USP28 participates in high glucose-mediated endothelial dysfunction via deubiquitinating SIRT1 protein in diabetic foot ulcers

J Orthop Surg Res. 2025 Sep 24;20(1):831. doi: 10.1186/s13018-025-06244-7.

Abstract

Background: Silent information regulator sirtuin 1 (SIRT1) protects and improves diabetic wound healing, but SIRT1 undergoes ubiquitination degradation in various cellular environments. The research aims to reveal a mechanism related to SIRT1 deubiquitination to attenuate HG-induced injury in human umbilical vein endothelial cells (HUVECs).

Methods: HUVECs treated with high glucose (HG) were utilized to simulate hyperglycemic conditions in vitro. Cell viability, proliferation, apoptosis, invasion, and angiogenesis were determined by 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2-H-tetrazolium bromide, 5-ethynyl-2'-deoxyuridine, flow cytometry, transwell, and tube formation assays, respectively. Ferroptosis was analyzed by analyzing Fe2+ levels, reactive oxygen species production, and glutathione activity. Endoplasmic reticulum stress (ERS) was evaluated by detecting CHOP and GRP78 protein levels. The interaction between SIRT1 and ubiquitin-specific peptidase 28 (USP28) was determined by co-immunoprecipitation analysis and ubiquitination assays.

Results: Serum SIRT1 mRNA levels were lower in patients with DFUs. SIRT1 overexpression impaired HG-induced injury, ERS, and ferroptosis in HUVECs. USP28 deubiquitinates and stabilizes SIRT1 protein. USP28 overexpression eased HG-induced injury, ERS, and ferroptosis in HUVECs, but the USP28 inhibitor AZ1 counteracted the function of USP28 overexpression. Furthermore, both SIRT1 knockdown and the SIRT1 inhibitor EX-527 undercut USP28 overexpression-mediated protective effect on HUVEC injury, ERS, and ferroptosis under HG stimulation. Additionally, USP28 regulated the NRF2/HO-1 pathway by deubiquitinating SIRT1 in HG-stimulated HUVECs.

Conclusion: USP28 weakens HG-mediated endothelial dysfunction via activating the NRF2/HO-1 pathway through stabilizing SIRT1 protein, indicating that targeting USP28 is the direction for developing clinical strategies for diabetic wound healing.

Keywords: Diabetic; Ferroptosis; SIRT1; USP28; Wound healing.

MeSH terms

  • Apoptosis
  • Cells, Cultured
  • Diabetic Foot* / genetics
  • Diabetic Foot* / metabolism
  • Diabetic Foot* / pathology
  • Endoplasmic Reticulum Chaperone BiP
  • Endoplasmic Reticulum Stress
  • Glucose* / metabolism
  • Glucose* / toxicity
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Male
  • Sirtuin 1* / genetics
  • Sirtuin 1* / metabolism
  • Ubiquitin Thiolesterase* / genetics
  • Ubiquitin Thiolesterase* / metabolism
  • Ubiquitination*

Substances

  • Sirtuin 1
  • Glucose
  • SIRT1 protein, human
  • Ubiquitin Thiolesterase
  • HSPA5 protein, human
  • Endoplasmic Reticulum Chaperone BiP