Zebrafish dnm1a gene plays a role in the formation of axons and synapses in the nervous tissue.

DAB (RRID:AB_2335241) Fiji software (RRID:SCR_002285) Prism GraphPad Software (RRID:SCR_002798) classical dynamins developmental and epileptic encephalopathy (DEE) disease dnm1a mouse anti-acetylated tubulin (RRID:AB_609894) nervous tissue neurodevelopment pBluescript SK- (RRID:Addgene_12306) vesicular transport protein zebrafish AB strain (RRID:ZIRC_ZL1) zebrafish embryos

Journal

Journal of neuroscience research
ISSN: 1097-4547
Titre abrégé: J Neurosci Res
Pays: United States
ID NLM: 7600111

Informations de publication

Date de publication:
08 2023
Historique:
revised: 27 02 2023
received: 29 11 2022
accepted: 24 03 2023
medline: 23 6 2023
pubmed: 10 4 2023
entrez: 9 4 2023
Statut: ppublish

Résumé

Classical dynamins (DNMs) are GTPase proteins engaged in endocytosis, a fundamental process for cargo internalization from the plasma membrane. In mammals, three DNM genes are present with different expression patterns. DNM1 is expressed at high levels in neurons, where it takes place in the recycling of synaptic vesicles; DNM2 is ubiquitously expressed, while DNM3 is found in the brain and in the testis. Due to the conservation of genes in comparison to mammals, we took advantage of a zebrafish model for functional characterization of dnm1a, ortholog of mammalian DNM1. Our data strongly demonstrated that dnm1a has a nervous tissue-specific expression pattern and plays a role in the formation of both axon and synapse. This is the first in vivo study that collects evidence about the effects of dnm1a loss of function in zebrafish, thus providing a new excellent model to be used in different scientific fields.

Identifiants

pubmed: 37031448
doi: 10.1002/jnr.25197
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1345-1359

Informations de copyright

© 2023 The Authors. Journal of Neuroscience Research published by Wiley Periodicals LLC.

Références

Allen, N. M., Conroy, J., Shahwan, A., Lynch, B., Correa, R. G., Pena, S. D., McCreary, D., Magalhaes, T. R., Ennis, S., Lynch, S. A., & King, M. D. (2016). Unexplained early onset epileptic encephalopathy: Exome screening and phenotype expansion. Epilepsia, 57, e12-e17. https://doi.org/10.1111/epi.13250
AlTassan, R., AlQudairy, H., Alromayan, R., Alfalah, A., AlHarbi, O. A., González-Álvarez, A. C., Arold, S. T., & Kaya, N. (2022). Clinical, radiological, and genetic characterization of a patient with a novel homoallelic loss-of-function variant in DNM1. Genes, 13(12), 2252. https://doi.org/10.3390/genes13122252
Asinof, S., Mahaffey, C., Beyer, B., Frankel, W. N., & Boumil, R. (2016, November). Dynamin 1 isoform roles in a mouse model of severe childhood epileptic encephalopathy. Neurobiology of Disease, 95, 1-11. https://doi.org/10.1016/j.nbd.2016.06.014
Balciuniene, J., Nagelberg, D., Walsh, K. T., Camerota, D., Georlette, D., Biemar, F., Bellipanni, G., & Balciunas, D. (2013, September 14). Efficient disruption of zebrafish genes using a Gal4-containing gene trap. BMC Genomics, 14, 619. https://doi.org/10.1186/1471-2164-14-619
Behra, M., Cousin, X., Bertrand, C., Vonesch, J. L., Biellmann, D., Chatonnet, A., & Strähle, U. (2002, February). Acetylcholinesterase is required for neuronal and muscular development in the zebrafish embryo. Nature Neuroscience, 5(2), 111-118. https://doi.org/10.1038/nn788
Boumil, R. M., Letts, V. A., Roberts, M. C., Lenz, C., Mahaffey, C. L., Zhang, Z. W., Moser, T., & Frankel, W. N. (2010, August 5). A missense mutation in a highly conserved alternate exon of dynamin-1 causes epilepsy in fitful mice. PLoS Genetics, 6(8), e1001046. https://doi.org/10.1371/journal.pgen.1001046
Bragato, C., Blasevich, F., Ingenito, G., Mantegazza, R., & Maggi, L. (2021, May). Therapeutic efficacy of 3,4-Diaminopyridine phosphate on neuromuscular junction in Pompe disease. Biomedicine & Pharmacotherapy, 137, 111357. https://doi.org/10.1016/j.biopha.2021.111357
Bragato, C., Gaudenzi, G., Blasevich, F., Pavesi, G., Maggi, L., Giunta, M., Cotelli, F., & Mora, M. (2016, February 4). Zebrafish as a model to investigate dynamin 2-related diseases. Scientific Reports, 6, 20466. https://doi.org/10.1038/srep20466
Brennan, C., Mangoli, M., Dyer, C. E., & Ashworth, R. (2005, November 15). Acetylcholine and calcium signalling regulates muscle fibre formation in the zebrafish embryo. Journal of Cell Science, 118(Pt 22), 5181-5190. https://doi.org/10.1242/jcs.02625
Chen, M. S., Burgess, C. C., Vallee, R. B., & Wadsworth, S. C. (1992, November). Developmental stage- and tissue-specific expression of shibire, a Drosophila gene involved in endocytosis. Journal of Cell Science, 103(Pt 3), 619-628. https://doi.org/10.1242/jcs.103.3.619
Chen, M. S., Obar, R. A., Schroeder, C. C., Austin, T. W., Poodry, C. A., Wadsworth, S. C., & Vallee, R. B. (1991, June 13). Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature, 351(6327), 583-586. https://doi.org/10.1038/351583a0
Choudhry, H., Aggarwal, M., & Pan, P. Y. (2021, November 20). Mini-review: Synaptojanin 1 and its implications in membrane trafficking. Neuroscience Letters, 765, 136288. https://doi.org/10.1016/j.neulet.2021.136288
Clark, S. G., Shurland, D. L., Meyerowitz, E. M., Bargmann, C. I., & van der Bliek, A. M. (1997, September 16). A dynamin GTPase mutation causes a rapid and reversible temperature-inducible locomotion defect in C. elegans. Proceedings of the National Academy of Sciences of the United States of America, 94(19), 10438-10443. https://doi.org/10.1073/pnas.94.19.10438
Cousin, M. A. (2017, August 3). Integration of synaptic vesicle cargo retrieval with endocytosis at central nerve terminals. Frontiers in Cellular Neuroscience, 11, 234. https://doi.org/10.3389/fncel.2017.00234
Damke, H., Baba, T., Warnock, D. E., & Schmid, S. L. (1994, November). Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. The Journal of Cell Biology, 127(4), 915-934. https://doi.org/10.1083/jcb.127.4.915
Ferguson, S. M., Brasnjo, G., Hayashi, M., Wölfel, M., Collesi, C., Giovedi, S., Raimondi, A., Gong, L. W., Ariel, P., Paradise, S., O'Toole, E., Flavell, R., Cremona, O., Miesenböck, G., Ryan, T. A., & De Camilli, P. (2007). A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science, 316, 570-574. https://doi.org/10.1126/science.1140621
Ferguson, S. M., & De Camilli, P. (2012, January 11). Dynamin, a membrane-remodelling GTPase. Nature Reviews. Molecular Cell Biology, 13(2), 75-88. https://doi.org/10.1038/nrm3266
Gibbs, E. M., Davidson, A. E., Trickey-Glassman, A., Backus, C., Hong, Y., Sakowski, S. A., Dowling, J. J., & Feldman, E. L. (2013). Two dynamin-2 genes are required for normal zebrafish development. PLoS One, 8(2), e55888. https://doi.org/10.1371/journal.pone.0055888
Griffin, A., Carpenter, C., Liu, J., Paterno, R., Grone, B., Hamling, K., Moog, M., Dinday, M. T., Figueroa, F., Anvar, M., Ononuju, C., Qu, T., & Baraban, S. C. (2021, June 3). Phenotypic analysis of catastrophic childhood epilepsy genes. Communications Biology, 4(1), 680. https://doi.org/10.1038/s42003-021-02221-y
Hegarty, S. V., Sullivan, A. M., & O'Keeffe, G. W. (2017, March 16). Endocytosis contributes to BMP2-induced Smad signalling and neuronal growth. Neuroscience Letters, 643, 32-37. https://doi.org/10.1016/j.neulet.2017.02.013
Hinshaw, J. E., & Schmid, S. L. (1995, March 9). Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature, 374(6518), 190-192. https://doi.org/10.1038/374190a0
Howe, K., Clark, M. D., Torroja, C. F., Torrance, J., Berthelot, C., Muffato, M., Collins, J. E., Humphray, S., McLaren, K., Matthews, L., McLaren, S., Sealy, I., Caccamo, M., Churcher, C., Scott, C., Barrett, J. C., Koch, R., Rauch, G. J., White, S., … Stemple, D. L. (2013, April 25). The zebrafish reference genome sequence and its relationship to the human genome. Nature, 496(7446), 498-503. https://doi.org/10.1038/nature12111. Erratum in: Nature. 2014 January 9;505(7482):248.
Kaksonen, M., & Roux, A. (2018, May). Mechanisms of clathrin-mediated endocytosis. Nature Reviews. Molecular Cell Biology, 19(5), 313-326. https://doi.org/10.1038/nrm.2017.132
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., & Schilling, T. F. (1995, July). Stages of embryonic development of the zebrafish. Developmental Dynamics, 203(3), 253-310. https://doi.org/10.1002/aja.1002030302
Koenig, J. H., & Ikeda, K. (1989, November). Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. The Journal of Neuroscience, 9(11), 3844-3860. https://doi.org/10.1523/JNEUROSCI.09-11-03844.1989
Kolnikova, M., Skopkova, M., Ilencikova, D., Foltan, T., Payerova, J., Danis, D., Klimes, I., Stanik, J., & Gasperikova, D. (2018, March). DNM1 encephalopathy-Atypical phenotype with hypomyelination due to a novel de novo variant in the DNM1 gene. Seizure, 56, 31-33. https://doi.org/10.1016/j.seizure.2018.01.020
Koonin, E. V. (2005). Orthologs, paralogs, and evolutionary genomics. Annual Review of Genetics, 39, 309-338. https://doi.org/10.1146/annurev.genet.39.073003.114725
Köster, R. W., & Fraser, S. E. (2001, November 27). Direct imaging of in vivo neuronal migration in the developing cerebellum. Current Biology, 11(23), 1858-1863. https://doi.org/10.1016/s0960-9822(01)00585-1
La, T. M., Tachibana, H., Li, S. A., Abe, T., Seiriki, S., Nagaoka, H., Takashima, E., Takeda, T., Ogawa, D., Makino, S. I., Asanuma, K., Watanabe, M., Tian, X., Ishibe, S., Sakane, A., Sasaki, T., Wada, J., Takei, K., & Yamada, H. (2020). Dynamin 1 is important for microtubule organization and stabilization in glomerular podocytes. The FASEB Journal, 34, 16449-16463.
Li, Z., Mericskay, M., Agbulut, O., Butler-Browne, G., Carlsson, L., Thornell, L. E., Babinet, C., & Paulin, D. (1997, October 6). Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. The Journal of Cell Biology, 139(1), 129-144. https://doi.org/10.1083/jcb.139.1.129
Masur, S. K., Kim, Y. T., & Wu, C. F. (1990, April). Reversible inhibition of endocytosis in cultured neurons from the Drosophila temperature-sensitive mutant shibirets1. Journal of Neurogenetics, 6(3), 191-206. https://doi.org/10.3109/01677069009107110
Narayanan, R., & Oates, A. C. (2019, March 20). Detection of mRNA by whole mount in situ hybridization and DNA extraction for genotyping of zebrafish embryos. Bio-Protocol, 9(6), e3193. https://doi.org/10.21769/BioProtoc.3193
Panzer, J. A., Gibbs, S. M., Dosch, R., Wagner, D., Mullins, M. C., Granato, M., & Balice-Gordon, R. J. (2005, September 15). Neuromuscular synaptogenesis in wild-type and mutant zebrafish. Developmental Biology, 285(2), 340-357. https://doi.org/10.1016/j.ydbio.2005.06.027
Parthasarathy, S., Ruggiero, S. M., Gelot, A., Soardi, F. C., Ribeiro, B. F. R., Pires, D. E. V., Ascher, D. B., Schmitt, A. S., Rambaud, C., Xie, H. M., Lusk, L., Wilmarth, O., McDonnell, P. P., Juarez, O. A., Grace, A. N., Buratti, J., Mignot, C., Gras, D., Nava, C., … Cuddapah, V. A. (2022). A recurrent de novo splice site variant involving DNM1 exon 10a causes developmental and epileptic encephalopathy through a dominant-negative mechanism. BioRxiv preprints. https://doi.org/10.1101/2022.06.02.492389
Ramachandran, R., & Schmid, S. L. (2018, April 23). The dynamin superfamily. Current Biology, 28(8), R411-R416. https://doi.org/10.1016/j.cub.2017.12.013
Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A., & Ekker, S. C. (2007, May 25). p53 activation by knockdown technologies. PLoS Genetics, 3(5), e78. https://doi.org/10.1371/journal.pgen.0030078
Sahly, A. N., Krochmalnek, E., St-Onge, J., Srour, M., & Myers, K. A. (2020, December). Severe DNM1 encephalopathy with dysmyelination due to recurrent splice site pathogenic variant. Human Genetics, 139(12), 1575-1578. https://doi.org/10.1007/s00439-020-02224-5
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., & Cardona, A. (2012, June 28). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676-682. https://doi.org/10.1038/nmeth.2019
Shehwana, H., & Konu, O. (2019). Comparative transcriptomics between zebrafish and mammals: A roadmap for discovery of conserved and unique signaling pathways in physiology and disease. Frontiers in Cell and Developmental Biology, 7, 5. https://doi.org/10.3389/fcell.2019.00005
Suster, M. L., Kikuta, H., Urasaki, A., Asakawa, K., & Kawakami, K. (2009). Transgenesis in zebrafish with the tol2 transposon system. Methods in Molecular Biology, 561, 41-63. https://doi.org/10.1007/978-1-60327-019-9_3
Thisse, B., & Thisse, C. (2014). In situ hybridization on whole-mount zebrafish embryos and young larvae. Methods in Molecular Biology, 1211, 53-67. https://doi.org/10.1007/978-1-4939-1459-3_5
Torre, E., McNiven, M. A., & Urrutia, R. (1994, December 23). Dynamin 1 antisense oligonucleotide treatment prevents neurite formation in cultured hippocampal neurons. The Journal of Biological Chemistry, 269(51), 32411-32417.
van der Bliek, A. M., & Meyerowitz, E. M. (1991, May 30). Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature, 351(6325), 411-414. https://doi.org/10.1038/351411a0
Von Spiczak, S., Helbig, K. L., Shinde, D. N., Huether, R., Pendziwiat, M., Lourenço, C., Nunes, M. E., Sarco, D. P., Kaplan, R. A., Dlugos, D. J., Kirsch, H., Slavotinek, A., Cilio, M. R., Cervenka, M. C., Cohen, J. S., McClellan, R., Fatemi, A., Yuen, A., Sagawa, Y., … Epi4K Consortium; EuroEPINOMICS-RES NLES Working Group. (2017, July 25). DNM1 encephalopathy: A new disease of vesicle fission. Neurology, 89(4), 385-394. https://doi.org/10.1212/WNL.0000000000004152
Westerfield, M., Stuart, G., & Wegner, J. (1993). Expression of foreign genes in zebrafish embryos. In W. C. Brown (Ed.), Developments in industrial microbiology (Vol. II, pp. 658-665). Springer.
Woods, I. G., Lyons, D. A., Voas, M. G., Pogoda, H. M., & Talbot, W. S. (2006, April 4). nsf is essential for organization of myelinated axons in zebrafish. Current Biology, 16(7), 636-648. https://doi.org/10.1016/j.cub.2006.02.067
Yigit, G., Sheffer, R., Daana, M., Li, Y., Kaygusuz, E., Mor-Shakad, H., Altmüller, J., Nürnberg, P., Douiev, L., Kaulfuss, S., Burfeind, P., Wollnik, B., & Brockmann, K. (2022, June). Loss-of-function variants in DNM1 cause a specific form of developmental and epileptic encephalopathy only in biallelic state. Journal of Medical Genetics, 59(6), 549-553. https://doi.org/10.1136/jmedgenet-2021-107769
Zhang, H., Bryson, V. G., Wang, C., Li, T., Kerr, J. P., Wilson, R., Muoio, D. M., Bloch, R. J., Ward, C., & Rosenberg, P. B. (2021, September 8). Desmin interacts with STIM1 and coordinates Ca2+ signaling in skeletal muscle. JCI Insight, 6(17), e143472. https://doi.org/10.1172/jci.insight.143472
Zhang, R., Lee, D. M., Jimah, J. R., Gerassimov, N., Yang, C., Kim, S., Luvsanjav, D., Winkelman, J., Mettlen, M., Abrams, M. E., Kalia, R., Keene, P., Pandey, P., Ravaux, B., Kim, J. H., Ditlev, J. A., Zhang, G., Rosen, M. K., Frost, A., … Chen, E. H. (2020, June). Dynamin regulates the dynamics and mechanical strength of the actin cytoskeleton as a multifilament actin-bundling protein. Nature Cell Biology, 22(6), 674-688. https://doi.org/10.1038/s41556-020-0519-7

Auteurs

Cinzia Bragato (C)

Department of Earth and Environmental Sciences, POLARIS Research Center, University of Milano-Bicocca, Milan, Italy.

Anna Pistocchi (A)

Dipartimento di Biotecnologie Mediche e Medicina Traslazionale, Università degli Studi di Milano, Milan, Italy.

Gianfranco Bellipanni (G)

Sbarro Institute for Cancer Research and Molecular Medicine, College of Science and Technology, Temple University, Philadelphia, Pennsylvania, USA.
Department of Biology, Center for Biotechnology, College of Science and Technology, Temple University, Philadelphia, Pennsylvania, USA.

Stefano Confalonieri (S)

IEO, European Institute of Oncology IRCCS, Milan, Italy.

Jorune Balciuniene (J)

Department of Biology, Center for Biotechnology, College of Science and Technology, Temple University, Philadelphia, Pennsylvania, USA.

Federica Maria Monastra (FM)

Dipartimento di Biotecnologie Mediche e Medicina Traslazionale, Università degli Studi di Milano, Milan, Italy.

Silvia Carra (S)

Laboratory of Endocrine and Metabolic Research, IRCCS, Istituto Auxologico Italiano, Milan, Italy.

Giovanni Vitale (G)

Dipartimento di Biotecnologie Mediche e Medicina Traslazionale, Università degli Studi di Milano, Milan, Italy.
Laboratory of Geriatric and Oncologic Neuroendocrinology Research, IRCCS, Istituto Auxologico Italiano, Milan, Italy.

Paride Mantecca (P)

Department of Earth and Environmental Sciences, POLARIS Research Center, University of Milano-Bicocca, Milan, Italy.

Franco Cotelli (F)

Department of Biosciences, University of Milan, Milan, Italy.

Germano Gaudenzi (G)

Laboratory of Geriatric and Oncologic Neuroendocrinology Research, IRCCS, Istituto Auxologico Italiano, Milan, Italy.

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