TXNIP-mediated crosstalk between oxidative stress and glucose metabolism

PLoS One. 2024 Feb 8;19(2):e0292655. doi: 10.1371/journal.pone.0292655. eCollection 2024.

Abstract

Thioredoxin-interacting protein (TXNIP) has emerged as a key player in cancer and diabetes since it targets thioredoxin (TRX)-mediated redox regulation and glucose transporter (GLUT)-mediated metabolism. TXNIP consists of two arrestin (ARR, N-ARR and C-ARR) domains at its amino-terminus and two PPxY (PY) motifs and a di-leucine (LL) motif for endocytosis at its carboxyl-terminus. Here, we report that TXNIP shuffles between TRX and GLUTs to regulate homeostasis of intracellular oxidative stress and glucose metabolism. While TXNIP functions as a gatekeeper of TRX by default, it robustly interacted with class I GLUTs through its C-ARR domain upon increase of intracellular reactive oxygen species. This interaction prompted the surface expression downregulation and lysosomal degradation of GLUTs by its carboxyl-terminal LL endocytic signaling motif to attenuate glucose uptake. Consequently, TXNIP expression significantly limited glucose uptake, leading to the suppression of glycolysis, hexosamine biosynthesis, and the pentose phosphate pathway. Our findings establish a fundamental link between ROS and glucose metabolism through TXNIP and provide a promising target for the drug development against GLUT-related metabolic disorders.

MeSH terms

  • Animals
  • Carrier Proteins* / genetics
  • Carrier Proteins* / metabolism
  • Diabetes Mellitus*
  • Glucose / metabolism
  • Humans
  • Mice
  • Oxidative Stress*
  • Reactive Oxygen Species / metabolism
  • Thioredoxins* / genetics
  • Thioredoxins* / metabolism

Substances

  • Carrier Proteins
  • Glucose
  • Reactive Oxygen Species
  • Thioredoxins
  • TXNIP protein, human
  • Txnip protein, mouse

Grants and funding

This research was partly supported by the National Institute of Health CA200422, CA251275, AI140705, AI140718, AI152190, AI171201, and DE028521, the Korea Research Institute of Bioscience and Biotechnology Research Initiative Program KGM9942012 (JUJ), the KRIBB Research Initiative Grant KGM2111733 (MHK), and the National Research Council of Science & Technology Grant CRC-15-02-KRIBB from the Korean Government (IC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.