1. На главную
  2. Электронные версии
  3. Российский физиологический журнал им. И.М. Сеченова
  4. T. 109, № 11, 2023

Российский физиологический журнал им. И.М. Сеченова, 2023, T. 109, № 11, стр. 1601-1616

Экспериментальные модели синаптопатий на основе рыб зебраданио

А. С. Лебедев 1, 2, 3, М. М. Котова 2, Н. П. Ильин 1, 3, Т. О. Колесникова 2, Д. С. Галстян 1, 3, 4, Т. В. Вьюнова 7, Е. В. Петерсен 5, А. В. Калуев 1, 2, 3, 4, 6, *

1 Научный центр мирового уровня “Центр персонализированной медицины”, Национальный медицинский исследовательский центр им. В.А. Алмазова МЗ РФ
Санкт-Петербург, Россия

2 Направление “Нейробиология”, Научный центр генетики и наук о жизни, Научно-технологический университет “Сириус”
Федеральная территория Сириус, Россия

3 Институт трансляционной биомедицины, Санкт-Петербургский государственный университет
Санкт-Петербург, Россия

4 Российский научный центр радиологии и хирургических технологий им. акад. А.М. Гранова МЗ РФ
Санкт-Петербург, Россия

5 Московский физико-технический институт
Москва, Россия

6 Уральский федеральный университет
Екатеринбург, Россия

7 Институт молекулярной генетики Национального исследовательского центра “Курчатовский институт”
Москва, Россия

* E-mail: avkalueff@gmail.com

Поступила в редакцию 23.08.2023
После доработки 04.10.2023
Принята к публикации 04.10.2023

Аннотация

Синаптопатии – разнородная группа неврологических заболеваний человека, вызванных нарушением структуры и функций синапсов. К распространенным синаптопатиям относятся эпилепсия, расстройства аутистического спектра, ряд аутоимунных заболеваний и слуховые синаптопатии. Патогенез синаптопатий обусловлен различными факторами, включая генетические и средовые. Тем не менее недостаток знаний об их системных механизмах и неэффективность терапии подчеркивают актуальность дальнейших клинических и экспериментальных исследований синаптопатий. В работе обсуждаются существующие экспериментальные модели синаптопатий на животных, с акцентом на использование альтернативных модельных объектов – рыб зебраданио (Danio rerio, zebrafish), а также рассматриваются возможные новые направления для исследований. В целом, зебраданио служит перспективным организмом для моделирования широкого спектра синаптопатий, дополняя и расширяя существующие модели на основе грызунов.

Ключевые слова: синаптическая передача, синаптопатии, патогенез, грызуны, рыбы, экспериментальные модели

Список литературы

  1. Grant SGN (2012) Synaptopathies: diseases of the synaptome. Curr Opin Neurobiol 22: 522–529. https://doi.org/10.1016/j.conb.2012.02.002

  2. Crisp SJ, Kullmann DM, Vincent A (2016) Autoimmune synaptopathies. Nat Rev Neurosci 17: 103–117. https://doi.org/10.1038/nrn.2015.27

  3. 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

  4. 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

  5. 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

  6. 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

  7. 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

  8. 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

  9. 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

  10. 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

  11. 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

  12. 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

  13. 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

  14. Cherington M (2004) Botulism: update and review. Semin Neurol 24: 155–163. https://doi.org/10.1055/s-2004-830901

  15. 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

  16. 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

  17. 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

  18. 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

  19. 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

  20. Papazian O, Alfonso I (2009) Juvenile myasthenia gravis. Medicina (Mex) 69:71–83

  21. Claytor B, Cho S-M, Li Y (2023) Myasthenic crisis. Muscle Nerve 68: 8–19. https://doi.org/10.1002/mus.27832

  22. 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

  23. 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

  24. Li D, Tansley SL (2019) Juvenile Dermatomyositis-Clinical Phenotypes. Curr Rheumatol Rep 21: 74. https://doi.org/10.1007/s11926-019-0871-4

  25. 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

  26. 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

  27. 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

  28. 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

  29. 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

  30. 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

  31. 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

  32. 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

  33. 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

  34. 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

  35. 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

  36. Keithley EM (2020) Pathology and mechanisms of cochlear aging. J Neurosci Res 98: 1674–1684. https://doi.org/10.1002/jnr.24439

  37. 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

  38. 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

  39. 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

  40. 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

  41. 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

  42. 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

  43. 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

  44. 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

  45. 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

  46. 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

  47. 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

  48. Pedersen BK (2019) Physical activity and muscle-brain crosstalk. Nat Rev Endocrinol 15: 383–392. https://doi.org/10.1038/s41574-019-0174-x

  49. 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

  50. 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

  51. 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

  52. 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

  53. 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

  54. 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

  55. 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

  56. 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

  57. 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

  58. 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

  59. 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

  60. 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

  61. 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

  62. 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

  63. 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

  64. 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

  65. 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

  66. 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

  67. 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

  68. 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

  69. 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

  70. 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

  71. 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

  72. 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

  73. 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

  74. 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

  75. 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

  76. 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

  77. 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

  78. 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

  79. 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

  80. 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

  81. 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

  82. 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

  83. 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

  84. 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

  85. 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

  86. 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

  87. 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

  88. Pașca SP (2018) The rise of three-dimensional human brain cultures. Nature 553: 437–445. https://doi.org/10.1038/nature25032

  89. 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

  90. 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

Дополнительные материалы отсутствуют.

Инструменты

следующая статья выпуска предыдущая статья выпуска содержание выпуска

Российский физиологический журнал им. И.М. Сеченова

Архивы выпусков Информация о журнале Отправить рукопись в журнал