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Conserved and context-dependent roles for Pdgfrb signaling during zebrafish vascular mural cell development

Koji Ando, Yu-Huan Shih, Lwaki Ebarasi, Ann Grosse, Daneal Portman, Ayano Chiba, Kenny Mattonet, Claudia Gerri, View ORCID ProfileDidier Y.R. Stainier, View ORCID ProfileNaoki Mochizuki, Shigetomo Fukuhara, Christer Betsholtz, View ORCID ProfileNathan D. Lawson
doi: https://doi.org/10.1101/2021.03.29.437552
Koji Ando
1Department of Immunology, Genetics and Pathology, Rudbeck Laboratory, Uppsala University, Dag Hammarskjölds väg 20, SE-751 85 Uppsala, Sweden
2Department of Molecular Pathophysiology, Institute of Advanced Medical Sciences, Nippon Medical School, Sendagi Bunkyo-ku, Tokyo 113 8602, JAPAN
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  • For correspondence: koji-ando@nms.ac.jp nathan.lawson@umassmed.edu
Yu-Huan Shih
3Department of Molecular, Cell, and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, 01650, United States
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Lwaki Ebarasi
4Department of Medical Biochemistry and Biophysics, Division of Vascular Biology, Karolinska Institute, Stockholm, Sweden
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Ann Grosse
3Department of Molecular, Cell, and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, 01650, United States
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Daneal Portman
3Department of Molecular, Cell, and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, 01650, United States
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Ayano Chiba
5Department of Cell Biology, National Cerebral and Cardiovascular Center Research Institute, Suita, Osaka 564 8565, Japan
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Kenny Mattonet
6Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Ludwigstrasse 43, 61231 Bad Nauheim, Germany
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Claudia Gerri
6Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Ludwigstrasse 43, 61231 Bad Nauheim, Germany
7Human Embryo and Stem Cell Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK
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Didier Y.R. Stainier
6Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Ludwigstrasse 43, 61231 Bad Nauheim, Germany
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  • ORCID record for Didier Y.R. Stainier
Naoki Mochizuki
5Department of Cell Biology, National Cerebral and Cardiovascular Center Research Institute, Suita, Osaka 564 8565, Japan
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Shigetomo Fukuhara
2Department of Molecular Pathophysiology, Institute of Advanced Medical Sciences, Nippon Medical School, Sendagi Bunkyo-ku, Tokyo 113 8602, JAPAN
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Christer Betsholtz
1Department of Immunology, Genetics and Pathology, Rudbeck Laboratory, Uppsala University, Dag Hammarskjölds väg 20, SE-751 85 Uppsala, Sweden
8Department of Medicine Huddinge (MedH), Karolinska Institutet, Campus Flemingsberg, Neo, Blickagången 16, Hiss S, plan 7, SE-141 57 Huddinge, Sweden
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Nathan D. Lawson
3Department of Molecular, Cell, and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, 01650, United States
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  • ORCID record for Nathan D. Lawson
  • For correspondence: koji-ando@nms.ac.jp nathan.lawson@umassmed.edu
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ABSTRACT

Platelet derived growth factor beta and its receptor, Pdgfrb, play essential roles in the development of vascular mural cells, including pericytes and vascular smooth muscle. To determine if this role was conserved in zebrafish, we analyzed pdgfb and pdgfrb mutant lines. Similar to mouse, pdgfb and pdgfrb mutant zebrafish lack brain pericytes and exhibit anatomically selective loss of vascular smooth muscle coverage. Despite these defects, pdgfrb mutant zebrafish did not otherwise exhibit circulatory defects at larval stages. However, beginning at juvenile stages, we observed severe cranial hemorrhage and vessel dilation associated with loss of pericytes and vascular smooth muscle cells in pdgfrb mutants. Similar to mouse, pdgfrb mutant zebrafish also displayed structural defects in the glomerulus, but normal development of hepatic stellate cells. We also noted defective mural cell investment on coronary vessels with concomitant defects in their development. Together, our studies support a conserved requirement for Pdgfrb signaling in mural cells. In addition, these mutants provide an important model for definitive investigation of mural cells during early embryonic stages without confounding secondary effects from circulatory defects.

Summary statement Genetic analysis in zebrafish demonstrates the conserved role of Pdgfb/Pdgfrb signaling in pericyte and vascular smooth muscle cell formation during vascular development in vertebrates.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted March 29, 2021.
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Conserved and context-dependent roles for Pdgfrb signaling during zebrafish vascular mural cell development
Koji Ando, Yu-Huan Shih, Lwaki Ebarasi, Ann Grosse, Daneal Portman, Ayano Chiba, Kenny Mattonet, Claudia Gerri, Didier Y.R. Stainier, Naoki Mochizuki, Shigetomo Fukuhara, Christer Betsholtz, Nathan D. Lawson
bioRxiv 2021.03.29.437552; doi: https://doi.org/10.1101/2021.03.29.437552
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Conserved and context-dependent roles for Pdgfrb signaling during zebrafish vascular mural cell development
Koji Ando, Yu-Huan Shih, Lwaki Ebarasi, Ann Grosse, Daneal Portman, Ayano Chiba, Kenny Mattonet, Claudia Gerri, Didier Y.R. Stainier, Naoki Mochizuki, Shigetomo Fukuhara, Christer Betsholtz, Nathan D. Lawson
bioRxiv 2021.03.29.437552; doi: https://doi.org/10.1101/2021.03.29.437552

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