FTO-mediated RNA m6A methylation regulates synovial aggression and inflammation in rheumatoid arthritis

Fibroblast-like synoviocytes (FLS) plays an important role in synovial inflammation and joint damage in rheumatoid arthritis (RA). As the most abundant mRNA modification, N6-methyladenosine (m6A) is involved in the development of various diseases; however, its role in RA remains to be defined. In th...

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Published inBiochimica et biophysica acta. Molecular basis of disease Vol. 1870; no. 7; p. 167341
Main Authors Li, Ruiru, Kuang, Yu, Niu, Yuanyuan, Zhang, Shuoyang, Chen, Simin, Su, Fan, Wang, Jingnan, Lin, Shuibin, Liu, Di, Shen, Chuyu, Liang, Liuqin, Zheng, Song Guo, Jie, Ligang, Xiao, Youjun, Xu, Hanshi
Format Journal Article
LanguageEnglish
Published Elsevier B.V 01.10.2024
Subjects
ADAMTS15
Fibroblast-like synoviocytes
FTO
Invasion
m6A modification
Migration
Rheumatoid arthritis
FTO
ADAMTS15
m6A modification
Rheumatoid arthritis
Migration
Fibroblast-like synoviocytes
Invasion
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Abstract Fibroblast-like synoviocytes (FLS) plays an important role in synovial inflammation and joint damage in rheumatoid arthritis (RA). As the most abundant mRNA modification, N6-methyladenosine (m6A) is involved in the development of various diseases; however, its role in RA remains to be defined. In this study, we reported the elevated expression of the m6A demethylase fat mass and obesity-associated protein (FTO) in FLS and synovium from RA patients. Functionally, FTO knockdown or treatment with FB23–2, an inhibitor of the mRNA m6A demethylase FTO, inhibited the migration, invasion and inflammatory response of RA FLS, however, FTO-overexpressed RA FLS exhibited increased migration, invasion and inflammatory response. We further demonstrated that FTO promoted ADAMTS15 mRNA stability in an m6A-IGF2BP1 dependent manner. Notably, the severity of arthritis was significantly reduced in CIA mice with FB23–2 administration or CIA rats with intra-articular injection of FTO shRNA. Our results illustrate the contribution of FTO-mediated m6A modification to joint damage and inflammation in RA and suggest that FTO might be a potential therapeutic target in RA. [Display omitted] •Increased FTO promotes the migration, invasion and inflammatory response of RA FLS.•FTO controls RA FLS functions by enhancing ADAMTS15 mRNA stability in an m6A-IGF2BP1dependent manner.•The FTO-mediated m6A modification plays an important role in regulating synovial inflammation and joint damage in RA.
AbstractList Fibroblast-like synoviocytes (FLS) plays an important role in synovial inflammation and joint damage in rheumatoid arthritis (RA). As the most abundant mRNA modification, N6-methyladenosine (m6A) is involved in the development of various diseases; however, its role in RA remains to be defined. In this study, we reported the elevated expression of the m6A demethylase fat mass and obesity-associated protein (FTO) in FLS and synovium from RA patients. Functionally, FTO knockdown or treatment with FB23-2, an inhibitor of the mRNA m6A demethylase FTO, inhibited the migration, invasion and inflammatory response of RA FLS, however, FTO-overexpressed RA FLS exhibited increased migration, invasion and inflammatory response. We further demonstrated that FTO promoted ADAMTS15 mRNA stability in an m6A-IGF2BP1 dependent manner. Notably, the severity of arthritis was significantly reduced in CIA mice with FB23-2 administration or CIA rats with intra-articular injection of FTO shRNA. Our results illustrate the contribution of FTO-mediated m6A modification to joint damage and inflammation in RA and suggest that FTO might be a potential therapeutic target in RA.Fibroblast-like synoviocytes (FLS) plays an important role in synovial inflammation and joint damage in rheumatoid arthritis (RA). As the most abundant mRNA modification, N6-methyladenosine (m6A) is involved in the development of various diseases; however, its role in RA remains to be defined. In this study, we reported the elevated expression of the m6A demethylase fat mass and obesity-associated protein (FTO) in FLS and synovium from RA patients. Functionally, FTO knockdown or treatment with FB23-2, an inhibitor of the mRNA m6A demethylase FTO, inhibited the migration, invasion and inflammatory response of RA FLS, however, FTO-overexpressed RA FLS exhibited increased migration, invasion and inflammatory response. We further demonstrated that FTO promoted ADAMTS15 mRNA stability in an m6A-IGF2BP1 dependent manner. Notably, the severity of arthritis was significantly reduced in CIA mice with FB23-2 administration or CIA rats with intra-articular injection of FTO shRNA. Our results illustrate the contribution of FTO-mediated m6A modification to joint damage and inflammation in RA and suggest that FTO might be a potential therapeutic target in RA.
Fibroblast-like synoviocytes (FLS) plays an important role in synovial inflammation and joint damage in rheumatoid arthritis (RA). As the most abundant mRNA modification, N6-methyladenosine (m6A) is involved in the development of various diseases; however, its role in RA remains to be defined. In this study, we reported the elevated expression of the m6A demethylase fat mass and obesity-associated protein (FTO) in FLS and synovium from RA patients. Functionally, FTO knockdown or treatment with FB23–2, an inhibitor of the mRNA m6A demethylase FTO, inhibited the migration, invasion and inflammatory response of RA FLS, however, FTO-overexpressed RA FLS exhibited increased migration, invasion and inflammatory response. We further demonstrated that FTO promoted ADAMTS15 mRNA stability in an m6A-IGF2BP1 dependent manner. Notably, the severity of arthritis was significantly reduced in CIA mice with FB23–2 administration or CIA rats with intra-articular injection of FTO shRNA. Our results illustrate the contribution of FTO-mediated m6A modification to joint damage and inflammation in RA and suggest that FTO might be a potential therapeutic target in RA. [Display omitted] •Increased FTO promotes the migration, invasion and inflammatory response of RA FLS.•FTO controls RA FLS functions by enhancing ADAMTS15 mRNA stability in an m6A-IGF2BP1dependent manner.•The FTO-mediated m6A modification plays an important role in regulating synovial inflammation and joint damage in RA.
ArticleNumber 167341
Author Zheng, Song Guo
Liang, Liuqin
Wang, Jingnan
Kuang, Yu
Niu, Yuanyuan
Li, Ruiru
Shen, Chuyu
Jie, Ligang
Chen, Simin
Xu, Hanshi
Lin, Shuibin
Su, Fan
Liu, Di
Xiao, Youjun
Zhang, Shuoyang
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  givenname: Ruiru
  surname: Li
  fullname: Li, Ruiru
  organization: Department of Rheumatology and Immunology, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
– sequence: 2
  givenname: Yu
  surname: Kuang
  fullname: Kuang, Yu
  organization: Department of Rheumatology and Immunology, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
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  givenname: Yuanyuan
  surname: Niu
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  organization: Department of General Practice, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
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  givenname: Shuoyang
  surname: Zhang
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  givenname: Fan
  surname: Su
  fullname: Su, Fan
  organization: Department of Geriatrics, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
– sequence: 7
  givenname: Jingnan
  surname: Wang
  fullname: Wang, Jingnan
  organization: Department of Rheumatology and Immunology, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
– sequence: 8
  givenname: Shuibin
  surname: Lin
  fullname: Lin, Shuibin
  organization: Center for Translational Medicine, The First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
– sequence: 9
  givenname: Di
  surname: Liu
  fullname: Liu, Di
  organization: Department of Rheumatology and Immunology, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
– sequence: 10
  givenname: Chuyu
  surname: Shen
  fullname: Shen, Chuyu
  organization: Department of Rheumatology and Immunology, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
– sequence: 11
  givenname: Liuqin
  surname: Liang
  fullname: Liang, Liuqin
  organization: Department of Rheumatology and Immunology, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
– sequence: 12
  givenname: Song Guo
  surname: Zheng
  fullname: Zheng, Song Guo
  organization: Department of Immunology, School of Cell and Gene Therapy, Song Jiang Research Institutes, Shanghai Jiaotong University, School of Medicine, Shanghai, China
– sequence: 13
  givenname: Ligang
  surname: Jie
  fullname: Jie, Ligang
  email: jieligang1976@smu.edu.cn
  organization: Department of Rheumatology, Zhujiang Hospital of Southern Medical University, Guangzhou, Guangdong Province, China
– sequence: 14
  givenname: Youjun
  surname: Xiao
  fullname: Xiao, Youjun
  email: xiaoyouj@mail2.sysu.edu.cn
  organization: Department of Rheumatology and Immunology, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
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  givenname: Hanshi
  surname: Xu
  fullname: Xu, Hanshi
  email: xuhanshi@mail.sysu.edu.cn
  organization: Department of Rheumatology and Immunology, the First Affiliated Hospital, Sun Yat-sen University, No.58 Zhongshan Er Road, Guangzhou 510080, Guangdong Province, China
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Keywords FTO
ADAMTS15
m6A modification
Rheumatoid arthritis
Migration
Fibroblast-like synoviocytes
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Snippet Fibroblast-like synoviocytes (FLS) plays an important role in synovial inflammation and joint damage in rheumatoid arthritis (RA). As the most abundant mRNA...
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StartPage 167341
SubjectTerms ADAMTS15
Fibroblast-like synoviocytes
FTO
Invasion
m6A modification
Migration
Rheumatoid arthritis
Title FTO-mediated RNA m6A methylation regulates synovial aggression and inflammation in rheumatoid arthritis
URI https://dx.doi.org/10.1016/j.bbadis.2024.167341
https://www.proquest.com/docview/3082626936/abstract/
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