Thioredoxin-interacting protein is required for endothelial NLRP3 inflammasome activation and cell death in a rat model of high-fat diet

Diabetologia. 2014 Feb;57(2):413-23. doi: 10.1007/s00125-013-3101-z. Epub 2013 Nov 8.

Abstract

Aims/hypothesis: Obesity and hypertension, known pro-inflammatory states, are identified determinants for increased retinal microvascular abnormalities. However, the molecular link between inflammation and microvascular degeneration remains elusive. Thioredoxin-interacting protein (TXNIP) is recognised as an activator of the NOD-like receptor pyrin domain containing-3 (NLRP3) inflammasome. This study aims to examine TXNIP expression and elucidate its role in endothelial inflammasome activation and retinal lesions.

Methods: Spontaneously hypertensive (SHR) and control Wistar (W) rats were compared with groups fed a high-fat diet (HFD) (W+F and SHR+F) for 8-10 weeks.

Results: Compared with W controls, HFD alone or in combination with hypertension significantly induced formation of acellular capillaries, a hallmark of retinal ischaemic lesions. These effects were accompanied by significant increases in lipid peroxidation, nitrotyrosine and expression of TXNIP, nuclear factor κB, TNF-α and IL-1β. HFD significantly increased interaction of TXNIP-NLRP3 and expression of cleaved caspase-1 and cleaved IL-1β. Immunolocalisation studies identified TXNIP expression within astrocytes and Müller cells surrounding retinal endothelial cells. To model HFD in vitro, human retinal endothelial (HRE) cells were stimulated with 400 μmol/l palmitate coupled to BSA (Pal-BSA). Pal-BSA triggered expression of TXNIP and its interaction with NLRP3, resulting in activation of caspase-1 and IL-1β in HRE cells. Silencing Txnip expression in HRE cells abolished Pal-BSA-mediated cleaved IL-1β release into medium and cell death, evident by decreases in cleaved caspase-3 expression and the proportion of live to dead cells.

Conclusions/interpretation: These findings provide the first evidence for enhanced TXNIP expression in hypertension and HFD-induced retinal oxidative/inflammatory response and suggest that TXNIP is required for HFD-mediated activation of the NLRP3 inflammasome and the release of IL-1β in endothelial cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Carrier Proteins / biosynthesis
  • Carrier Proteins / metabolism*
  • Caspase Inhibitors / metabolism*
  • Cell Cycle Proteins
  • Cell Death
  • Diet, High-Fat
  • Endothelial Cells / metabolism*
  • Eye Diseases / metabolism*
  • Eye Diseases / pathology
  • Inflammasomes / metabolism*
  • Inflammation / metabolism
  • Male
  • Microcirculation
  • NF-kappa B / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Obesity / complications
  • Obesity / metabolism*
  • Oxidative Stress
  • Rats
  • Rats, Wistar
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Retina / metabolism*
  • Retina / pathology

Substances

  • Carrier Proteins
  • Caspase Inhibitors
  • Cell Cycle Proteins
  • Inflammasomes
  • NF-kappa B
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, rat
  • Receptors, Cytoplasmic and Nuclear
  • TXNIP protein, rat