Osteopontin-driven T-cell accumulation and function in adipose tissue and liver promoted insulin resistance and MAFLD

Obesity (Silver Spring). 2023 Oct;31(10):2568-2582. doi: 10.1002/oby.23868.

Abstract

Objective: This study investigated the contribution of osteopontin/secreted phosphoprotein 1 (SPP1) to T-cell regulation in initiation of obesity-driven adipose tissue (AT) inflammation and macrophage infiltration and the subsequent impact on insulin resistance (IR) and metabolic-associated fatty liver disease (MAFLD) development.

Methods: SPP1 and T-cell marker expression was evaluated in AT and liver according to type 2 diabetes and MAFLD in human individuals with obesity. The role of SPP1 on T cells was evaluated in Spp1-knockout mice challenged with a high-fat diet.

Results: In humans with obesity, elevated SPP1 expression in AT was parallel to T-cell marker expression (CD4, CD8A) and IR. Weight loss reversed AT inflammation with decreased SPP1 and CD8A expression. In liver, elevated SPP1 expression correlated with MAFLD severity and hepatic T-cell markers. In mice, although Spp1 deficiency did not impact obesity, it did improve AT IR associated with prevention of proinflammatory T-cell accumulation at the expense of regulatory T cells. Spp1 deficiency also decreased ex vivo helper T cell, subtype 1 (Th1) polarization of AT CD4+ and CD8+ T cells. In addition, Spp1 deficiency significantly reduced obesity-associated liver steatosis and inflammation.

Conclusions: Current findings highlight a critical role of SPP1 in the initiation of obesity-driven chronic inflammation by regulating accumulation and/or polarization of T cells. Early targeting of SPP1 could be beneficial for IR and MAFLD treatment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue
  • Animals
  • CD8-Positive T-Lymphocytes
  • Diabetes Mellitus, Type 2*
  • Humans
  • Inflammation
  • Insulin Resistance*
  • Mice
  • Mice, Knockout
  • Non-alcoholic Fatty Liver Disease*
  • Osteopontin* / genetics

Substances

  • Osteopontin
  • Spp1 protein, mouse