Experimental Models of Synaptopathies Based on Zebrafish
- Authors: Lebedev A.S.1,2,3, Kotova M.M.2, Ilyin N.P.1,3, Kolesnikova T.O.2, Galstyan D.S.1,3,4, Vyunova T.V.5, Petersen E.V.6, Kalueff A.1,2,3,4,7
-
Affiliations:
- World-class Scientific Research Center “Center of Personalized Medicine”, Almazov National Medical Research Center Ministry of Healthcare of Russian Federation
- Neurobiology Department Research Center for Genetics and Life Sciences, Sirius University of Science and Technology
- Institute of Translational Biomedicine, St. Petersburg State University
- Granov Russian Scientific Center for Radiology and Surgical Technologies, Ministry of Healthcare of Russian Federation
- Institute of Molecular Genetics, National Research Center “Kurchatov Institute”
- Moscow Institute of Physics and Technology
- Ural Federal University
- Issue: Vol 109, No 11 (2023)
- Pages: 1601-1616
- Section: REVIEW AND PROBLEM ARTICLES
- URL: https://journals.rcsi.science/0869-8139/article/view/232276
- DOI: https://doi.org/10.31857/S0869813923110092
- EDN: https://elibrary.ru/AEMSZN
- ID: 232276
Cite item
Abstract
Synaptopathies include a heterogeneous group of severely debilitating neurological diseases characterized by structural and functional deficits of neuronal synapses. Common synaptopathies include epilepsy, schizophrenia, prion diseases, autism spectrum disorders, various autoimmune diseases and cochlear synaptopathies. Their pathogenesis is caused by both genetic and environmental factors. However, the relationship between the cause and clinical manifestations of each particular synaptopathy, and their therapy, remain poorly understood. Here, we discuss animal models of synaptopathies, with a specific emphasis on zebrafish (Danio rerio), as well as outline several lines of future research in this field. Overall, zebrafish emerge as a promising organism to mimic a wide range of synaptopahies, paralleling and complementing their existing models in rodents.
About the authors
A. S. Lebedev
World-class Scientific Research Center “Center of Personalized Medicine”,Almazov National Medical Research Center Ministry of Healthcare of Russian Federation; Neurobiology Department Research Center for Genetics and Life Sciences,
Sirius University of Science and Technology; Institute of Translational Biomedicine, St. Petersburg State University
Email: avkalueff@gmail.com
Russia, St. Petersburg; Russia, Sirius Federal Territory; Russia, St. Petersburg
M. M. Kotova
Neurobiology Department Research Center for Genetics and Life Sciences,Sirius University of Science and Technology
Email: avkalueff@gmail.com
Russia, Sirius Federal Territory
N. P. Ilyin
World-class Scientific Research Center “Center of Personalized Medicine”,Almazov National Medical Research Center Ministry of Healthcare of Russian Federation; Institute of Translational Biomedicine, St. Petersburg State University
Email: avkalueff@gmail.com
Russia, St. Petersburg; Russia, St. Petersburg
T. O. Kolesnikova
Neurobiology Department Research Center for Genetics and Life Sciences,Sirius University of Science and Technology
Email: avkalueff@gmail.com
Russia, Sirius Federal Territory
D. S. Galstyan
World-class Scientific Research Center “Center of Personalized Medicine”,Almazov National Medical Research Center Ministry of Healthcare of Russian Federation; Institute of Translational Biomedicine, St. Petersburg State University; Granov Russian Scientific Center for Radiology and Surgical Technologies,
Ministry of Healthcare of Russian Federation
Email: avkalueff@gmail.com
Russia, St. Petersburg; Russia, St. Petersburg; Russia, St. Petersburg
T. V. Vyunova
Institute of Molecular Genetics, National Research Center “Kurchatov Institute”
Email: avkalueff@gmail.com
Russia, Moscow
E. V. Petersen
Moscow Institute of Physics and Technology
Email: avkalueff@gmail.com
Russia, Moscow
A.V. Kalueff
World-class Scientific Research Center “Center of Personalized Medicine”,Almazov National Medical Research Center Ministry of Healthcare of Russian Federation; Neurobiology Department Research Center for Genetics and Life Sciences,
Sirius University of Science and Technology; Institute of Translational Biomedicine, St. Petersburg State University; Granov Russian Scientific Center for Radiology and Surgical Technologies,
Ministry of Healthcare of Russian Federation; Ural Federal University
Author for correspondence.
Email: avkalueff@gmail.com
Russia, St. Petersburg; Russia, Sirius Federal Territory; Russia, St. Petersburg; Russia, St. Petersburg; Russia, Yekaterinburg
References
- Grant SGN (2012) Synaptopathies: diseases of the synaptome. Curr Opin Neurobiol 22: 522–529. https://doi.org/10.1016/j.conb.2012.02.002
- Crisp SJ, Kullmann DM, Vincent A (2016) Autoimmune synaptopathies. Nat Rev Neurosci 17: 103–117. https://doi.org/10.1038/nrn.2015.27
- Wang X, Kery R, Xiong Q (2018) Synaptopathology in autism spectrum disorders: Complex effects of synaptic genes on neural circuits. Prog Neuropsychopharmacol Biol Psychiatry 84: 398–415. https://doi.org/10.1016/j.pnpbp.2017.09.026
- Fewou SN, Plomp JJ, Willison HJ (2014) The pre-synaptic motor nerve terminal as a site for antibody-mediated neurotoxicity in autoimmune neuropathies and synaptopathies. J Anat 224: 36–44. https://doi.org/10.1111/joa.12088
- Bagni C, Zukin RS (2019) A Synaptic Perspective of Fragile X Syndrome and Autism Spectrum Disorders. Neuron 101: 1070–1088. https://doi.org/10.1016/j.neuron.2019.02.041
- Keller R, Basta R, Salerno L, Elia M (2017) Autism, epilepsy, and synaptopathies: a not rare association. Neurol Sci Off J Ital Neurol Soc Ital Soc Clin Neurophysiol 38: 1353–1361. https://doi.org/10.1007/s10072-017-2974-x
- Luo J, Norris RH, Gordon SL, Nithianantharajah J (2018) Neurodevelopmental synaptopathies: Insights from behaviour in rodent models of synapse gene mutations. Prog Neuropsychopharmacol Biol Psychiatry 84: 424–439. https://doi.org/10.1016/j.pnpbp.2017.12.001
- Fukata Y, Fukata M (2017) Epilepsy and synaptic proteins. Curr Opin Neurobiol 45: 1–8. https://doi.org/10.1016/j.conb.2017.02.001
- Obi-Nagata K, Temma Y, Hayashi-Takagi A (2019) Synaptic functions and their disruption in schizophrenia: From clinical evidence to synaptic optogenetics in an animal model. Proc Jpn Acad Ser B Phys Biol Sci 95: 179–197. https://doi.org/10.2183/pjab.95.014
- Asuni AA, Perry VH, O’Connor V (2010) Change in tau phosphorylation associated with neurodegeneration in the ME7 model of prion disease. Biochem Soc Trans 38: 545–551. https://doi.org/10.1042/BST0380545
- Aedo C, Aguilar E (2020) Cochlear synaptopathy: new findings in animal and human research. Rev Neurosci 31: 605–615. https://doi.org/10.1515/revneuro-2020-0002
- Yeh FL, Dong M, Yao J, Tepp WH, Lin G, Johnson EA, Chapman ER (2010) SV2 mediates entry of tetanus neurotoxin into central neurons. PLoS Pathog 6: e1001207. https://doi.org/10.1371/journal.ppat.1001207
- Figgitt DP, Noble S (2002) Botulinum toxin B: a review of its therapeutic potential in the management of cervical dystonia. Drugs 62: 705–722. https://doi.org/10.2165/00003495-200262040-00011
- Cherington M (2004) Botulism: update and review. Semin Neurol 24: 155–163. https://doi.org/10.1055/s-2004-830901
- Farrar JJ, Yen LM, Cook T, Fairweather N, Binh N, Parry J, Parry CM (2000) Tetanus. J Neurol Neurosurg Psychiatry 69: 292–301. https://doi.org/10.1136/jnnp.69.3.292
- Liberman MC, Kujawa SG (2017) Cochlear synaptopathy in acquired sensorineural hearing loss: Manifestations and mechanisms. Hear Res 349: 138–147. https://doi.org/10.1016/j.heares.2017.01.003
- Rodríguez-Caballero A, Torres-Lagares D, Rodríguez-Pérez A, Serrera-Figallo M-A, Hernández-Guisado J-M, Machuca-Portillo G (2010) Cri du chat syndrome: a critical review. Med Oral Patol Oral Cirugia Bucal 15: e473–478. https://doi.org/10.4317/medoral.15.e473
- Kyle SM, Vashi N, Justice MJ (2018) Rett syndrome: a neurological disorder with metabolic components. Open Biol 8: 170216. https://doi.org/10.1098/rsob.170216
- Alfaro-Paredes K, Aguilar-Ydiáquez C, Aguirre-Flores R, Schulz-Cáceres H (2022) Myasthenia gravis and pregnancy: impact and approach. Rev Neurol 75: 117–122. https://doi.org/10.33588/rn.7505.2022207
- Papazian O, Alfonso I (2009) Juvenile myasthenia gravis. Medicina (Mex) 69:71–83
- Claytor B, Cho S-M, Li Y (2023) Myasthenic crisis. Muscle Nerve 68: 8–19. https://doi.org/10.1002/mus.27832
- Kesner VG, Oh SJ, Dimachkie MM, Barohn RJ (2018) Lambert-Eaton Myasthenic Syndrome. Neurol Clin 36: 379–394. https://doi.org/10.1016/j.ncl.2018.01.008
- Eaton LM, Lambert EH (1957) Electromyography and electric stimulation of nerves in diseases of motor unit; observations on myasthenic syndrome associated with malignant tumors. J Am Med Assoc 163: 1117–1124. https://doi.org/10.1001/jama.1957.02970480021005
- Li D, Tansley SL (2019) Juvenile Dermatomyositis-Clinical Phenotypes. Curr Rheumatol Rep 21: 74. https://doi.org/10.1007/s11926-019-0871-4
- Aggarwal R, Charles-Schoeman C, Schessl J, Bata-Csörgő Z, Dimachkie MM, Griger Z, Moiseev S, Oddis C, Schiopu E, Vencovský J, Beckmann I, Clodi E, Bugrova O, Dankó K, Ernste F, Goyal NA, Heuer M, Hudson M, Hussain YM, Karam C, Magnolo N, Nelson R, Pozur N, Prystupa L, Sárdy M, Valenzuela G, van der Kooi AJ, Vu T, Worm M, Levine T, ProDERM Trial Group (2022) Trial of Intravenous Immune Globulin in Dermatomyositis. N Engl J Med 387: 1264–1278. https://doi.org/10.1056/NEJMoa2117912
- Sonoda Y, Arimura K, Kurono A, Suehara M, Kameyama M, Minato S, Hayashi A, Osame M (1996) Serum of Isaacs’ syndrome suppresses potassium channels in PC-12 cell lines. Muscle Nerve 19: 1439–1446. https://doi.org/10.1002/mus.880191102
- Araya EI, Carvalho EC, Andreatini R, Zamponi GW, Chichorro JG (2022) Trigeminal neuropathic pain causes changes in affective processing of pain in rats. Mol Pain 18: 17448069211057750. https://doi.org/10.1177/17448069211057750
- Luo Y, Xu N, Yi W, Yu T, Yang Z (2011) Study on the correlation between synaptic reconstruction and astrocyte after ischemia and the influence of electroacupuncture on rats. Chin J Integr Med 17:750–757. https://doi.org/10.1007/s11655-011-0754-7
- Levy AM, Gomez-Puertas P, Tümer Z (2022) Neurodevelopmental Disorders Associated with PSD-95 and Its Interaction Partners. Int J Mol Sci 23: 4390. https://doi.org/10.3390/ijms23084390
- Levy NS, Umanah GKE, Rogers EJ, Jada R, Lache O, Levy AP (2019) IQSEC2-Associated Intellectual Disability and Autism. Int J Mol Sci 20: 3038. https://doi.org/10.3390/ijms20123038
- Peça J, Feliciano C, Ting JT, Wang W, Wells MF, Venkatraman TN, Lascola CD, Fu Z, Feng G (2011) Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472: 437–442. https://doi.org/10.1038/nature09965
- Hoover BR, Reed MN, Su J, Penrod RD, Kotilinek LA, Grant MK, Pitstick R, Carlson GA, Lanier LM, Yuan L-L, Ashe KH, Liao D (2010) Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron 68: 1067–1081. https://doi.org/10.1016/j.neuron.2010.11.030
- Palmieri M, Frati A, Santoro A, Frati P, Fineschi V, Pesce A (2021) Diffuse Axonal Injury: Clinical Prognostic Factors, Molecular Experimental Models and the Impact of the Trauma Related Oxidative Stress. An Extensive Review Concerning Milestones and Advances. Int J Mol Sci 22: 10865. https://doi.org/10.3390/ijms221910865
- Lee J-H, Lee MY, Chung P-S, Jung JY (2019) Photobiomodulation using low-level 808 nm diode laser rescues cochlear synaptopathy after acoustic overexposure in rat. J Biophotonics 12: e201900145. https://doi.org/10.1002/jbio.201900145
- Varela-Nieto I, Murillo-Cuesta S, Calvino M, Cediel R, Lassaletta L (2020) Drug development for noise-induced hearing loss. Expert Opin Drug Discov 15: 1457–1471. https://doi.org/10.1080/17460441.2020.1806232
- Keithley EM (2020) Pathology and mechanisms of cochlear aging. J Neurosci Res 98: 1674–1684. https://doi.org/10.1002/jnr.24439
- Herrera MI, Otero-Losada M, Udovin LD, Kusnier C, Kölliker-Frers R, de Souza W, Capani F (2017) Could Perinatal Asphyxia Induce a Synaptopathy? New Highlights from an Experimental Model. Neural Plast 2017: 3436943. https://doi.org/10.1155/2017/3436943
- Herrera MI, Kobiec T, Kölliker-Frers R, Otero-Losada M, Capani F (2020) Synaptoprotection in Perinatal Asphyxia: An Experimental Approach. Front Synaptic Neurosci 12: 35. https://doi.org/10.3389/fnsyn.2020.00035
- Ortiz M, Loidl F, Vázquez-Borsetti P (2022) Transition to extrauterine life and the modeling of perinatal asphyxia in rats. WIREs Mech Dis 14: e1568. https://doi.org/10.1002/wsbm.1568
- Wyart C, Del Bene F (2011) Let there be light: zebrafish neurobiology and the optogenetic revolution. Rev Neurosci 22: 121–130. https://doi.org/10.1515/RNS.2011.013
- Key B, Devine CA (2003) Zebrafish as an experimental model: strategies for developmental and molecular neurobiology studies. Methods Cell Sci 25: 1–6. https://doi.org/10.1023/B:MICS.0000006849.98007.03
- Hill AJ, Teraoka H, Heideman W, Peterson RE (2005) Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci Off J Soc Toxicol 86: 6–19. https://doi.org/10.1093/toxsci/kfi110
- Freifeld L, Odstrcil I, Förster D, Ramirez A, Gagnon JA, Randlett O, Costa EK, Asano S, Celiker OT, Gao R, Martin-Alarcon DA, Reginato P, Dick C, Chen L, Schoppik D, Engert F, Baier H, Boyden ES (2017) Expansion microscopy of zebrafish for neuroscience and developmental biology studies. Proc Natl Acad Sci U S A 114: E10799–E10808. https://doi.org/10.1073/pnas.1706281114
- Choe S-K, Kim C-H (2023) Zebrafish: A Powerful Model for Genetics and Genomics. Int J Mol Sci 24: 8169. https://doi.org/10.3390/ijms24098169
- Chen Y, Zhang S, Chai R, Li H (2019) Hair Cell Regeneration. Adv Exp Med Biol 1130: 1–16. https://doi.org/10.1007/978-981-13-6123-4_1
- Schmidt R, Strähle U, Scholpp S (2013) Neurogenesis in zebrafish – from embryo to adult. Neural Develop 8: 3. https://doi.org/10.1186/1749-8104-8-3
- Chang W, Pedroni A, Bertuzzi M, Kizil C, Simon A, Ampatzis K (2021) Locomotion dependent neuron-glia interactions control neurogenesis and regeneration in the adult zebrafish spinal cord. Nat Commun 12: 4857. https://doi.org/10.1038/s41467-021-25052-1
- Pedersen BK (2019) Physical activity and muscle-brain crosstalk. Nat Rev Endocrinol 15: 383–392. https://doi.org/10.1038/s41574-019-0174-x
- Lucini C, D’Angelo L, Cacialli P, Palladino A, de Girolamo P (2018) BDNF, Brain, and Regeneration: Insights from Zebrafish. Int J Mol Sci 19: 3155. https://doi.org/10.3390/ijms19103155
- Yu Y, Schachner M (2013) Syntenin-a promotes spinal cord regeneration following injury in adult zebrafish. Eur J Neurosci 38(2): 2280-2289. https://doi.org/10.1111/ejn.12222
- Tian J, Shao J, Liu C, Hou H-Y, Chou C-W, Shboul M, Li G-Q, El-Khateeb M, Samarah OQ, Kou Y, Chen Y-H, Chen M-J, Lyu Z, Chen W-L, Chen Y-F, Sun Y-H, Liu Y-W (2019) Deficiency of lrp4 in zebrafish and human LRP4 mutation induce aberrant activation of Jagged–Notch signaling in fin and limb development. Cell Mol Life Sci CMLS 76: 163–178. https://doi.org/10.1007/s00018-018-2928-3
- Shah AN, Davey CF, Whitebirch AC, Miller AC, Moens CB (2015) Rapid reverse genetic screening using CRISPR in zebrafish. Nat Methods 12: 535–540. https://doi.org/10.1038/nmeth.3360
- Ogino K, Hirata H (2016) Defects of the Glycinergic Synapse in Zebrafish. Front Mol Neurosci 9: 50. https://doi.org/10.3389/fnmol.2016.00050
- Aramaki S, Hatta K (2006) Visualizing neurons one-by-one in vivo: optical dissection and reconstruction of neural networks with reversible fluorescent proteins. Dev Dyn 235: 2192–2199. https://doi.org/10.1002/dvdy.20826
- Wiegert JS, Bengtson CP, Bading H (2007) Diffusion and not active transport underlies and limits ERK1/2 synapse-to-nucleus signaling in hippocampal neurons. J Biol Chem 282: 29621–29633. https://doi.org/10.1074/jbc.M701448200
- Takeuchi M, Matsuda K, Yamaguchi S, Asakawa K, Miyasaka N, Lal P, Yoshihara Y, Koga A, Kawakami K, Shimizu T, Hibi M (2015) Establishment of Gal4 transgenic zebrafish lines for analysis of development of cerebellar neural circuitry. Dev Biol 397: 1–17. https://doi.org/10.1016/j.ydbio.2014.09.030
- Sebe JY, Cho S, Sheets L, Rutherford MA, von Gersdorff H, Raible DW (2017) Ca2+-Permeable AMPARs Mediate Glutamatergic Transmission and Excitotoxic Damage at the Hair Cell Ribbon Synapse. J Neurosci Off J Soc Neurosci 37: 6162–6175. https://doi.org/10.1523/JNEUROSCI.3644-16.2017
- Kindt KS, Sheets L (2018) Transmission Disrupted: Modeling Auditory Synaptopathy in Zebrafish. Front Cell Dev Biol 6: 114. https://doi.org/10.3389/fcell.2018.00114
- Moser T, Starr A (2016) Auditory neuropathy–neural and synaptic mechanisms. Nat Rev Neurol 12: 135–149. https://doi.org/10.1038/nrneurol.2016.10
- Uribe PM, Villapando BK, Lawton KJ, Fang Z, Gritsenko D, Bhandiwad A, Sisneros JA, Xu J, Coffin AB (2018) Larval Zebrafish Lateral Line as a Model for Acoustic Trauma. eNeuro 5: ENEURO.0206-18.2018. https://doi.org/10.1523/ENEURO.0206-18.2018
- Prats E, Gómez-Canela C, Ben-Lulu S, Ziv T, Padrós F, Tornero D, Garcia-Reyero N, Tauler R, Admon A, Raldúa D (2017) Modelling acrylamide acute neurotoxicity in zebrafish larvae. Sci Rep 7: 13952. https://doi.org/10.1038/s41598-017-14460-3
- Meshalkina DA, N Kizlyk M, V Kysil E, Collier AD, Echevarria DJ, Abreu MS, Barcellos LJG, Song C, Warnick JE, Kyzar EJ, Kalueff AV (2018) Zebrafish models of autism spectrum disorder. Exp Neurol 299: 207–216. https://doi.org/10.1016/j.expneurol.2017.02.004
- Bacila I, Cunliffe VT, Krone NP (2021) Interrenal development and function in zebrafish. Mol Cell Endocrinol 535: 111372. https://doi.org/10.1016/j.mce.2021.111372
- Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn Off Publ Am Assoc Anat 203: 253–310. https://doi.org/10.1002/aja.1002030302
- Hoon M, Okawa H, Della Santina L, Wong ROL (2014) Functional architecture of the retina: development and disease. Prog Retin Eye Res 42: 44–84. https://doi.org/10.1016/j.preteyeres.2014.06.003
- Damo JLK, Boiangiu RS, Brinza I, Kenko Djoumessi LB, Rebe RN, Kamleu BN, Guedang SDN, Camdi GW, Bouvourné P, Keugong EW, Ngatanko HHA, Cioanca O, Hancianu M, Foyet HS, Hritcu L (2022) Neuroprotective Potential of Guiera senegalensis (Combretaceae) Leaf Hydroethanolic Extract against Cholinergic System Dysfunctions and Oxidative Stress in Scopolamine-Induced Cognitive Impairment in Zebrafish (Danio rerio). Plants Basel Switz 11: 1149. https://doi.org/10.3390/plants11091149
- Boiangiu RS, Mihasan M, Gorgan DL, Stache BA, Hritcu L (2021) Anxiolytic, Promnesic, Anti-Acetylcholinesterase and Antioxidant Effects of Cotinine and 6-Hydroxy-L-Nicotine in Scopolamine-Induced Zebrafish (Danio rerio) Model of Alzheimer’s Disease. Antioxid Basel Switz 10: 212. https://doi.org/10.3390/antiox10020212
- Kaur K, Narang RK, Singh S (2022) AlCl3 induced learning and memory deficit in zebrafish. Neurotoxicology 92: 67–76. https://doi.org/10.1016/j.neuro.2022.07.004
- Kodera K, Matsui H (2022) Zebrafish, Medaka and Turquoise Killifish for Understanding Human Neurodegenerative/Neurodevelopmental Disorders. Int J Mol Sci 23: 1399. https://doi.org/10.3390/ijms23031399
- Orger MB, de Polavieja GG (2017) Zebrafish Behavior: Opportunities and Challenges. Annu Rev Neurosci 40: 125–147. https://doi.org/10.1146/annurev-neuro-071714-033857
- Vaz R, Edwards S, Dueñas-Rey A, Hofmeister W, Lindstrand A (2023) Loss of ctnnd2b affects neuronal differentiation and behavior in zebrafish. Front Neurosci 17: 1205653. https://doi.org/10.3389/fnins.2023.1205653
- Donta MS, Srivastava Y, McCrea PD (2022) Delta-Catenin as a Modulator of Rho GTPases in Neurons. Front Cell Neurosci 16: 939143. https://doi.org/10.3389/fncel.2022.939143
- Arikkath J, Peng I-F, Ng YG, Israely I, Liu X, Ullian EM, Reichardt LF (2009) Delta-catenin regulates spine and synapse morphogenesis and function in hippocampal neurons during development. J Neurosci Off J Soc Neurosci 29: 5435–5442. https://doi.org/10.1523/JNEUROSCI.0835-09.2009
- Dykens EM, Clarke DJ (1997) Correlates of maladaptive behavior in individuals with 5p- (cri du chat) syndrome. Dev Med Child Neurol 39: 752–756. https://doi.org/10.1111/j.1469-8749.1997.tb07377.x
- Constantin L, Poulsen RE, Scholz LA, Favre-Bulle IA, Taylor MA, Sun B, Goodhill GJ, Vanwalleghem GC, Scott EK (2020) Altered brain-wide auditory networks in a zebrafish model of fragile X syndrome. BMC Biol 18: 125. https://doi.org/10.1186/s12915-020-00857-6
- Wu Y-J, Hsu M-T, Ng M-C, Amstislavskaya TG, Tikhonova MA, Yang Y-L, Lu K-T (2017) Fragile X Mental Retardation-1 Knockout Zebrafish Shows Precocious Development in Social Behavior. Zebrafish 14: 438–443. https://doi.org/10.1089/zeb.2017.1446
- Barthelson K, Baer L, Dong Y, Hand M, Pujic Z, Newman M, Goodhill GJ, Richards RI, Pederson SM, Lardelli M (2021) Zebrafish Chromosome 14 Gene Differential Expression in the fmr1 h u2787 Model of Fragile X Syndrome. Front Genet 12: 625466. https://doi.org/10.3389/fgene.2021.625466
- Richter JD, Zhao X (2021) The molecular biology of FMRP: new insights into fragile X syndrome. Nat Rev Neurosci 22: 209–222. https://doi.org/10.1038/s41583-021-00432-0
- Walker LJ, Roque RA, Navarro MF, Granato M (2021) Agrin/Lrp4 signal constrains MuSK-dependent neuromuscular synapse development in appendicular muscle. Dev Camb Engl 148: dev199790. https://doi.org/10.1242/dev.199790
- Durmaz AA, Karaca E, Demkow U, Toruner G, Schoumans J, Cogulu O (2015) Evolution of Genetic Techniques: Past, Present, and Beyond. BioMed Res Int 2015: 461524. https://doi.org/10.1155/2015/461524
- Esposito G, Tremolaterra MR, Savarese M, Spiniello M, Patrizio MP, Lombardo B, Pastore L, Salvatore F, Carsana A (2018) Unraveling unusual X-chromosome patterns during fragile-X syndrome genetic testing. Clin Chim Acta Int J Clin Chem 476: 167–172. https://doi.org/10.1016/j.cca.2017.11.016
- Molloy CJ, Cooke J, Gatford NJF, Rivera-Olvera A, Avazzadeh S, Homberg JR, Grandjean J, Fernandes C, Shen S, Loth E, Srivastava DP, Gallagher L (2023) Bridging the translational gap: what can synaptopathies tell us about autism? Front Mol Neurosci 27(16): 1191323. https://doi.org/10.3389/fnmol.2023.1191323
- Cho S-J, Park E, Baker A, Reid AY (2021) Post-Traumatic Epilepsy in Zebrafish Is Drug-Resistant and Impairs Cognitive Function. J Neurotrauma 38: 3174–3183. https://doi.org/10.1089/neu.2021.0156
- Spoto G, Valentini G, Saia MC, Butera A, Amore G, Salpietro V, Nicotera AG, Di Rosa G (2022) Synaptopathies in Developmental and Epileptic Encephalopathies: A Focus on Pre-synaptic Dysfunction. Front Neurol 13: 826211. https://doi.org/10.3389/fneur.2022.826211
- Di Miceli M, Bosch-Bouju C, Layé S (2020) PUFA and their derivatives in neurotransmission and synapses: a new hallmark of synaptopathies. Proc Nutr Soc 1–16. https://doi.org/10.1017/S0029665120000129
- Taoufik E, Kouroupi G, Zygogianni O, Matsas R (2018) Synaptic dysfunction in neurodegenerative and neurodevelopmental diseases: an overview of induced pluripotent stem-cell-based disease models. Open Biol 8: 180138. https://doi.org/10.1098/rsob.180138
- Clapcote SJ (2022) How can we obtain truly translational mouse models to improve clinical outcomes in schizophrenia? Dis Model Mech 15: dmm049970. https://doi.org/10.1242/dmm.049970
- Pașca SP (2018) The rise of three-dimensional human brain cultures. Nature 553: 437–445. https://doi.org/10.1038/nature25032
- Mitoma H, Manto M (2023) Advances in the Pathogenesis of Auto-antibody-Induced Cerebellar Synaptopathies. Cerebellum Lond Engl 22: 129–147. https://doi.org/10.1007/s12311-021-01359-z
- Pozzi D, Menna E, Canzi A, Desiato G, Mantovani C, Matteoli M (2018) The Communication Between the Immune and Nervous Systems: The Role of IL-1β in Synaptopathies. Front Mol Neurosci 11: 111. https://doi.org/10.3389/fnmol.2018.00111
Supplementary files
