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Impairments of cerebellar structure and function in a zebrafish KO of neuropsychiatric risk gene znf536.

التفاصيل البيبلوغرافية
العنوان: Impairments of cerebellar structure and function in a zebrafish KO of neuropsychiatric risk gene znf536.
المؤلفون: Kim TY; Department of Biology, Chungnam National University, Daejeon, 34134, South Korea., Roychaudhury A; Department of Biology, Chungnam National University, Daejeon, 34134, South Korea., Kim HT; Soonchunhyang Institute of Medi-bio Science (SIMS), Soonchunhyang University, Cheonan, 31151, South Korea., Choi TI; Department of Biology, Chungnam National University, Daejeon, 34134, South Korea., Baek ST; Department of Life Sciences, Pohang University of Science and Technology (POSTECH), Pohang, 37673, South Korea., Thyme SB; Department of Neurobiology, University of Alabama at Birmingham, Birmingham, AL, USA. Summer.Thyme@umassmed.edu.; Department of Biochemistry and Molecular Biotechnology, UMass Chan Medical School, Worcester, MA, USA. Summer.Thyme@umassmed.edu., Kim CH; Department of Biology, Chungnam National University, Daejeon, 34134, South Korea. zebrakim@cnu.ac.kr.
المصدر: Translational psychiatry [Transl Psychiatry] 2024 Feb 08; Vol. 14 (1), pp. 82. Date of Electronic Publication: 2024 Feb 08.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: United States NLM ID: 101562664 Publication Model: Electronic Cited Medium: Internet ISSN: 2158-3188 (Electronic) Linking ISSN: 21583188 NLM ISO Abbreviation: Transl Psychiatry Subsets: MEDLINE
أسماء مطبوعة: Original Publication: New York, NY : Nature Pub. Group
مواضيع طبية MeSH: Zebrafish*/genetics , Zebrafish*/metabolism , Cerebellum*/metabolism, Animals ; Animals, Genetically Modified/metabolism ; Zebrafish Proteins/genetics ; Zebrafish Proteins/metabolism ; Brain/metabolism
مستخلص: Genetic variants in ZNF536 contribute to the risk for neuropsychiatric disorders such as schizophrenia, autism, and others. The role of this putative transcriptional repressor in brain development and function is, however, largely unknown. We generated znf536 knockout (KO) zebrafish and studied their behavior, brain anatomy, and brain function. Larval KO zebrafish showed a reduced ability to compete for food, resulting in decreased total body length and size. This phenotype can be rescued by segregating the homozygous KO larvae from their wild-type and heterozygous siblings, enabling studies of adult homozygous KO animals. In adult KO zebrafish, we observed significant reductions in anxiety-like behavior and social interaction. These znf536 KO zebrafish have decreased cerebellar volume, corresponding to decreased populations of specific neuronal cells, especially in the valvular cerebelli (Va). Finally, using a Tg[mbp:mgfp] line, we identified a previously undetected myelin structure located bilaterally within the Va, which also displayed a reduction in volume and disorganization in KO zebrafish. These findings indicate an important role for ZNF536 in brain development and implicate the cerebellum in the pathophysiology of neuropsychiatric disorders.
(© 2024. The Author(s).)
References: Owen MJ, Sawa A. Mortensen pb. Schizophrenia Lancet. 2016;388:86–97. (PMID: 2677791710.1016/S0140-6736(15)01121-6)
Schizophrenia Working Group of the Psychiatric Genomics Consortium. Biological insights from 108 schizophrenia-associated genetic loci. Nature. 2014;511:421–7.
Trubetskoy V, Pardiñas AF, Qi T, Panagiotaropoulou G, Awasthi S, Bigdeli TB, et al. Mapping genomic loci implicate genes and synaptic biology in schizophrenia. Nature. 2022;604:502–8. (PMID: 35396580939246610.1038/s41586-022-04434-5)
Pocklington AJ, Rees E, Walters JT, Han J, Kavanagh DH, Chambert KD, et al. Novel findings from CNVs implicate inhibitory and excitatory signalling complexes in schizophrenia. Neuron. 2015;86:1203–14. (PMID: 26050040446018710.1016/j.neuron.2015.04.022)
Singh T, Poterba T, Curtis D, Akil H, Al Eissa M, Barchas JD, et al. Rare coding variants in ten genes confer substantial risk for schizophrenia. Nature. 2022;604:509–16. (PMID: 35396579980580210.1038/s41586-022-04556-w)
Alerts GN, Get RS. Effect of chlorpromazine or haloperidol on formation of 3-methoxytyramine and normetanephrine in mouse brain. Acta Pharmacol Toxicol. 1963;20:140–4. (PMID: 10.1111/j.1600-0773.1963.tb01730.x)
Van Rossum JM. The significance of dopamine-receptor blockade for the mechanism of action of neuroleptic drugs. Arch Int Pharmacodyn Ther. 1996;160:492–4.
Satterstrom FK, Walters RK, Singh T, Wigdor EM, Lescai F, Demontis D, et al. Autism spectrum disorder and attention deficit hyperactivity disorder have a similar burden of rare protein-truncating variants. Nat Neurosci. 2019;22:1961–5. (PMID: 31768057688469510.1038/s41593-019-0527-8)
Turner TN, Coe BP, Dickel DE, Hoekzema K, Nelson BJ, Zody MC, et al. Genomic patterns of de novo mutation in simplex autism. Cell. 2017;171:710–22. (PMID: 28965761567971510.1016/j.cell.2017.08.047)
Winham SJ, Cuellar-Barboza AB, McElroy SL, Oliveros A, Crow S, Colby CL, et al. Bipolar disorder with comorbid binge eating history: a genome-wide association study implicates APOB. J Affect Disord. 2014;165:151–8. (PMID: 24882193422414610.1016/j.jad.2014.04.026)
Lin E, Kuo PH, Liu YL, Yu YW, Yang AC, Tsai SJ. A deep learning approach for predicting antidepressant response in major depression using clinical and genetic biomarkers. Front Psychiatry. 2018;9:290. (PMID: 30034349604386410.3389/fpsyt.2018.00290)
Dmitrzak-Weglarz M, Paszynska E, Bilska K, Szczesniewska P, Bryl E, Duda J, et al. Common and unique genetic background between attention-deficit/hyperactivity disorder and excessive body weight. Genes. 2021;12:1407. (PMID: 34573389846491710.3390/genes12091407)
Qin Z, Ren F, Xu X, Ren Y, Li H, Wang Y, et al. ZNF536, a novel zinc finger protein specifically expressed in the brain, negatively regulates neuron differentiation by repressing retinoic acid-induced gene transcription. Mol Cell Biol. 2009;29:3633–43. (PMID: 19398580269876210.1128/MCB.00362-09)
Thyme SB, Pieper LM, Li EH, Pandey S, Wang Y, Morris NS, et al. Phenotypic landscape of schizophrenia-associated genes defines candidates and their shared functions. Cell. 2019;177:478–91. (PMID: 30929901649445010.1016/j.cell.2019.01.048)
Kalueff AV, Stewart AM, Gerlai R. Zebrafish as an emerging model for studying complex brain disorders. Trend Pharmacol Sci. 2014;35:63–75. (PMID: 10.1016/j.tips.2013.12.002)
Kim OH, Cho HJ, Han E, Hong TI, Ariyasiri K, Choi JH, et al. Zebrafish knockout of Down syndrome gene, DYRK1A, shows social impairments relevant to autism. Mol Autism. 2017;8:1–4.
Choi JH, Jeong YM, Kim S, Lee B, Ariyasiri K, Kim HT, et al. Targeted knockout of a chemokine-like gene increases anxiety and fear responses. Proc Natl Acad Sci USA. 2018;115:E1041–50. (PMID: 29339520579831910.1073/pnas.1707663115)
Geng Y, Zhang T, Alonzo IG, Godar SC, Yates C, Pluimer BR, et al. Top2a promotes the development of social behavior via PRC2 and H3K27me3. Sci Adv. 2022;8:eabm7069. (PMID: 36417527968371410.1126/sciadv.abm7069)
May M, Hwang KS, Miles J, Williams C, Niranjan T, Kahler SG, et al. ZC4H2, an XLID gene, is required for the generation of a specific subset of CNS interneurons. Hum Mol Genet. 2015;24:4848–61. (PMID: 26056227452748810.1093/hmg/ddv208)
Lee YR, Khan K, Armfield-Uhas K, Srikanth S, Thompson NA, Pardo M, et al. Mutations in FAM50A suggest that Armfield XLID syndrome is a spliceosomopathy. Nat Commun. 2020;11:3698. (PMID: 32703943737824510.1038/s41467-020-17452-6)
Lee YR, Kim SH, Ben-Mahmoud A, Kim OH, Choi TI, Lee KH, et al. Eif2b3 mutants recapitulate phenotypes of vanishing white matter disease and validate novel disease alleles in zebrafish. Hum Mol Genet. 2021;30:331–42. (PMID: 3351744910.1093/hmg/ddab033)
Mendes HW, Neelakantan U, Liu Y, Fitzpatrick SE, Chen T, Wu W, et al. High-throughput functional analysis of autism genes in zebrafish identifies convergence in dopaminergic and neuroimmune pathways. Cell Rep. 2023;42:112243. (PMID: 10.1016/j.celrep.2023.112243)
Geng Y, Peterson RT. The zebrafish subcortical social brain as a model for studying social behavior disorders. Dis Model Mech. 2019;12:dmm039446. (PMID: 31413047673794510.1242/dmm.039446)
Bae YK, Kani S, Shimizu T, Tanabe K, Nojima H, Kimura Y, et al. Anatomy of zebrafish cerebellum and screen for mutations affecting its development. Dev Biol. 2009;330:406–26. (PMID: 1937173110.1016/j.ydbio.2009.04.013)
Thisse B, Heyer V, Lux A, Alunni V, Degrave A, Seiliez I, et al. Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. In: Methods in cell biology. vol. 77. Academic Press; 2004. pp. 505–19.
Kirshenbaum AP, Chabot E, Gibney N. Startle, pre-pulse sensitization, and habituation in zebrafish. J Neurosci Method. 2019;313:54–9. (PMID: 10.1016/j.jneumeth.2018.12.017)
Strähle U, Scholz S, Geisler R, Greiner P, Hollert H, Rastegar S, et al. Zebrafish embryos as an alternative to animal experiments—a commentary on the definition of the onset of protected life stages in animal welfare regulations. Reprod Toxicol. 2012;33:128–32. (PMID: 2172662610.1016/j.reprotox.2011.06.121)
Cachat J, Stewart A, Grossman L, Gaikwad S, Kadri F, Chung KM, et al. Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. Nat Protocol. 2010;5:1786–99. (PMID: 10.1038/nprot.2010.140)
Egan RJ, Bergner CL, Hart PC, Cachat JM, Canavello PR, Elegante MF, et al. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res. 2009;205:38–44. (PMID: 19540270292290610.1016/j.bbr.2009.06.022)
Chanin S, Fryar C, Varga D, Raymond J, Kyzar E, Enriquez J, et al. Assessing startle responses and their habituation in adult zebrafish. Zebrafish Protocol Neurobehav Res. 2012;66:287–300. (PMID: 10.1007/978-1-61779-597-8_22)
Ro Y, Noronha M, Mirza B, Ansari R, Gerlai R. The Tapping assay: a simple method to induce fear responses in zebrafish. Behav Res Method 2021;16:1–4.
Miller N, Gerlai R. Quantification of shoaling behaviour in zebrafish (Danio rerio). Behav Brain Res. 2007;184:157–66. (PMID: 1770752210.1016/j.bbr.2007.07.007)
Wright D, Krause J. Repeated measures of shoaling tendency in zebrafish (Danio rerio) and other small teleost fishes. Nat Protocol. 2006;1:1828–31. (PMID: 10.1038/nprot.2006.287)
Buske C, Gerlai R. Shoaling develops with age in Zebrafish (Danio rerio). Progr Neuro-Psychopharmacol Biol Psychiatry. 2011;35:1409–15. (PMID: 10.1016/j.pnpbp.2010.09.003)
Gerlai R. Social behavior of zebrafish: from synthetic images to biological mechanisms of shoaling. J Neurosci Methods. 2014;234:59–65. (PMID: 2479340010.1016/j.jneumeth.2014.04.028)
Reyhanian N, Volkova K, Hallgren S, Bollner T, Olsson PE, Olsén H, et al. 17α-Ethinyl estradiol affects anxiety and shoaling behavior in adult male zebra fish (Danio rerio). Aqua Toxicol. 2011;105:41–8. (PMID: 10.1016/j.aquatox.2011.05.009)
Miller N, Greene K, Dydinski A, Gerlai R. Effects of nicotine and alcohol on zebrafish (Danio rerio) shoaling. Behav Brain Res. 2013;240:192–6. (PMID: 2321996610.1016/j.bbr.2012.11.033)
Dreosti E, Lopes G, Kampff AR, Wilson SW. Development of social behavior in young zebrafish. Front Neural Circuit. 2015;9:39. (PMID: 10.3389/fncir.2015.00039)
Saverino C, Gerlai R. The social zebrafish: behavioural responses to conspecific, heterospecific, and computer animated fish. Behav Brain Res. 2008;191:77–87. (PMID: 18423643248643810.1016/j.bbr.2008.03.013)
Mahabir S, Chatterjee D, Buske C, Gerlai R. Maturation of shoaling in two zebrafish strains: a behavioral and neurochemical analysis. Behav Brain Rese. 2013;247:1–8. (PMID: 10.1016/j.bbr.2013.03.013)
Miyamura Y, Nakayasu H. Zonal distribution of purkinje cells in the zebrafish cerebellum: analysis by means of a specific monoclonal antibody. Cell Tissue Res. 2001;305:299–305. (PMID: 1157208310.1007/s004410100421)
Tanabe K, Kani S, Shimizu T, Bae YK, Abe T, Hibi M. Atypical protein kinase C regulates primary dendrite specification of cerebellar purkinje cells by localizing Golgi apparatus. J Neurosci. 2010;30:16983–92. (PMID: 21159968663491510.1523/JNEUROSCI.3352-10.2010)
Seeman P. Schizophrenia and dopamine receptors. Eur Neuropsychopharmacol. 2013;23:999–1009. (PMID: 2386035610.1016/j.euroneuro.2013.06.005)
Jung SH, Kim S, Chung AY, Kim HT, So JH, Ryu J, et al. Visualization of myelination in GFP‐transgenic zebrafish. Dev Dyn. 2010;239:592–7. (PMID: 1991888210.1002/dvdy.22166)
Bielsky IF, Hu SB, Szegda KL, Westphal H, Young LJ. Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology. 2004;29:483–93. (PMID: 1464748410.1038/sj.npp.1300360)
Egashira N, Tanoue A, Matsuda T, Koushi E, Harada S, Takano Y, et al. Impaired social interaction and reduced anxiety-related behaviour in vasopressin V1a receptor knockout mice. Behav Brain Res. 2007;178:123–7. (PMID: 1722768410.1016/j.bbr.2006.12.009)
Liu CX, Li CY, Hu CC, Wang Y, Lin J, Jiang YH, et al. CRISPR/Cas9-induced shank3b mutant zebrafish display autism-like behaviors. Mol Autism. 2018;9:1–3. (PMID: 10.1186/s13229-018-0204-x)
Ruzzo EK, Pérez-Cano L, Jung JY, Wang LK, Kashef-Haghighi D, Hartl C, et al. Inherited and de novo genetic risk for autism impacts shared networks. Cell. 2019;178:850–66. (PMID: 31398340710290010.1016/j.cell.2019.07.015)
Bohne P, Mourabit DB, Josten M, Mark MD. Cognitive deficits in episodic ataxia type 2 mouse models. Hum Mol Genet. 2021;30:1811–32. (PMID: 34077522844444910.1093/hmg/ddab149)
Russell CJ, Bell CC. Neuronal responses to electrosensory input in mormyrid valvula cerebelli. J Neurophysiol. 1978;41:1495–510. (PMID: 73128710.1152/jn.1978.41.6.1495)
Van Overwalle F, Baetens K, Mariën P, Vandekerckhove M. Social cognition and the cerebellum: a meta-analysis of over 350 fMRI studies. Neuroimage. 2014;86:554–72. (PMID: 2407620610.1016/j.neuroimage.2013.09.033)
Schmahmann JD, Guell X, Stoodley CJ, Halko MA. The theory and neuroscience of cerebellar cognition. Ann Rev Neurosci. 2019;42:337–64. (PMID: 3093910110.1146/annurev-neuro-070918-050258)
Wang SS, Kloth AD, Badura A. The cerebellum, sensitive periods, and autism. Neuron. 2014;83:518–32. (PMID: 25102558413547910.1016/j.neuron.2014.07.016)
Andreasen NC, Pierson R. The role of the cerebellum in schizophrenia. Biol Psychiatry. 2008;64:81–8. (PMID: 18395701317549410.1016/j.biopsych.2008.01.003)
Maloku E, Covelo IR, Hanbauer I, Guidotti A, Kadriu B, Hu Q, et al. Lower number of cerebellar purkinje neurons in psychosis is associated with reduced reelin expression. Proc Natl Acad Sci USA. 2010;107:4407–11. (PMID: 20150511284012110.1073/pnas.0914483107)
Tran KD, Smutzer GS, Doty RL, Arnold SE. Reduced purkinje cell size in the cerebellar vermis of elderly patients with schizophrenia. Am J Psychiatr. 1998;155:1288–90. (PMID: 973455810.1176/ajp.155.9.1288)
Skefos J, Cummings C, Enzer K, Holiday J, Weed K, Levy E, et al. Regional alterations in purkinje cell density in patients with autism. PLoS ONE. 2014;9:e81255. (PMID: 24586223393333310.1371/journal.pone.0081255)
Shevelkin AV, Terrillion CE, Abazyan BN, Kajstura TJ, Jouroukhin YA, Rudow GL, et al. Expression of mutant DISC1 in Purkinje cells increases their spontaneous activity and impairs cognitive and social behaviors in mice. Neurobiol Dis. 2017;103:144–53. (PMID: 28392471544244710.1016/j.nbd.2017.04.008)
Veleanu M, Urrieta-Chávez B, Sigoillot SM, Paul MA, Usardi A, Iyer K, et al. Modified climbing fiber/Purkinje cell synaptic connectivity in the cerebellum of the neonatal phencyclidine model of schizophrenia. Proc Natl Acad Sci USA. 2022;119:e2122544119. (PMID: 35588456917378310.1073/pnas.2122544119)
Tsai PT, Hull C, Chu Y, Greene-Colozzi E, Sadowski AR, Leech JM, et al. Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Nature. 2012;488:647–51. (PMID: 22763451361542410.1038/nature11310)
Magnotta VA, Adix ML, Caprahan A, Lim K, Gollub R, Andreasen NC. Investigating connectivity between the cerebellum and thalamus in schizophrenia using diffusion tensor tractography: a pilot study. Psychiatry Res Neuroimaging. 2008;163:193–200. (PMID: 10.1016/j.pscychresns.2007.10.005)
Chang X, Jia X, Wang Y, Dong D. Alterations of cerebellar white matter integrity and associations with cognitive impairments in schizophrenia. Front Psychiatry. 2022;13:993866. (PMID: 36226106954914510.3389/fpsyt.2022.993866)
Kebschull JM, Casoni F, Consalez GG, Goldowitz D, Hawkes R, Ruigrok TJ, et al. Cerebellum lecture: the cerebellar nuclei—core of the cerebellum. Cerebellum. 2023;13:1–58.
Kebschull JM, Richman EB, Ringach N, Friedmann D, Albarran E, Kolluru SS, et al. Cerebellar nuclei evolved by repeatedly duplicating a conserved cell-type set. Science. 2020;370:eabd5059. (PMID: 33335034851050810.1126/science.abd5059)
Lee YR, Thomas M, Roychaudhury A, Skinner C, Maconachie G, Crosier M, et al. Eye movement defects in KO zebrafish reveals SRPK3 as a causative gene for an X-linked intellectual disability. Res Sq. 20:rs.3.rs-2683050. https://doi.org/10.21203/rs.3.rs-2683050/v1 (2023).
معلومات مُعتمدة: R00 MH110603 United States MH NIMH NIH HHS
المشرفين على المادة: 0 (Zebrafish Proteins)
تواريخ الأحداث: Date Created: 20240208 Date Completed: 20240214 Latest Revision: 20240214
رمز التحديث: 20240214
مُعرف محوري في PubMed: PMC10853220
DOI: 10.1038/s41398-024-02806-1
PMID: 38331943
قاعدة البيانات: MEDLINE
الوصف
تدمد:2158-3188
DOI:10.1038/s41398-024-02806-1