Deficiency of the ywhaz gene, involved in neurodevelopmental disorders, alters brain activity and behaviour in zebrafish.


Journal

Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835

Informations de publication

Date de publication:
09 2022
Historique:
received: 02 10 2021
accepted: 12 04 2022
revised: 06 04 2022
pubmed: 3 5 2022
medline: 2 12 2022
entrez: 2 5 2022
Statut: ppublish

Résumé

Genetic variants in YWHAZ contribute to psychiatric disorders such as autism spectrum disorder and schizophrenia, and have been related to an impaired neurodevelopment in humans and mice. Here, we have used zebrafish to investigate the mechanisms by which YWHAZ contributes to neurodevelopmental disorders. We observed that ywhaz expression was pan-neuronal during developmental stages and restricted to Purkinje cells in the adult cerebellum, cells that are described to be reduced in number and size in autistic patients. We then performed whole-brain imaging in wild-type and ywhaz CRISPR/Cas9 knockout (KO) larvae and found altered neuronal activity and connectivity in the hindbrain. Adult ywhaz KO fish display decreased levels of monoamines in the hindbrain and freeze when exposed to novel stimuli, a phenotype that can be reversed with drugs that target monoamine neurotransmission. These findings suggest an important role for ywhaz in establishing neuronal connectivity during development and modulating both neurotransmission and behaviour in adults.

Identifiants

pubmed: 35501409
doi: 10.1038/s41380-022-01577-9
pii: 10.1038/s41380-022-01577-9
doi:

Substances chimiques

14-3-3 Proteins 0
YWHAZ protein, human 0
Zebrafish Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3739-3748

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Jia Y, Yu X, Zhang B, Yuan Y, Xu Q, Shen Y, et al. An association study between polymorphisms in three genes of 14-3-3 (tyrosine 3-monooxygenase/tryptophan 5-monooxygenase activation protein) family and paranoid schizophrenia in northern Chinese population. Eur Psychiatry. 2004;19:377–9.
pubmed: 15363479
Torrico B, Antón-Galindo E, Fernàndez-Castillo N, Rojo-Francàs E, Ghorbani S, Pineda-Cirera L, et al. Involvement of the 14-3-3 gene family in autism spectrum disorder and schizophrenia: genetics, transcriptomics and functional analyses. J Clin Med. 2020;9:1851.
pubmed: 32545830 pmcid: 7356291
Toma C, Torrico B, Hervás A, Valdés-Mas R, Tristán-Noguero A, Padillo V, et al. Exome sequencing in multiplex autism families suggests a major role for heterozygous truncating mutations. Mol Psychiatry. 2014;19:784–90.
pubmed: 23999528
Middleton FA, Peng L, Lewis DA, Levitt P, Mirnics K. Altered expression of 14-3-3 in the prefrontal cortex of subjects with schizophrenia. Neuropsychopharmacology. 2005;30:974–83.
pubmed: 15726117
English JA, Pennington K, Dunn MJ, Cotter DR. The neuroproteomics of schizophrenia. Biol Psychiatry. 2011;69:163–72.
pubmed: 20887976
Pagan C, Delorme R, Callebert J, Goubran-Botros H, Amsellem F, Drouot X, et al. The serotonin-N-acetylserotonin-melatonin pathway as a biomarker for autism spectrum disorders. Transl Psychiatry. 2014;4:e479.
pubmed: 25386956 pmcid: 4259991
Pagan C, Goubran-Botros H, Delorme R, Benabou M, Lemière N, Murray K, et al. Disruption of melatonin synthesis is associated with impaired 14-3-3 and miR-451 levels in patients with autism spectrum disorders. Sci Rep. 2017;7:2096.
pubmed: 28522826 pmcid: 5437096
Cornell B, Toyo-oka K. 14-3-3 proteins in brain development: neurogenesis, neuronal migration and neuromorphogenesis. Front Mol Neurosci. 2017;10:318.
pubmed: 29075177 pmcid: 5643407
Xu X, Jaehne EJ, Greenberg Z, McCarthy P, Saleh E, Parish CL, et al. 14-3-3ζ deficient mice in the BALB/c background display behavioural and anatomical defects associated with neurodevelopmental disorders. Sci Rep. 2015;5:12434.
pubmed: 26207352 pmcid: 4513550
Toyo-Oka K, Wachi T, Hunt RF, Baraban SC, Taya S, Ramshaw H, et al. 14-3-3Ε and Ζ regulate neurogenesis and differentiation of neuronal progenitor cells in the developing brain. J Neurosci. 2014;34:12168–81.
pubmed: 25186760 pmcid: 4152612
Jaehne EJ, Ramshaw H, Xu X, Saleh E, Clark SR, Schubert KO, et al. In-vivo administration of clozapine affects behaviour but does not reverse dendritic spine deficits in the 14-3-3ζ KO mouse model of schizophrenia-like disorders. Pharm Biochem Behav. 2015;138:1–8.
Cheah PS, Ramshaw HS, Thomas PQ, Toyo-Oka K, Xu X, Martin S, et al. Neurodevelopmental and neuropsychiatric behaviour defects arise from 14-3-3ζ deficiency. Mol Psychiatry. 2012;17:451–66.
pubmed: 22124272
Kalueff AV, Stewart AM, Gerlai R. Zebrafish as an emerging model for studying complex brain disorders. Trends Pharm Sci. 2014;35:63–75.
pubmed: 24412421
Norton W. Towards developmental models of psychiatric disorders in zebrafish. Front Neural Circuits. 2013;7:79.
pubmed: 23637652 pmcid: 3636468
Vaz R, Hofmeister W, Lindstrand A. Zebrafish models of neurodevelopmental disorders: limitations and benefits of current tools and techniques. Int J Mol Sci. 2019;20:1296.
pubmed: 30875831 pmcid: 6471844
Kozol RA, Abrams AJ, James DM, Buglo E, Yan Q, Dallman JE. Function over form: Modeling groups of inherited neurological conditions in zebrafish. Front Mol Neurosci. 2016;9:55.
pubmed: 27458342 pmcid: 4935692
Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods. 2013;10:413–20.
pubmed: 23524393
Vanwalleghem GC, Ahrens MB, Scott EK. Integrative whole-brain neuroscience in larval zebrafish. Curr Opin Neurobiol. 2018;50:136–45.
pubmed: 29486425
Olarte OE, Andilla J, Gualda EJ, Loza-Alvarez P. Light-sheet microscopy: a tutorial. Adv Opt Photonics. 2018;10:111–79.
Giovannucci A, Friedrich J, Gunn P, Kalfon J, Brown BL, Koay SA, et al. CaImAn an open-source tool for scalable calcium imaging data analysis. Elife. 2019;8:e38173.
pubmed: 30652683 pmcid: 6342523
Orlandi JG, Fernández-García S, Comella-Bolla A, Masana M, Barriga GG-D, Yaghoubi M, et al. NETCAL: an interactive platform for large-scale, NETwork and population dynamics analysis of CALcium imaging recordings (7.0.0 Open Beta). Zenodo. 2017: https://doi.org/10.5281/zenodo.1119026 .
Young AMJ. Increased extracellular dopamine in nucleus accumbens in response to unconditioned and conditioned aversive stimuli: Studies using 1 min microdialysis in rats. J Neurosci Methods. 2004;138:57–63.
pubmed: 15325112
Ahn AH, Dziennis S, Hawkes R, Herrup K. The cloning of zebrin II reveals its identity with aldolase C. Development. 1994;120:2081–90.
pubmed: 7925012
McFarland KA, Topczewska JM, Weidinger G, Dorsky RI, Appel B. Hh and Wnt signaling regulate formation of olig2+ neurons in the zebrafish cerebellum. Dev Biol. 2008;318:162–71.
pubmed: 18423594 pmcid: 2474464
Biechl D, Dorigo A, Köster RW, Grothe B, Wullimann MF. Eppur Si muove: Evidence for an external granular layer and possibly transit amplification in the teleostean cerebellum. Front Neuroanat. 2016;10:49.
pubmed: 27199681 pmcid: 4852188
Kai W, Kunwar KCJ, Elisa DV, Sunil P, Norbert G, Anne D, et al. Cysteine modification by ebselen reduces the stability and cellular levels of 14-3-3 proteins. Mol Pharmacol. 2021;100:155–69.
Molnár Z, Luhmann HJ, Kanold PO. Transient cortical circuits match spontaneous and sensory-driven activity during development. Science. 2020;370:eabb2153.
pubmed: 33060328 pmcid: 8050953
Marachlian E, Avitan L, Goodhill GJ, Sumbre G. Principles of functional circuit connectivity: Insights from spontaneous activity in the zebrafish optic tectum. Front Neural Circuits. 2018;12:46.
pubmed: 29977193 pmcid: 6021757
Avitan L, Pujic Z, Mölter J, Van De Poll M, Sun B, Teng H, et al. Spontaneous activity in the zebrafish tectum reorganizes over development and is influenced by visual experience. Curr Biol. 2017;27:2407–24.e4.
pubmed: 28781054
Momose-Sato Y, Sato K. Development of spontaneous activity in the avian hindbrain. Front Neural Circuits. 2016;10:63.
pubmed: 27570506 pmcid: 4981603
Aitken A. 14-3-3 proteins: a historic overview. Semin Cancer Biol. 2006;16:162–72.
pubmed: 16678438
Vaswani M, Linda FK, Ramesh S. Role of selective serotonin reuptake inhibitors in psychiatric disorders: a comprehensive review. Prog Neuro-Psychopharmacol. Biol Psychiatry. 2003;27:85–102.
Millan MJ, Maiofiss L, Cussac D, Audinot V, Boutin JA, Newman-Tancredi A. Differential actions of antiparkinson agents at multiple classes of monoaminergic receptor. I. A multivariate analysis of the binding profiles of 14 drugs at 21 native and cloned human receptor subtypes. J Pharm Exp Ther. 2002;303:791–804.
Packer A. Neocortical neurogenesis and the etiology of autism spectrum disorder. Neurosci Biobehav Rev. 2016;64:185–95.
pubmed: 26949225
Stoodley CJ. The cerebellum and neurodevelopmental disorders. Cerebellum. 2016;15:34–37.
pubmed: 26298473 pmcid: 4811332
van der Heijden ME, Gill JS, Sillitoe RV. Abnormal cerebellar development in autism spectrum disorders. Dev Neurosci. 2021;43:181–90.
pubmed: 33823515
Fatemi SH, Halt AR, Realmuto G, Earle J, Kist DA, Thuras P, et al. Purkinje cell size is reduced in cerebellum of patients with autism. Cell Mol Neurobiol. 2002;22:171–5.
pubmed: 12363198
Palmen SJMC, van Engeland H, Hof PR, Schmitz C. Neuropathological findings in autism. Brain. 2004;127:2572–83.
pubmed: 15329353
Bailey A, Luthert P, Dean A, Harding B, Janota I, Montgomery M, et al. A clinicopathological study of autism. Brain. 1998;121:889–905.
pubmed: 9619192
Skefos J, Cummings C, Enzer K, Holiday J, Weed K, Levy E. et al. Regional alterations in Purkinje cell density. PLoS One. 2014;9:e81255
pubmed: 24586223 pmcid: 3933333
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.
pubmed: 22763451 pmcid: 3615424
Kirkby LA, Sack GS, Firl A, Feller MB. A role for correlated spontaneous activity in the assembly of neural circuits. Neuron. 2013;80:1129–44.
pubmed: 24314725 pmcid: 4560201
Blanquie O, Yang JW, Kilb W, Sharopov S, Sinning A, Luhmann HJ. Electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortex. Elife. 2017;6:e27696.
pubmed: 28826501 pmcid: 5582867
O’Reilly C, Lewis JD, Elsabbagh M. Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies. PLoS One. 2017;12:e0175870.
pubmed: 28467487 pmcid: 5414938
Rane P, Cochran D, Hodge SM, Haselgrove C, Kennedy DN, Frazier JA. Connectivity in autism: a review of MRI connectivity studies. Harv Rev Psychiatry. 2015;23:223–44.
pubmed: 26146755 pmcid: 5083037
Li X, Zhang K, He X, Zhou J, Jin C. Structural, functional, and molecular imaging of autism spectrum disorder. Neurosci Bull. 2021;37:1051–71.
pubmed: 33779890 pmcid: 8275699
Sheffield JM, Barch DM. Cognition and resting-state functional connectivity in schizophrenia. Neurosci Biobehav Rev. 2016;61:108–20.
pubmed: 26698018
Van Den Heuvel MP, Fornito A. Brain networks in schizophrenia. Neuropsychol Rev. 2014;24:32–48.
pubmed: 24500505
Wang J, Lou H, Pedersen CJ, Smith AD, Perez RG. 14-3-3ζ contributes to tyrosine hydroxylase activity in MN9D cells: Localization of dopamine regulatory proteins to mitochondria. J Biol Chem. 2009;284:14011–9.
pubmed: 19289463 pmcid: 2682849
Kesby JP, Eyles DW, McGrath JJ, Scott JG. Dopamine, psychosis and schizophrenia: the widening gap between basic and clinical neuroscience. Transl Psychiatry. 2018;8:30.
pubmed: 29382821 pmcid: 5802623
Pavǎl D. A dopamine hypothesis of autism spectrum disorder. Dev Neurosci. 2017;39:355–60.
pubmed: 28750400
Tripp G, Wickens JR. Neurobiology of ADHD. Neuropharmacology. 2009;57:579–89.
pubmed: 19627998
Zakzanis KK, Hansen KT. Dopamine D2 densities and the schizophrenic brain. Schizophr Res. 1998;32:201–6.
pubmed: 9720125
Kestler LP, Walker E, Vega EM. Dopamine receptors in the brains of schizophrenia patients: a meta-analysis of the findings. Behav Pharmacol. 2001;12:355–71.
pubmed: 11710751
Gabriele S, Sacco R, Persico AM. Blood serotonin levels in autism spectrum disorder: a systematic review and meta-analysis. Eur Neuropsychopharmacol. 2014;24:919–29.
pubmed: 24613076
Muck-Seler D, Pivac N, Mustapic M, Crncevic Z, Jakovljevic M, Sagud M. Platelet serotonin and plasma prolactin and cortisol in healthy, depressed and schizophrenic women. Psychiatry Res. 2004;127:217–26.
pubmed: 15296821
Ramshaw H, Xu X, Jaehne EJ, McCarthy P, Greenberg Z, Saleh E, et al. Locomotor hyperactivity in 14-3-3ζ KO mice is associated with dopamine transporter dysfunction. Transl Psychiatry. 2013;3:e327.
pubmed: 24301645 pmcid: 4030331
Persico AM, Ricciardello A, Lamberti M, Turriziani L, Cucinotta F, Brogna C, et al. The pediatric psychopharmacology of autism spectrum disorder: a systematic review—Part I: the past and the present. Prog Neuro-Psychopharmacol. Biol Psychiatry. 2021;110:110326.
Jacob SN, Nienborg H. Monoaminergic neuromodulation of sensory processing. Front Neural Circuits. 2018;12:51.
pubmed: 30042662 pmcid: 6048220
Fernández M, Mollinedo-Gajate I, Peñagarikano O. Neural circuits for social cognition: implications for autism. Neuroscience. 2018;370:148–62.
pubmed: 28729065
Rademacher L, Schulte-Rüther M, Hanewald B, Lammertz S. Reward: from basic reinforcers to anticipation of social cues. Curr Top Behav Neurosci.2016;30:207–21.
Franceschini A, Fattore L. Gender-specific approach in psychiatric diseases: because sex matters. Eur J Pharmacol. 2021;896:173895.
pubmed: 33508283

Auteurs

Ester Antón-Galindo (E)

Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain.
Centro de Investigación Biomédica en Red de Enfermedades raras (CIBERER), Madrid, 28029, Spain.
Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Catalunya, 08028, Spain.
Institut de Recerca Sant Joan de Déu (IRSJD), Esplugues de Llobregat, Catalunya, 08950, Spain.

Elisa Dalla Vecchia (E)

Department of Genetics and Genome Biology, College of Life Sciences, University of Leicester, Leicester, LE1 7RH, UK.

Javier G Orlandi (JG)

RIKEN Center for Brain Science, Wako-shi, Saitama, 351-0198, Japan.

Gustavo Castro (G)

ICFO - Institut de Ciències Fotòniques, The Barcelona Institute of Science and Technology, Castelldefels, Catalunya, 08860, Spain.

Emilio J Gualda (EJ)

ICFO - Institut de Ciències Fotòniques, The Barcelona Institute of Science and Technology, Castelldefels, Catalunya, 08860, Spain.

Andrew M J Young (AMJ)

Department of Neuroscience, Psychology and Behaviour, College of Life Sciences, University of Leicester, Leicester, LE1 7RH, UK.

Marc Guasch-Piqueras (M)

Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain.
Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Catalunya, 08028, Spain.

Concepció Arenas (C)

Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain.

Carlos Herrera-Úbeda (C)

Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain.
Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Catalunya, 08028, Spain.

Jordi Garcia-Fernàndez (J)

Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain.
Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Catalunya, 08028, Spain.

Fernando Aguado (F)

Departament de Biologia cel·lular, Fisiologia i Immunologia, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain.
Institute of Neurosciences, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain.

Pablo Loza-Alvarez (P)

ICFO - Institut de Ciències Fotòniques, The Barcelona Institute of Science and Technology, Castelldefels, Catalunya, 08860, Spain.

Bru Cormand (B)

Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain. bcormand@ub.edu.
Centro de Investigación Biomédica en Red de Enfermedades raras (CIBERER), Madrid, 28029, Spain. bcormand@ub.edu.
Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Catalunya, 08028, Spain. bcormand@ub.edu.
Institut de Recerca Sant Joan de Déu (IRSJD), Esplugues de Llobregat, Catalunya, 08950, Spain. bcormand@ub.edu.

William H J Norton (WHJ)

Department of Genetics and Genome Biology, College of Life Sciences, University of Leicester, Leicester, LE1 7RH, UK. whjn1@leicester.ac.uk.

Noèlia Fernàndez-Castillo (N)

Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain. noefernandez@ub.edu.
Centro de Investigación Biomédica en Red de Enfermedades raras (CIBERER), Madrid, 28029, Spain. noefernandez@ub.edu.
Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Catalunya, 08028, Spain. noefernandez@ub.edu.
Institut de Recerca Sant Joan de Déu (IRSJD), Esplugues de Llobregat, Catalunya, 08950, Spain. noefernandez@ub.edu.

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