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characterization of the enzyme for 5-hydroxymethyluridine production and its role in silencing transposable elements in dinoflagellates

Characterization of the enzyme for 5-hydroxymethyluridine production and its role in silencing transposable elements in dinoflagellates.

机构信息

Department of Human Cell Biology and Genetics, Joint Laboratory of Guangdong & Hong Kong Universities for Vascular Homeostasis and Diseases, School of Medicine, Shenzhen 518055, China.

The First Affiliated Hospital of Zhengzhou University & Institute of Reproductive Health, Henan Academy of Innovations in Medical Science, Zhengzhou 450000, China.

出版信息

Proc Natl Acad Sci U S A. 2024 Nov 12;121(46):e2400906121. doi: 10.1073/pnas.2400906121. Epub 2024 Nov 7.

DOI:10.1073/pnas.2400906121
PMID:39508766
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC11572971/
Abstract

Dinoflagellate chromosomes are extraordinary, as their organization is independent of architectural nucleosomes unlike typical eukaryotes and shows a cholesteric liquid crystal state. 5-hydroxymethyluridine (5hmU) is present at unusually high levels and its function remains an enigma in dinoflagellates chromosomal DNA for several decades. Here, we demonstrate that 5hmU contents vary among different dinoflagellates and are generated through thymidine hydroxylation. Importantly, we identified the enzyme, which is a putative dinoflagellate TET/JBP homolog, catalyzing 5hmU production using both in vivo and in vitro biochemical assays. Based on the near-chromosomal level genome assembly of dinoflagellate , we depicted a comprehensive 5hmU landscape and found that 5hmU loci are significantly enriched in repeat elements. Moreover, inhibition of 5hmU via dioxygenase inhibitor leads to transcriptional activation of 5hmU-marked transposable elements, implying that 5hmU appears to serve as an epigenetic mark for silencing transposon. Together, our results revealed the biogenesis, genome-wide landscape, and molecular function of dinoflagellate 5hmU, providing mechanistic insight into the function of this enigmatic DNA mark.

摘要

甲藻染色体结构独特，其组织与典型真核生物不同，不依赖于建筑核小体，而是呈现胆甾型液晶状态。5-羟甲基尿嘧啶（5hmU）的含量异常高，但几十年来，其在甲藻染色体 DNA 中的功能仍然是一个谜。本研究表明，5hmU 含量在不同的甲藻中存在差异，是通过胸苷羟化产生的。重要的是，我们通过体内和体外生化实验鉴定了一种酶，它是一种假定的甲藻 TET/JBP 同源物，可催化 5hmU 的产生。基于甲藻近染色体水平的基因组组装，我们描绘了一个全面的 5hmU 图谱，发现 5hmU 位点在重复元件中显著富集。此外，通过双加氧酶抑制剂抑制 5hmU 会导致 5hmU 标记的转座元件的转录激活，这表明 5hmU 似乎作为沉默转座子的表观遗传标记。总之，我们的研究结果揭示了甲藻 5hmU 的生物发生、全基因组景观和分子功能，为这一神秘 DNA 标记的功能提供了机制见解。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/8e1338c19b78/pnas.2400906121fig06.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/6750cf5266c8/pnas.2400906121fig01.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/cb5c6e19ff27/pnas.2400906121fig02.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/c8a55ca21888/pnas.2400906121fig03.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/a232fa37f857/pnas.2400906121fig04.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/a6185d27a572/pnas.2400906121fig05.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/8e1338c19b78/pnas.2400906121fig06.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/6750cf5266c8/pnas.2400906121fig01.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/cb5c6e19ff27/pnas.2400906121fig02.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/c8a55ca21888/pnas.2400906121fig03.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/a232fa37f857/pnas.2400906121fig04.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/a6185d27a572/pnas.2400906121fig05.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/fefc/11572971/8e1338c19b78/pnas.2400906121fig06.jpg

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