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A versatile transcription factor: Multiple roles of orthopedia a (otpa) beyond its restricted localization in dopaminergic systems of developing and adult zebrafish (Danio rerio) brains

Eugenin von Bernhardi, Jaime and Biechl, Daniela and Miek, Laura and Herget, Ulrich and Ryu, Soojin and Wullimann, Mario F. (2022) A versatile transcription factor: Multiple roles of orthopedia a (otpa) beyond its restricted localization in dopaminergic systems of developing and adult zebrafish (Danio rerio) brains. Journal of Comparative Neurology, 530 (14). pp. 2537-2561. ISSN 0021-9967. doi:10.1002/cne.25351. https://resolver.caltech.edu/CaltechAUTHORS:20220715-744223000

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Abstract

Many transcription factors boost neural development and differentiation in specific directions and serve for identifying similar or homologous structures across species. The expression of Orthopedia (Otp) is critical for the development of certain cell groups along the vertebrate neuraxis, for example, the medial amygdala or hypothalamic neurosecretory neurons. Therefore, the primary focus of the present study is the distribution of Orthopedia a (Otpa) in the larval and adult zebrafish (Danio rerio) brain. Since Otpa is also critical for the development of zebrafish basal diencephalic dopaminergic cells, colocalization of Otpa with the catecholamine synthesizing enzyme tyrosine hydroxylase (TH) is studied. Cellular colocalization of Otpa and dopamine is only seen in magnocellular neurons of the periventricular posterior tubercular nucleus and in the posterior tuberal nucleus. Otpa-positive cells occur in many additional structures along the zebrafish neuraxis, from the secondary prosencephalon down to the hindbrain. Furthermore, Otpa expression is studied in shh-GFP and islet1-GFP transgenic zebrafish. Otpa-positive cells only express shh in dopaminergic magnocellular periventricular posterior tubercular cells, and only colocalize with islet1-GFP in the ventral zone and prerecess caudal periventricular hypothalamic zone and the perilemniscal nucleus. The scarcity of cellular colocalization of Otpa in islet1-GFP cells indicates that the Shh-islet1 neurogenetic pathway is not active in most Otpa-expressing domains. Our analysis reveals detailed correspondences between mouse and zebrafish forebrain territories including the zebrafish intermediate nucleus of the ventral telencephalon and the mouse medial amygdala. The zebrafish preoptic Otpa-positive domain represents the neuropeptidergic supraopto-paraventricular region of all tetrapods. Otpa domains in the zebrafish basal plate hypothalamus suggest that the ventral periventricular hypothalamic zone corresponds to the otp-expressing basal hypothalamic tuberal field in the mouse. Furthermore, the mouse otp domain in the mammillary hypothalamus compares partly to our Otpa-positive domain in the prerecess caudal periventricular hypothalamic zone (Hc-a).


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1002/cne.25351DOIArticle
ORCID:
AuthorORCID
Eugenin von Bernhardi, Jaime0000-0003-1092-6942
Herget, Ulrich0000-0002-4419-1414
Ryu, Soojin0000-0002-7059-0160
Wullimann, Mario F.0000-0001-9292-2851
Additional Information:© 2022 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. Issue Online: 27 July 2022. Version of Record online: 16 June 2022. Manuscript accepted: 11 May 2022. Manuscript revised: 09 May 2022. Manuscript received: 01 December 2021. We thank Bea Stiening for various laboratory-related support and the Faculty of Biology of the Ludwig-Maximilians Universität München (LMU Munich) and the Graduate School for Systemic Neurosciences (GSN), as well as the Division of Neurobiology (Prof. Benedikt Grothe) at the LMU Munich for financial and infrastructural support. We also thank Prof. Reinhard Köster (Technical University Braunschweig) for providing fixed transgenic fish used in this study. Open access funding is enabled and organized by Projekt DEAL. AUTHOR CONTRIBUTION. Jaime Eugenin von Bernhardi, Daniela Biechl, Laura Miek, Ulrich Herget, Soojin Ryu, and Mario F Wullimann performed experiments. All authors contributed to the analysis of data and writing of the manuscript. DATA AVAILABILITY STATEMENT. The data that support the findings of this study are available from the corresponding author upon reasonable request. The authors declare that there are no conflict of interest.
Funders:
Funding AgencyGrant Number
Ludwig-Maximilians Universität MünchenUNSPECIFIED
Projekt DEALUNSPECIFIED
Subject Keywords:catecholamines; dopamine; hypothalamus; islet1; medial amygdala; mesodiencephalic complex; orthopedia; preoptic region; sonic hedgehog; tyrosine hydroxylase; zebrafish
Issue or Number:14
DOI:10.1002/cne.25351
Record Number:CaltechAUTHORS:20220715-744223000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220715-744223000
Official Citation:Eugenin von Bernhardi, J., Biechl, D., Miek, L., Herget, U., Ryu, S., & Wullimann, M. F. (2022). A versatile transcription factor: Multiple roles of orthopedia a (otpa) beyond its restricted localization in dopaminergic systems of developing and adult zebrafish (Danio rerio) brains. Journal of Comparative Neurology, 530, 2537–2561. https://doi.org/10.1002/cne.25351
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:115643
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:20 Jul 2022 20:58
Last Modified:15 Aug 2022 22:23

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