215.
[http://dx.doi.org/10.15212/AMM-2023-0001]
[32]
Van Norman GA. Limitations of animal studies for predicting toxicity in clinical trials. JACC Basic Transl Sci 2019; 4(7): 845-54.
[http://dx.doi.org/10.1016/j.jacbts.2019.10.008] [PMID: 31998852]
[33]
Newman M, Verdile G, Martins RN, Lardelli M. Zebrafish as a tool in Alzheimer’s disease research. Biochim Biophys Acta Mol Basis Dis 2011; 1812(3): 346-52.
[http://dx.doi.org/10.1016/j.bbadis.2010.09.012]
[34]
Sanchez-Varo R, Mejias-Ortega M, Fernandez-Valenzuela JJ, Nuñez-Diaz C, Caceres-Palomo L, Vegas-Gomez L. Transgenic mouse models of alzheimer’s disease: An integrative analysis. Int J Mol Sci 2022; 23(10): 5404.
[35]
Bailone RL, Fukushima HCS, Fernandes BH, et al. Zebrafish as an alternative animal model in human and animal vaccination research. Lab Anim Res 2020; 36(1): 13.
[http://dx.doi.org/10.1186/s42826-020-00042-4] [PMID: 32382525]
[36]
Shenoy A, Banerjee M, Upadhya A, Bagwe-Parab S, Kaur G. The brilliance of the zebrafish model: Perception on behavior and alzheimer’s Disease. Front Behav Neurosci 2022; 16: 861155.
[http://dx.doi.org/10.3389/fnbeh.2022.861155] [PMID: 35769627]
[37]
Saleem S, Kannan RR. Zebrafish: An emerging real-time model system to study Alzheimer’s disease and neurospecific drug discovery. Cell Death Discov 2018; 4: 45.
[http://dx.doi.org/10.1038/s41420-018-0109-7]
[38]
Santana S, Rico EP, Burgos JS. Can zebrafish be used as animal model to study Alzheimer’s disease? Am J Neurodegener Dis 2012; 1(1): 32.
[39]
Panula P, Sallinen V, Sundvik M, Kolehmainen J, Torkko V, Tiittula A. Modulatory neurotransmitter systems and behavior: Towards zebrafish models of neurodegenerative diseases. Zebrafish 2006; 3(2): 235-47.
[40]
Saleem S, Kannan RR. Zebrafish: An emerging real-time model system to study Alzheimer’s disease and neurospecific drug discovery. Cell Death Discov 2018; 4: 45.
[http://dx.doi.org/10.1038/s41420-018-0109-7]
[41]
Chakraborty C, Hsu C, Wen Z, Lin C, Agoramoorthy G. Zebrafish: A complete animal model for in vivo drug discovery and development. Curr Drug Metab 2009; 10(2): 116-24.
[http://dx.doi.org/10.2174/138920009787522197] [PMID: 19275547]
[42]
Williams FE, Messer WS Jr. Muscarinic acetylcholine receptors in the brain of the zebrafish (Danio rerio) measured by radioligand binding techniques. Comp Biochem Physiol C Toxicol Pharmacol 2004; 137(4): 349-53.
[http://dx.doi.org/10.1016/j.cca.2004.03.002] [PMID: 15228953]
[43]
Park E, Lee Y, Kim Y, Lee CJ. Cholinergic modulation of neural activity in the telencephalon of the zebrafish. Neurosci Lett 2008; 439(1): 79-83.
[http://dx.doi.org/10.1016/j.neulet.2008.04.064] [PMID: 18501513]
[44]
Mans RA, Hinton KD, Payne CH, Powers GE, Scheuermann NL, Saint-Jean M. Cholinergic stimulation of the adult zebrafish brain induces phosphorylation of glycogen synthase kinase-3 β and extracellular signal-regulated kinase in the telencephalon. Front Mol Neurosci 2019; 12: 91.
[http://dx.doi.org/10.3389/fnmol.2019.00091] [PMID: 31040768]
[45]
Chen X, Gays D, Santoro MM. Transgenic zebrafish. Methods Mol Biol 2016; 1464: 107-14.
[http://dx.doi.org/10.1007/978-1-4939-3999-2_10] [PMID: 27858360]
[46]
Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT, Akerboom J. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat Methods 2013; 10(2): 162-70.
[http://dx.doi.org/10.1038/nmeth.2333]
[47]
MacDonald RB, Kashikar ND, Lagnado L, Harris WA. A novel tool to measure extracellular glutamate in the zebrafish nervous system in vivo. Zebrafish 2017; 14(3): 284-6.
[http://dx.doi.org/10.1089/zeb.2016.1385] [PMID: 28027028]
[48]
Gesemann M, Maurer CM, Neuhauss SCF. Excitatory amino acid transporters in the zebrafish. Brain Res Bull 2010; 83(5): 202-6.
[http://dx.doi.org/10.1016/j.brainresbull.2010.04.018] [PMID: 20466040]
[49]
Li F, Tsien JZ. Memory and the NMDA receptors. N Engl J Med 2009; 361(3): 302-3.
[http://dx.doi.org/10.1056/NEJMcibr0902052]
[50]
Clemente D, Porteros Á, Weruaga E, et al. Cholinergic elements in the zebrafish central nervous system: Histochemical and immunohistochemical analysis. J Comp Neurol 2004; 474(1): 75-107.
[http://dx.doi.org/10.1002/cne.20111] [PMID: 15156580]
[51]
Yegambaram M, Manivannan B, Beach T, Halden R. Role of environmental contaminants in the etiology of Alzheimer’s disease: A review. Curr Alzheimer Res 2015; 12(2): 116-46.
[http://dx.doi.org/10.2174/1567205012666150204121719] [PMID: 25654508]
[52]
Kamat PK, Rai S, Swarnkar S, Shukla R, Nath C. Mechanism of synapse redox stress in Okadaic acid (ICV) induced memory impairment: Role of NMDA receptor. Neurochem Int 2014; 76: 32-41.
[http://dx.doi.org/10.1016/j.neuint.2014.06.012] [PMID: 24984170]
[53]
Rudrabhatla P, Pant HC. Role of protein phosphatase 2A in Alzheimer’s disease. Curr Alzheimer Res 2011; 8(6): 623-32.
[http://dx.doi.org/10.2174/156720511796717168] [PMID: 21605044]
[54]
Williams FE, Koehler D. Utilizing zebrafish and okadaic acid to study Alzheimer’s disease. Neural Regen Res 2018; 13(9): 1538-41.
[http://dx.doi.org/10.4103/1673-5374.237111] [PMID: 30127109]
[55]
Sontag JM, Sontag E. Protein phosphatase 2A dysfunction in Alzheimer’s disease. Front Mol Neurosci 2014; 7: 16.
[PMID: 24653673]
[56]
Nada SE, Williams FE, Shah ZA. Development of a novel and robust pharmacological model of okadaic acid-induced alzheimer’s disease in zebrafish. CNS Neurol Disord Drug Targets 2016; 15(1): 86-94.
[http://dx.doi.org/10.2174/1871527314666150821105602] [PMID: 26295819]
[57]
Cacialli P, Gueguen MM, Coumailleau P, et al. BDNF expression in larval and adult zebrafish brain: Distribution and cell identification. PLoS One 2016; 11(6): e0158057.
[http://dx.doi.org/10.1371/journal.pone.0158057] [PMID: 27336917]
[58]
Koehler D, Shah ZA, Hensley K, Williams FE. Lanthionine ketimine-5-ethyl ester provides neuroprotection in a zebrafish model of okadaic acid-induced Alzheimer’s disease. Neurochem Int 2018; 115: 61-8.
[http://dx.doi.org/10.1016/j.neuint.2018.02.002] [PMID: 29475037]
[59]
Koehler D, Shah ZA, Williams FE. The GSK3β inhibitor, TDZD-8, rescues cognition in a zebrafish model of okadaic acid-induced Alzheimer’s disease. Neurochem Int 2019; 122: 31-7.
[http://dx.doi.org/10.1016/j.neuint.2018.10.022] [PMID: 30392874]
[60]
Serrano-Pozo A, Frosch MP, Masliah E, Hyman BT. Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med 2011; 1(1): a006189.
[http://dx.doi.org/10.1101/cshperspect.a006189] [PMID: 22229116]
[61]
Johnson GVW, Stoothoff WH. Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 2004; 117(24): 5721-9.
[http://dx.doi.org/10.1242/jcs.01558] [PMID: 15537830]
[62]
Medina M, Avila J, Villanueva N. Use of okadaic acid to identify relevant phosphoepitopes in pathology: A focus on neurodegeneration. Mar Drugs 2013; 11(5): 1656-68.
[http://dx.doi.org/10.3390/md11051656]
[63]
Ryu AR, Kim DH, Kim E, Lee MY. Use of okadaic acid to identify relevant phosphoepitopes in pathology: A focus on neurodegeneration. Mar Drugs 2018; 11(5): 1656-568.
[http://dx.doi.org/10.1155/2018/4692081]
[64]
Naik P, Fofaria N, Prasad S, et al. Oxidative and pro-inflammatory impact of regular and denicotinized cigarettes on blood brain barrier endothelial cells: Is smoking reduced or nicotine-free products really safe? BMC Neurosci 2014; 15(1): 51.
[http://dx.doi.org/10.1186/1471-2202-15-51] [PMID: 24755281]
[65]
Naik P, Sajja RK, Prasad S, Cucullo L. Effect of full flavor and denicotinized cigarettes exposure on the brain microvascular endothelium: A microarray-based gene expression study using a human immortalized BBB endothelial cell line. BMC Neurosci 2015; 16(1): 38.
[http://dx.doi.org/10.1186/s12868-015-0173-3] [PMID: 26099276]
[66]
Alrouji M, Manouchehrinia A, Gran B, Constantinescu CS. Effects of cigarette smoke on immunity, neuroinflammation and multiple sclerosis. J Neuroimmunol 2019; 329: 24-34.
[http://dx.doi.org/10.1016/j.jneuroim.2018.10.004] [PMID: 30361070]
[67]
Aedo G, Miranda M, Chávez MN, Allende ML, Egaña JT. A reliable preclinical model to study the impact of cigarette smoke in development and disease. Curr Protoc Toxicol 2019; 80(1): e78.
[http://dx.doi.org/10.1002/cptx.78] [PMID: 31058471]
[68]
Muthuraman A, Thilagavathi L, Jabeen S, Ravishankar SB, Ahmed SS, George T. Curcumin prevents cigarette smoke extract induced cognitive impairment. Front Biosci 2019; 11(1): 109-20.
[http://dx.doi.org/10.2741/e850]
[69]
Muthuraman A, Nafisa K, Sowmya MS, et al. Role of ambrisentan (selective endothelin-A receptor antagonist) on cigarette smoke exposure induced cognitive impairment in Danio rerio. Life Sci 2019; 222: 133-9.
[http://dx.doi.org/10.1016/j.lfs.2019.03.002] [PMID: 30844374]
[70]
Paduraru E, Iacob D, Rarinca V, Plavan G, Ureche D, Jijie R. Zebrafish as a potential model for neurodegenerative diseases: A focus on toxic metals implications. Int J Mol Sci 2023; 24(4): 3428.
[http://dx.doi.org/10.3390/ijms24043428]
[71]
Lopes AC, Peixe TS, Mesas AE, Paoliello MMB. Lead exposure and oxidative stress: A systematic review. Rev Environ Contam Toxicol 2016; 236: 193-238.
[PMID: 26423075]
[72]
Rossi E. Low level environmental lead exposure – a continuing challenge. Clin Biochem Rev 2008; 29(2): 63.
[73]
Mansouri MT, Muñoz-Fambuena I, Cauli O. Cognitive impairment associated with chronic lead exposure in adults. Neurol Psychiatry Brain Res 2018; 30: 5-8.
[http://dx.doi.org/10.1016/j.npbr.2018.04.001]
[74]
Mu Y, Yu J, Ji W, Chen L, Wang X, Yan B. Alleviation of Pb2+ pollution-induced oxidative stress and toxicity in microglial cells and zebrafish larvae by chicoric acid. Ecotoxicol Environ Saf 2019; 180: 396-402.
[http://dx.doi.org/10.1016/j.ecoenv.2019.05.040] [PMID: 31108416]
[75]
Tisato F, Marzano C, Porchia M, Pellei M, Santini C. Copper in diseases and treatments, and copper-based anticancer strategies. Med Res Rev 2010; 30(4): 708-49.
[http://dx.doi.org/10.1002/med.20174] [PMID: 19626597]
[76]
Huffman DL, O’Halloran TV. Energetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2. J Biol Chem 2000; 275(25): 18611-4.
[http://dx.doi.org/10.1074/jbc.C000172200] [PMID: 10764731]
[77]
Labbé S, Zhu Z, Thiele DJ. Copper-specific transcriptional repression of yeast genes encoding critical components in the copper transport pathway. J Biol Chem 1997; 272(25): 15951-8.
[http://dx.doi.org/10.1074/jbc.272.25.15951] [PMID: 9188496]
[78]
Mackenzie NC, Brito M, Reyes AE, Allende ML. Cloning, expression pattern and essentiality of the high-affinity copper transporter 1 (ctr1) gene in zebrafish. Gene 2004; 328(1–2): 113-20.
[http://dx.doi.org/10.1016/j.gene.2003.11.019] [PMID: 15019990]
[79]
Bellingham SA, Ciccotosto GD, Needham BE, et al. Gene knockout of amyloid precursor protein and amyloid precursor-like protein-2 increases cellular copper levels in primary mouse cortical neurons and embryonic fibroblasts. J Neurochem 2004; 91(2): 423-8.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02731.x] [PMID: 15447675]
[80]
Tõugu V, Tiiman A, Palumaa P. Interactions of Zn(ii) and Cu(ii) ions with Alzheimer’s amyloid-beta peptide. Metal ion binding, contribution to fibrillization and toxicity. Metallomics 2011; 3(3): 250-61.
[http://dx.doi.org/10.1039/c0mt00073f] [PMID: 21359283]
[81]
Xiao T, Ackerman CM, Carroll EC, Jia S, Hoagland A, Chan J. Copper regulates rest-activity cycles through the locus coeruleus-norepinephrine system. Nat Chem Biol 2018; 14: 655-63.
[http://dx.doi.org/10.1038/s41589-018-0062-z]
[82]
Crouch PJ, Hung LW, Adlard PA, et al. Increasing Cu bioavailability inhibits Aβ oligomers and tau phosphorylation. Proc Natl Acad Sci 2009; 106(2): 381-6.
[http://dx.doi.org/10.1073/pnas.0809057106] [PMID: 19122148]
[83]
Rihel J. Copper on the brain. Nat Chem Biol 2018; 14(7): 638-9.
[http://dx.doi.org/10.1038/s41589-018-0089-1]
[84]
McLaughlin AIG, Kazantzis G, King E, Teare D, Porter RJ, Owen R. Pulmonary fibrosis and encephalopathy associated with the inhalation of aluminium dust. Occup Environ Med 1962; 19(4): 253-63.
[http://dx.doi.org/10.1136/oem.19.4.253]
[85]
Crapper DR, Krishnan SS, Dalton AJ. Distribution in alzheimer’s disease and experimental neurofibrillary degeneration. Science 1979; 180(4085): 511-3.
[86]
Bondy SC. Low levels of aluminum can lead to behavioral and morphological changes associated with Alzheimer’s disease and age-related neurodegeneration. Neurotoxicology 2016; 52: 222-9.
[http://dx.doi.org/10.1016/j.neuro.2015.12.002] [PMID: 26687397]
[87]
Wang Z, Wei X, Yang J, et al. Chronic exposure to aluminum and risk of Alzheimer’s disease: A meta-analysis. Neurosci Lett 2016; 610: 200-6.
[http://dx.doi.org/10.1016/j.neulet.2015.11.014] [PMID: 26592479]
[88]
Dave G. The influence of pH on the toxicity of aluminum, cadmium, and iron to eggs and larvae of the zebrafish, Brachydanio rerio. Ecotoxicol Environ Saf 1985; 10(2): 253-67.
[http://dx.doi.org/10.1016/0147-6513(85)90072-7] [PMID: 4085384]
[89]
Monaco A, Grimaldi MC, Ferrandino I. Aluminium chloride-induced toxicity in zebrafish larvae. J Fish Dis 2017; 40(5): 629-35.
[http://dx.doi.org/10.1111/jfd.12544] [PMID: 27523735]
[90]
Xiong H, Zhao-Ming Z, Yi C, Xiong H, Zhao-Ming Z, Yi C. Locomotor activity and learning and memory abilities in Alzheimer’s disease induced by aluminum in an acid environment in zebrafish. Dongwuxue Yanjiu 2012; 33(2): 231-6.
[91]
Senger MR, Seibt KJ, Ghisleni GC, Dias RD, Bogo MR, Bonan CD. Aluminum exposure alters behavioral parameters and increases acetylcholinesterase activity in zebrafish (Danio rerio) brain. Cell Biol Toxicol 2011; 27(3): 199-205.
[http://dx.doi.org/10.1007/s10565-011-9181-y] [PMID: 21240652]
[92]
Chiswell B, Mokhtar MB. The speciation of manganese in freshwaters. Talanta 1986; 33(8): 669-77.
[http://dx.doi.org/10.1016/0039-9140(86)80156-4] [PMID: 18964165]
[93]
Lee E, Karki P, Johnson J Jr, Hong P, Aschner M. Manganese control of glutamate transporters’ gene expression. Adv Neurobiol 2017; 16: 1-12.
[http://dx.doi.org/10.1007/978-3-319-55769-4_1] [PMID: 28828603]
[94]
Harford AJ, Mooney TJ, Trenfield MA, van Dam RA. Manganese toxicity to tropical freshwater species in low hardness water. Environ Toxicol Chem 2015; 34(12): 2856-63.
[http://dx.doi.org/10.1002/etc.3135] [PMID: 26118763]
[95]
Peres TV, Schettinger MRC, Chen P, Carvalho F, Avila DS, Bowman AB. Manganese-induced neurotoxicity: A review of its behavioral consequences and neuroprotective strategies. BMC Pharmacol Toxicol 2016; 17: 57.
[http://dx.doi.org/10.1186/s40360-016-0099-0]
[96]
Tuschl K, Mills PB, Clayton PT. Manganese and the Brain. Int Rev Neurobiol 2013; 110: 277-312.
[http://dx.doi.org/10.1016/B978-0-12-410502-7.00013-2] [PMID: 24209443]
[97]
Horning KJ, Caito SW, Tipps KG, Bowman AB, Aschner M. Manganese is essential for neuronal health. Annu Rev Nutr 2015; 35: 71-108.
[http://dx.doi.org/10.1146/annurev-nutr-071714-034419]
[98]
Chen P, Miah MR, Aschner M. Metals and neurodegeneration. F1000Res 2016; 5: F1000 Faculty Rev-366.
[99]
Kim H, Harrison FE, Aschner M, Bowman AB. Exposing the role of metals in neurological disorders: A focus on manganese. Trends Mol Med 2022; 28(7): 555-68.
[http://dx.doi.org/10.1016/j.molmed.2022.04.011] [PMID: 35610122]
[100]
Altenhofen S, Wiprich MT, Nery LR, Leite CE, Vianna MRMR, Bonan CD. Manganese(II) chloride alters behavioral and neurochemical parameters in larvae and adult zebrafish. Aquat Toxicol 2017; 182: 172-83.
[http://dx.doi.org/10.1016/j.aquatox.2016.11.013] [PMID: 27912164]
[101]
Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L. The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol 2014; 13(10): 1045-60.
[http://dx.doi.org/10.1016/S1474-4422(14)70117-6] [PMID: 25231526]
[102]
Ashraf A, So PW. Spotlight on ferroptosis: Iron-dependent cell death in alzheimer’s disease. Front Aging Neurosci 2020; 12: 196.
[http://dx.doi.org/10.3389/fnagi.2020.00196] [PMID: 32760266]
[103]
Wang F, Wang J, Shen Y, Li H, Rausch WD, Huang X. Iron dyshomeostasis and ferroptosis: A new Alzheimer’s Disease hypothesis? Front Aging Neurosci 2022; 14: 830569.
[http://dx.doi.org/10.3389/fnagi.2022.830569] [PMID: 35391749]
[104]
Peng Y, Chang X, Lang M. Iron homeostasis disorder and alzheimer’s disease. Int J Mol Sci 2021; 22(22): 12442.
[http://dx.doi.org/10.3390/ijms222212442]
[105]
Cassidy L, Fernandez F, Johnson JB, Naiker M, Owoola AG, Broszczak DA. Oxidative stress in alzheimer’s disease: A review on emergent natural polyphenolic therapeutics. Complement Ther Med 2020; 49: 102294.
[http://dx.doi.org/10.1016/j.ctim.2019.102294] [PMID: 32147039]
[106]
Acosta DS, Danielle NM, Altenhofen S, et al. Copper at low levels impairs memory of adult zebrafish (Danio rerio) and affects swimming performance of larvae. Comp Biochem Physiol C Toxicol Pharmacol 2016; 185-186: 122-30.
[http://dx.doi.org/10.1016/j.cbpc.2016.03.008] [PMID: 27012768]
[107]
Haverroth GMB, Welang C, Mocelin RN, et al. Copper acutely impairs behavioral function and muscle acetylcholinesterase activity in zebrafish (Danio rerio). Ecotoxicol Environ Saf 2015; 122: 440-7.
[http://dx.doi.org/10.1016/j.ecoenv.2015.09.012] [PMID: 26386335]
[108]
Xu X, Weber D, Burge R, VanAmberg K. Neurobehavioral impairments produced by developmental lead exposure persisted for generations in zebrafish (Danio rerio). Neurotoxicology 2016; 52: 176-85.
[http://dx.doi.org/10.1016/j.neuro.2015.12.009] [PMID: 26688331]
[109]
Zhu B, Wang Q, Shi X, Guo Y, Xu T, Zhou B. Effect of combined exposure to lead and decabromodiphenyl ether on neurodevelopment of zebrafish larvae. Chemosphere 2016; 144: 1646-54.
[http://dx.doi.org/10.1016/j.chemosphere.2015.10.056] [PMID: 26519795]
[110]
Cras P, Kawai M, Lowery D, Gonzalez-DeWhitt P, Greenberg B, Perry G. Senile plaque neurites in Alzheimer disease accumulate amyloid precursor protein. Proc Natl Acad Sci 1991; 88(17): 7552-6.
[http://dx.doi.org/10.1073/pnas.88.17.7552] [PMID: 1652752]
[111]
Bai Q, Burton EA. Zebrafish models of Tauopathy. Biochim Biophys Acta Mol Basis Dis 2011; 1812(3): 353-63.
[http://dx.doi.org/10.1016/j.bbadis.2010.09.004]
[112]
Weber T, Köster R. Genetic tools for multicolor imaging in zebrafish larvae. Methods 2013; 62(3): 279-91.
[http://dx.doi.org/10.1016/j.ymeth.2013.07.028] [PMID: 23886907]
[113]
Lee JA, Cole GJ. Generation of transgenic zebrafish expressing green fluorescent protein under control of zebrafish amyloid precursor protein gene regulatory elements. Zebrafish 2007; 4(4): 277-86.
[http://dx.doi.org/10.1089/zeb.2007.0516] [PMID: 18284334]
[114]
Shakes LA, Malcolm TL, Allen KL, De S, Harewood KR, Chatterjee PK. Context dependent function of APPb enhancer identified using enhancer trap-containing BACs as transgenes in zebrafish. Nucleic Acids Res 2008; 36(19): 6237-48.
[http://dx.doi.org/10.1093/nar/gkn628] [PMID: 18832376]
[115]
Nik SH, Wilson L, Newman M, et al. The BACE1-PSEN-AβPP regulatory axis has an ancient role in response to low oxygen/oxidative stress. J Alzheimers Dis 2012; 28(3): 515-30.
[http://dx.doi.org/10.3233/JAD-2011-110533] [PMID: 22045484]
[116]
Pu YZ, Liang L, Fu AL, et al. Generation of Alzheimer’s disease transgenic zebrafish expressing human app mutation under control of zebrafish appb promotor. Curr Alzheimer Res 2017; 14(6): 668-79.
[http://dx.doi.org/10.2174/1567205013666161201202000] [PMID: 27978793]
[117]
Cameron DJ, Galvin C, Alkam T, Sidhu H, Ellison J, Luna S. Alzheimer’s-related peptide amyloid-β plays a conserved role in angiogenesis. PLoS One 2012; 7(7): e39598.
[118]
Cunvong K, Huffmire D, Ethell DW, Cameron DJ. Amyloid-β increases capillary bed density in the adult zebrafish retina. Invest Ophthalmol Vis Sci 2013; 54(2): 1516-21.
[http://dx.doi.org/10.1167/iovs.12-10821] [PMID: 23404118]
[119]
McGowan E, Pickford F, Kim J, Onstead L, Eriksen J, Yu C A. Aβ42 is essential for parenchymal and vascular amyloid deposition in mice. Neuron 2005; 47(2): 191.
[http://dx.doi.org/10.1016/j.neuron.2005.06.030]
[120]
Meyer EP, 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 2008; 105(9): 3587.
[121]
Hannan SB, Dräger NM, Rasse TM, Voigt A, Jahn TR. Cellular and molecular modifier pathways in tauopathies: the big picture from screening invertebrate models. J Neurochem 2016; 137(1): 12-25.
[http://dx.doi.org/10.1111/jnc.13532] [PMID: 26756400]
[122]
Liu Y. Zebrafish as a model organism for studying pathologic mechanisms of neurodegenerative diseases and other neural disorders. Cell Mol Neurobiol 2023; 43(6): 2603-20.
[http://dx.doi.org/10.1007/s10571-023-01340-w]
[123]
De Strooper B, Saftig P, Craessaerts K, et al. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 1998; 391(6665): 387-90.
[http://dx.doi.org/10.1038/34910] [PMID: 9450754]
[124]
Paquet D, Schmid B, Haass C. Transgenic zebrafish as a novel animal model to study tauopathies and other neurodegenerative disorders in vivo. Neurodegener Dis 2010; 7(1-3): 99-102.
[http://dx.doi.org/10.1159/000285515] [PMID: 20173336]
[125]
De Strooper B, Iwatsubo T, Wolfe MS. Presenilins and γ-secretase: Structure, function, and role in alzheimer disease. Cold Spring Harb Perspect Med 2012; 2(1)
[126]
Bentahir M, Nyabi O, Verhamme J, et al. Presenilin clinical mutations can affect γ-secretase activity by different mechanisms. J Neurochem 2006; 96(3): 732-42.
[http://dx.doi.org/10.1111/j.1471-4159.2005.03578.x] [PMID: 16405513]
[127]
Barbier P, Zejneli O, Martinho M, et al. Role of tau as a microtubule-associated protein: Structural and functional aspects. Front Aging Neurosci 2019; 11: 204.
[http://dx.doi.org/10.3389/fnagi.2019.00204] [PMID: 31447664]
[128]
Takashima A, Murayama M, Murayama O, et al. Presenilin 1 associates with glycogen synthase kinase-3β and its substrate tau. Proc Natl Acad Sci 1998; 95(16): 9637-41.
[http://dx.doi.org/10.1073/pnas.95.16.9637] [PMID: 9689133]
[129]
Köpke E, Tung YC, Shaikh S, Alonso AC, Iqbal K, Grundke-Iqbal I. Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J Biol Chem 1993; 268(32): 24374-84.
[http://dx.doi.org/10.1016/S0021-9258(20)80536-5] [PMID: 8226987]
[130]
Flament S, Delacourte A, Verny M, Hauw JJ, Javoy-Agid F. Abnormal Tau proteins in progressive supranuclear palsy. Acta Neuropathol 1991; 81(6): 591-6.
[http://dx.doi.org/10.1007/BF00296367] [PMID: 1831952]
[131]
Andreadis A. Tau gene alternative splicing: expression patterns, regulation and modulation of function in normal brain and neurodegenerative diseases. Biochim Biophys Acta Mol Basis Dis 2005; 1739(2-3): 91-103.
[http://dx.doi.org/10.1016/j.bbadis.2004.08.010] [PMID: 15615629]
[132]
Barbereau C, Cubedo N, Maurice T, Rossel M. Zebrafish models to study new pathways in tauopathies. Int J Mol Sci 2021; 22(9): 4626.
[http://dx.doi.org/10.3390/ijms22094626]
[133]
Nery LR, Silva NE, Fonseca R, Vianna MRM. Presenilin-1 targeted morpholino induces cognitive deficits, increased brain aβ1-42 and decreased synaptic marker psd-95 in zebrafish larvae. Neurochem Res 2017; 42(10): 2959-67.
[http://dx.doi.org/10.1007/s11064-017-2327-4] [PMID: 28623607]
[134]
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): 124-32.
[http://dx.doi.org/10.1016/S0014-4827(03)00257-X] [PMID: 12941610]
[135]
Sharma P, Saraswathy VM, Xiang L, Fürthauer M. Notch-mediated inhibition of neurogenesis is required for zebrafish spinal cord morphogenesis. Sci Rep 2019; 9(1): 9958.
[http://dx.doi.org/10.1038/s41598-019-46067-1]
[136]
Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C A. A γ‐ secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep 2002; 3(7): 688-94.
[http://dx.doi.org/10.1093/embo-reports/kvf124] [PMID: 12101103]
[137]
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): 834-42.
[http://dx.doi.org/10.1523/JNEUROSCI.21-03-00834.2001] [PMID: 11157069]
[138]
Nornes S, Newman M, Wells S, Verdile G, Martins RN, Lardelli M. Independent and cooperative action of Psen2 with Psen1 in zebrafish embryos. Exp Cell Res 2009; 315(16): 2791-801.
[http://dx.doi.org/10.1016/j.yexcr.2009.06.023] [PMID: 19563801]
[139]
Barazzuol L, Cieri D, Facchinello N, et al. Unraveling presenilin 2 functions in a knockout zebrafish line to shed light into alzheimer’s disease pathogenesis. Cells 2023; 12(3): 376.
[http://dx.doi.org/10.3390/cells12030376] [PMID: 36766721]
[140]
Weller J, Budson A. Current understanding of Alzheimer’s disease diagnosis and treatment. F1000Res 2018; 7: F1000 Faculty Rev- 1161.
[141]
Dong Y, Newman M, Pederson SM, Barthelson K, Hin N, Lardelli M. Transcriptome analyses of 7-day-old zebrafish larvae possessing a familial Alzheimer’s disease-like mutation in psen1 indicate effects on oxidative phosphorylation, ECM and MCM functions, and iron homeostasis. BMC Genomics 2021; 22(1): 211.
[http://dx.doi.org/10.1186/s12864-021-07509-1] [PMID: 33761877]
[142]
Howe K, Clark MD, Torroja CF, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496(7446): 498-503.
[http://dx.doi.org/10.1038/nature12111] [PMID: 23594743]
[143]
van Tijn P, Kamphuis W, Marlatt MW, Hol EM, Lucassen PJ. Presenilin mouse and zebrafish models for dementia: Focus on neurogenesis. Prog Neurobiol 2011; 93(2): 149-64.
[http://dx.doi.org/10.1016/j.pneurobio.2010.10.008] [PMID: 21056616]
[144]
Delabio R, Rasmussen L, Mizumoto I, et al. PSEN1 and PSEN2 gene expression in Alzheimer’s disease brain: a new approach. J Alzheimers Dis 2014; 42(3): 757-60.
[http://dx.doi.org/10.3233/JAD-140033] [PMID: 24927704]
[145]
Hin N, Newman M, Kaslin J, et al. Accelerated brain aging towards transcriptional inversion in a zebrafish model of the K115fs mutation of human PSEN2. PLoS One 2020; 15(1): e0227258.
[http://dx.doi.org/10.1371/journal.pone.0227258] [PMID: 31978074]
[146]
Lanoiselée HM, Nicolas G, Wallon D, Rovelet-Lecrux A, Lacour M, Rousseau S. APP, PSEN1, and PSEN2 mutations in early-onset Alzheimer disease: A genetic screening study of familial and sporadic cases. PLoS Med 2017; 14(3): e1002270.
[147]
Musa A, Lehrach H, Russo V. Distinct expression patterns of two zebrafish homologues of the human APP gene during embryonic development. Dev Genes Evol 2001; 211(11): 563-7.
[http://dx.doi.org/10.1007/s00427-001-0189-9] [PMID: 11862463]
[148]
Durliat M, André M, Babin PJ. Conserved protein motifs and structural organization of a fish gene homologous to mammalian apolipoprotein E. Eur J Biochem 2000; 267(2): 549-59.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01033.x] [PMID: 10632725]
[149]
Lee J, Peterson SM, Freeman JL. Alzheimer’s disease risk genes in wild-type adult zebrafish exhibit gender-specific expression changes during aging. Neurogenetics 2016; 17(3): 197-9.
[http://dx.doi.org/10.1007/s10048-016-0485-1] [PMID: 27234028]
[150]
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): 471-81.
[http://dx.doi.org/10.1111/jnc.12198] [PMID: 23406323]
[151]
Campbell WA, Yang H, Zetterberg H, et al. Zebrafish lacking Alzheimer presenilin enhancer 2 (Pen-2) demonstrate excessive p53-dependent apoptosis and neuronal loss. J Neurochem 2006; 96(5): 1423-40.
[http://dx.doi.org/10.1111/j.1471-4159.2006.03648.x] [PMID: 16464238]
[152]
Francis R, McGrath G, Zhang J, et al. 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]
[153]
Lim A, Nik SH, Ebrahimie E, Lardelli M. Analysis of nicastrin gene phylogeny and expression in zebrafish. Dev Genes Evol 2015; 225(3): 171-8.
[http://dx.doi.org/10.1007/s00427-015-0500-9] [PMID: 25940938]
[154]
Leimer U, Lun K, Romig H, et al. 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): 13602-9.
[http://dx.doi.org/10.1021/bi991453n] [PMID: 10521267]
[155]
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): 486-90.
[http://dx.doi.org/10.1007/s00427-002-0269-5] [PMID: 12424519]
[156]
Lee J, Peterson SM, Freeman JL. 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): 400-7.
[http://dx.doi.org/10.1002/jat.3372] [PMID: 27535807]
[157]
Strang KH, Golde TE, Giasson BI. MAPT mutations, tauopathy, and mechanisms of neurodegeneration. Lab Invest 2019; 99(7): 912-28.
[http://dx.doi.org/10.1038/s41374-019-0197-x] [PMID: 30742061]
[158]
Dib S, Pahnke J, Gosselet F. Role of ABCA7 in human health and in alzheimer’s disease. Int J Mol Sci 2021; 22(9): 4603.
[http://dx.doi.org/10.3390/ijms22094603]

Rights & Permissions Print Cite
Article Metrics
17
1
© 2024 Bentham Science Publishers | Privacy Policy