WTAP-mediated m6A modification of TRIM22 promotes diabetic nephropathy by inducing mitochondrial dysfunction via ubiquitination of OPA1

Redox Rep. 2024 Dec;29(1):2404794. doi: 10.1080/13510002.2024.2404794. Epub 2024 Sep 23.

Abstract

Objectives: Diabetic nephropathy (DN) is one of the most serious microvascular complications of diabetes and is the most common cause of end-stage renal disease. Tripartite motif-containing (TRIM) proteins are a large family of E3 ubiquitin ligases that contribute to protein quality control by regulating the ubiquitin - proteasome system. However, the detailed mechanisms through which various TRIM proteins regulate downstream events have not yet been fully elucidated. The current research aimed to determine the function and mechanism of TRIM22 in DN.

Methods: DN models were established by inducing HK-2 cells using high glucose (HG) and diabetic mice (db/db mice). Cell viability, apoptosis, mitochondrial reactive oxygen species, and mitochondrial membrane potential were detected by Cell Counting Kit-8 and flow cytometry, respectively. Pathological changes were evaluated using hematoxylin and eosin, periodic acid schiff and Masson staining. The binding between TRIM22 and optic atrophy 1 (OPA1) was analyzed using co-immunoprecipitation. The m6A level of TRIM22 5'UTR was detected using RNA immunoprecipitation.

Results: TRIM22 was highly expressed in patients with DN. TRIM22 silencing inhibited HG-induced apoptosis and mitochondrial dysfunction in HK-2 cells. Promoting mitochondrial fusion alleviated TRIM22 overexpression-induced cell apoptosis, mitochondrial dysfunction in HK-2 cells, and kidney damage in mice. Mechanistically, TRIM22 interacted with OPA1 and induced its ubiquitination. Wilms tumor 1-associating protein (WTAP) promoted m6A modification of TRIM22 through the m6A reader insulin-like growth factor 2 mRNA-binding protein 1 (IGF2BP1).

Discussion: TRIM22 silencing inhibited the progression of DN by interacting with OPA1 and inducing its ubiquitination. Furthermore, WTAP promoted m6A modification of TRIM22 via IGF2BP1.

Keywords: OPA1; TRIM22; WTAP; diabetic nephropathy; m6A; mitochondrial dysfunction.

MeSH terms

  • Animals
  • Apoptosis
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetic Nephropathies* / metabolism
  • Diabetic Nephropathies* / pathology
  • GTP Phosphohydrolases* / genetics
  • GTP Phosphohydrolases* / metabolism
  • Humans
  • Male
  • Mice
  • Minor Histocompatibility Antigens* / genetics
  • Minor Histocompatibility Antigens* / metabolism
  • Mitochondria* / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Tripartite Motif Proteins* / genetics
  • Tripartite Motif Proteins* / metabolism
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination*

Substances

  • Tripartite Motif Proteins
  • GTP Phosphohydrolases
  • TRIM22 protein, human
  • Minor Histocompatibility Antigens
  • Repressor Proteins
  • Opa1 protein, mouse
  • Ubiquitin-Protein Ligases

Grants and funding

This study was supported by the National Natural Science Foundation of China (81973818) and Youth Project of National Natural Science Foundation of China (82004263).