SNORD80-guided 2’-O-methylation stabilizes the lncRNA GAS5 to regulate cellular stress responses

L Liang Xu X Xiao Hong Zhao (School of Biomedical Sciences and Pharmacy, The University of Newcastle) Y Yuan Yuan Zhang (School of Biomedical Sciences and Pharmacy, The University of Newcastle) M Meng Yao Zhang (Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University) L Long Yue Zhang (Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University) K Kai Hong Ye (Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University) L Liu Teng (Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University) M Man Man Han (Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University) Y Yi Meng Yue (Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University) J Jiezhen Yang (Department of Pathology, Zhongshan Hospital (Xiamen Branch), Fudan University) R Rachel Ogle (School of Biomedical Sciences and Pharmacy, The University of Newcastle) J Jacob Netherton (School of Biomedical Sciences and Pharmacy, The University of Newcastle) D Deng Tang (West China School of Basic Medical Science and Forensic Medicine, Sichuan University) S Siqi Lan (West China School of Basic Medical Science and Forensic Medicine, Sichuan University) M Mark Baker (School of Biomedical Sciences and Pharmacy, The University of Newcastle) Y Yan Ye (State Key Laboratory of Chemistry for NBC Hazards Protection, College of Chemistry) T Tao Liu Y Yu Fang Wang (West China School of Basic Medical Science and Forensic Medicine, Sichuan University) X Xu Dong Zhang (School of Biomedical Sciences and Pharmacy, The University of Newcastle) T Tianli Fan (Department of Pharmacology, School of Basic Medicine, Zhengzhou University) L Lei Jin

Abstract

The introns of the gene encoding the long noncoding RNA (lncRNA) GAS5 host up to 10 C/D box small nucleolar RNAs (snoRNAs). However, whether there is a regulatory and functional relationship between these snoRNAs and GAS5 is unknown. Here, we show that the expression of SNORD80, but not the other snoRNAs, parallels GAS5 expression and is regulated alongside GAS5 in response to cellular stress. The 2′-O-methylation at the A496 site, located within a segment of GAS5 complementing the conserved RNA-binding region on SNORD80, promotes GAS5 stability and consequent upregulation. This methylation requires SNORD80, as it is diminished by knockdown of SNORD80 and increased by SNORD80 overexpression, similar to the effects of manipulating the expression of fibrillarin, the methyltransferase of the box C/D small nucleolar ribonucleoprotein particle (snoRNP). The upregulation of SNORD80 in response to cellular stress is due to an enhancement in its stability, which is associated with an increase in its interaction with fibrillarin. Collectively, these results identify a role for SNORD80 in guiding 2′-O-methylation to stabilize GAS5. This uncovers a feedforward regulatory loop at the GAS5 gene locus in response to cellular stress and sheds light on posttranscriptional mechanisms governing lncRNA expression.

Article Details

Volume / Issue Vol. 122, Issue 7
Published February 18, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (21)

L

Liang Xu

X

Xiao Hong Zhao

School of Biomedical Sciences and Pharmacy, The University of Newcastle

Y

Yuan Yuan Zhang

School of Biomedical Sciences and Pharmacy, The University of Newcastle

M

Meng Yao Zhang

Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University

L

Long Yue Zhang

Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University

K

Kai Hong Ye

Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University

L

Liu Teng

Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University

M

Man Man Han

Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University

Y

Yi Meng Yue

Translational Research Institute, Henan Provincial and Zhengzhou City Key laboratory of Non-coding RNA and Cancer Metabolism, Henan International Join Laboratory of Non-coding RNA and Metabolism in Cancer, Henan Provincial People’s Hospital, Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University

J

Jiezhen Yang

Department of Pathology, Zhongshan Hospital (Xiamen Branch), Fudan University

R

Rachel Ogle

School of Biomedical Sciences and Pharmacy, The University of Newcastle

J

Jacob Netherton

School of Biomedical Sciences and Pharmacy, The University of Newcastle

D

Deng Tang

West China School of Basic Medical Science and Forensic Medicine, Sichuan University

S

Siqi Lan

West China School of Basic Medical Science and Forensic Medicine, Sichuan University

M

Mark Baker

School of Biomedical Sciences and Pharmacy, The University of Newcastle

Y

Yan Ye

State Key Laboratory of Chemistry for NBC Hazards Protection, College of Chemistry

T

Tao Liu

Y

Yu Fang Wang

West China School of Basic Medical Science and Forensic Medicine, Sichuan University

X

Xu Dong Zhang

School of Biomedical Sciences and Pharmacy, The University of Newcastle

T

Tianli Fan

Department of Pharmacology, School of Basic Medicine, Zhengzhou University

L

Lei Jin