Evolutionary Differences in the Vegf/Vegfr Code Reveal Organotypic Roles for the Endothelial Cell Receptor Kdr in Developmental Lymphangiogenesis.


Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
20 08 2019
Historique:
received: 05 12 2018
revised: 11 06 2019
accepted: 16 07 2019
entrez: 22 8 2019
pubmed: 23 8 2019
medline: 1 9 2020
Statut: ppublish

Résumé

Lymphatic vascular development establishes embryonic and adult tissue fluid balance and is integral in disease. In diverse vertebrate organs, lymphatic vessels display organotypic function and develop in an organ-specific manner. In all settings, developmental lymphangiogenesis is considered driven by vascular endothelial growth factor (VEGF) receptor-3 (VEGFR3), whereas a role for VEGFR2 remains to be fully explored. Here, we define the zebrafish Vegf/Vegfr code in receptor binding studies. We find that while Vegfd directs craniofacial lymphangiogenesis, it binds Kdr (a VEGFR2 homolog) but surprisingly, unlike in mammals, does not bind Flt4 (VEGFR3). Epistatic analyses and characterization of a kdr mutant confirm receptor-binding analyses, demonstrating that Kdr is indispensible for rostral craniofacial lymphangiogenesis, but not caudal trunk lymphangiogenesis, in which Flt4 is central. We further demonstrate an unexpected yet essential role for Kdr in inducing lymphatic endothelial cell fate. This work reveals evolutionary divergence in the Vegf/Vegfr code that uncovers spatially restricted mechanisms of developmental lymphangiogenesis.

Identifiants

pubmed: 31433980
pii: S2211-1247(19)30959-3
doi: 10.1016/j.celrep.2019.07.055
pii:
doi:

Substances chimiques

Ligands 0
Vascular Endothelial Growth Factor C 0
Zebrafish Proteins 0
vascular endothelial growth factor C, zebrafish 0
Vascular Endothelial Growth Factor Receptor-2 EC 2.7.10.1
kdr protein, zebrafish EC 2.7.10.1

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2023-2036.e4

Informations de copyright

Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved.

Auteurs

Adam J Vogrin (AJ)

Tumour Angiogenesis and Microenvironment Program, Peter MacCallum Cancer Centre, Melbourne, VIC 3000, Australia.

Neil I Bower (NI)

Division of Genomics of Development and Disease, Institute for Molecular Bioscience, University of Queensland, St. Lucia, QLD 4072, Australia.

Menachem J Gunzburg (MJ)

Monash Institute of Pharmaceutical Sciences, Monash University, Melbourne, VIC 3052, Australia.

Sally Roufail (S)

Tumour Angiogenesis and Microenvironment Program, Peter MacCallum Cancer Centre, Melbourne, VIC 3000, Australia.

Kazuhide S Okuda (KS)

Division of Genomics of Development and Disease, Institute for Molecular Bioscience, University of Queensland, St. Lucia, QLD 4072, Australia.

Scott Paterson (S)

Division of Genomics of Development and Disease, Institute for Molecular Bioscience, University of Queensland, St. Lucia, QLD 4072, Australia.

Stephen J Headey (SJ)

Monash Institute of Pharmaceutical Sciences, Monash University, Melbourne, VIC 3052, Australia.

Steven A Stacker (SA)

Tumour Angiogenesis and Microenvironment Program, Peter MacCallum Cancer Centre, Melbourne, VIC 3000, Australia; Department of Surgery, Royal Melbourne Hospital, and Sir Peter MacCallum Department of Oncology, University of Melbourne, Melbourne, VIC 3000, Australia.

Benjamin M Hogan (BM)

Division of Genomics of Development and Disease, Institute for Molecular Bioscience, University of Queensland, St. Lucia, QLD 4072, Australia. Electronic address: ben.hogan@petermac.org.

Marc G Achen (MG)

Tumour Angiogenesis and Microenvironment Program, Peter MacCallum Cancer Centre, Melbourne, VIC 3000, Australia; Department of Surgery, Royal Melbourne Hospital, and Sir Peter MacCallum Department of Oncology, University of Melbourne, Melbourne, VIC 3000, Australia. Electronic address: marc.achen@petermac.org.

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Classifications MeSH