Nuclear S-nitrosylation impacts tissue regeneration in zebrafish

Gianfranco Matrone (), Sung Yun Jung, Jong Min Choi, Antrix Jain, Hon-Chiu Eastwood Leung, Kimal Rajapakshe, Cristian Coarfa, Julie Rodor, Martin A. Denvir, Andrew H. Baker and John P. Cooke
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Gianfranco Matrone: The University of Edinburgh
Sung Yun Jung: Baylor College of Medicine
Jong Min Choi: Baylor College of Medicine
Antrix Jain: Baylor College of Medicine
Hon-Chiu Eastwood Leung: Baylor College of Medicine
Kimal Rajapakshe: Baylor College of Medicine
Cristian Coarfa: Baylor College of Medicine
Julie Rodor: The University of Edinburgh
Martin A. Denvir: The University of Edinburgh
Andrew H. Baker: The University of Edinburgh
John P. Cooke: Houston Methodist Research Institute

Nature Communications, 2021, vol. 12, issue 1, 1-13

Abstract: Abstract Despite the importance of nitric oxide signaling in multiple biological processes, its role in tissue regeneration remains largely unexplored. Here, we provide evidence that inducible nitric oxide synthase (iNos) translocates to the nucleus during zebrafish tailfin regeneration and is associated with alterations in the nuclear S-nitrosylated proteome. iNos inhibitors or nitric oxide scavengers reduce protein S-nitrosylation and impair tailfin regeneration. Liquid chromatography/tandem mass spectrometry reveals an increase of up to 11-fold in the number of S-nitrosylated proteins during regeneration. Among these, Kdm1a, a well-known epigenetic modifier, is S-nitrosylated on Cys334. This alters Kdm1a binding to the CoRest complex, thus impairing its H3K4 demethylase activity, which is a response specific to the endothelial compartment. Rescue experiments show S-nitrosylation is essential for tailfin regeneration, and we identify downstream endothelial targets of Kdm1a S-nitrosylation. In this work, we define S-nitrosylation as an essential post-translational modification in tissue regeneration.

Date: 2021
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DOI: 10.1038/s41467-021-26621-0

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