S-nitrosylation of EZH2 alters PRC2 assembly, methyltransferase activity, and EZH2 stability to maintain endothelial homeostasis

Abstract Nitric oxide (NO), a versatile bio-active molecule modulates cellular functions through diverse mechanisms including S-nitrosylation of proteins. Herein, we report S-nitrosylation of selected cysteine residues of EZH2 in endothelial cells, which interplays with its stability and functions....

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Main Authors: Ashima Sakhuja, Ritobrata Bhattacharyya, Yash Tushar Katakia, Shyam Kumar Ramakrishnan, Srinjoy Chakraborty, Hariharan Jayakumar, Shailesh Mani Tripathi, Niyati Pandya Thakkar, Sumukh Thakar, Sandeep Sundriyal, Shibasish Chowdhury, Syamantak Majumder
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59003-x
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author Ashima Sakhuja
Ritobrata Bhattacharyya
Yash Tushar Katakia
Shyam Kumar Ramakrishnan
Srinjoy Chakraborty
Hariharan Jayakumar
Shailesh Mani Tripathi
Niyati Pandya Thakkar
Sumukh Thakar
Sandeep Sundriyal
Shibasish Chowdhury
Syamantak Majumder
author_facet Ashima Sakhuja
Ritobrata Bhattacharyya
Yash Tushar Katakia
Shyam Kumar Ramakrishnan
Srinjoy Chakraborty
Hariharan Jayakumar
Shailesh Mani Tripathi
Niyati Pandya Thakkar
Sumukh Thakar
Sandeep Sundriyal
Shibasish Chowdhury
Syamantak Majumder
author_sort Ashima Sakhuja
collection DOAJ
description Abstract Nitric oxide (NO), a versatile bio-active molecule modulates cellular functions through diverse mechanisms including S-nitrosylation of proteins. Herein, we report S-nitrosylation of selected cysteine residues of EZH2 in endothelial cells, which interplays with its stability and functions. We detect a significant reduction in H3K27me3 upon S-nitrosylation of EZH2 as contributed by the early dissociation of SUZ12 from the PRC2. Moreover, S-nitrosylation of EZH2 causes its cytosolic translocation, ubiquitination, and degradation. Further analysis reveal S-nitrosylation of cysteine 329 induces EZH2 instability, whereas S-nitrosylation of cysteine 700 abrogates its catalytic activity. We further show that S-nitrosylation-dependent regulation of EZH2 maintains endothelial homeostasis in both physiological and pathological settings. Molecular dynamics simulation reveals the inability of SUZ12 to efficiently bind to the SAL domain of EZH2 upon S-nitrosylation. Taken together, our study reports S-nitrosylation-dependent regulation of EZH2 and its associated PRC2 complex, thereby influencing the epigenetics of endothelial homeostasis.
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spelling doaj-art-be0faebe0ef14efc93f66dd80d9f73532025-08-20T03:52:19ZengNature PortfolioNature Communications2041-17232025-04-0116112310.1038/s41467-025-59003-xS-nitrosylation of EZH2 alters PRC2 assembly, methyltransferase activity, and EZH2 stability to maintain endothelial homeostasisAshima Sakhuja0Ritobrata Bhattacharyya1Yash Tushar Katakia2Shyam Kumar Ramakrishnan3Srinjoy Chakraborty4Hariharan Jayakumar5Shailesh Mani Tripathi6Niyati Pandya Thakkar7Sumukh Thakar8Sandeep Sundriyal9Shibasish Chowdhury10Syamantak Majumder11Department of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Pharmacy, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Pharmacy, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusDepartment of Biological Sciences, Birla Institute of Technology and Science (BITS) Pilani, Pilani CampusAbstract Nitric oxide (NO), a versatile bio-active molecule modulates cellular functions through diverse mechanisms including S-nitrosylation of proteins. Herein, we report S-nitrosylation of selected cysteine residues of EZH2 in endothelial cells, which interplays with its stability and functions. We detect a significant reduction in H3K27me3 upon S-nitrosylation of EZH2 as contributed by the early dissociation of SUZ12 from the PRC2. Moreover, S-nitrosylation of EZH2 causes its cytosolic translocation, ubiquitination, and degradation. Further analysis reveal S-nitrosylation of cysteine 329 induces EZH2 instability, whereas S-nitrosylation of cysteine 700 abrogates its catalytic activity. We further show that S-nitrosylation-dependent regulation of EZH2 maintains endothelial homeostasis in both physiological and pathological settings. Molecular dynamics simulation reveals the inability of SUZ12 to efficiently bind to the SAL domain of EZH2 upon S-nitrosylation. Taken together, our study reports S-nitrosylation-dependent regulation of EZH2 and its associated PRC2 complex, thereby influencing the epigenetics of endothelial homeostasis.https://doi.org/10.1038/s41467-025-59003-x
spellingShingle Ashima Sakhuja
Ritobrata Bhattacharyya
Yash Tushar Katakia
Shyam Kumar Ramakrishnan
Srinjoy Chakraborty
Hariharan Jayakumar
Shailesh Mani Tripathi
Niyati Pandya Thakkar
Sumukh Thakar
Sandeep Sundriyal
Shibasish Chowdhury
Syamantak Majumder
S-nitrosylation of EZH2 alters PRC2 assembly, methyltransferase activity, and EZH2 stability to maintain endothelial homeostasis
Nature Communications
title S-nitrosylation of EZH2 alters PRC2 assembly, methyltransferase activity, and EZH2 stability to maintain endothelial homeostasis
title_full S-nitrosylation of EZH2 alters PRC2 assembly, methyltransferase activity, and EZH2 stability to maintain endothelial homeostasis
title_fullStr S-nitrosylation of EZH2 alters PRC2 assembly, methyltransferase activity, and EZH2 stability to maintain endothelial homeostasis
title_full_unstemmed S-nitrosylation of EZH2 alters PRC2 assembly, methyltransferase activity, and EZH2 stability to maintain endothelial homeostasis
title_short S-nitrosylation of EZH2 alters PRC2 assembly, methyltransferase activity, and EZH2 stability to maintain endothelial homeostasis
title_sort s nitrosylation of ezh2 alters prc2 assembly methyltransferase activity and ezh2 stability to maintain endothelial homeostasis
url https://doi.org/10.1038/s41467-025-59003-x
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