Calcium-mediated oxidative stress: a common mechanism in tight junction disruption by different types of cellular stress

Biochem J. 2017 Feb 20;474(5):731-749. doi: 10.1042/BCJ20160679.

Abstract

The role of reactive oxygen species (ROS) in osmotic stress, dextran sulfate sodium (DSS) and cyclic stretch-induced tight junction (TJ) disruption was investigated in Caco-2 cell monolayers in vitro and restraint stress-induced barrier dysfunction in mouse colon in vivo Live cell imaging showed that osmotic stress, cyclic stretch and DSS triggered rapid production of ROS in Caco-2 cell monolayers, which was blocked by depletion of intracellular Ca2+ by 1,2-bis-(o-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid. Knockdown of CaV1.3 or TRPV6 channels blocked osmotic stress and DSS-induced ROS production and attenuated TJ disruption and barrier dysfunction. N-Acetyl l-cysteine (NAC) and l-NG-Nitroarginine methyl ester (l-NAME) blocked stress-induced TJ disruption and barrier dysfunction. NAC and l-NAME also blocked stress-induced activation of c-Jun N-terminal kinase (JNK) and c-Src. ROS was colocalized with the mitochondrial marker in stressed cells. Cyclosporin A blocked osmotic stress and DSS-induced ROS production, barrier dysfunction, TJ disruption and JNK activation. Mitochondria-targeted Mito-TEMPO blocked osmotic stress and DSS-induced barrier dysfunction and TJ disruption. Chronic restraint stress in mice resulted in the elevation of intracellular Ca2+, activation of JNK and c-Src, and disruption of TJ in the colonic epithelium. Furthermore, corticosterone administration induced JNK and c-Src activation, TJ disruption and protein thiol oxidation in colonic mucosa. The present study demonstrates that oxidative stress is a common signal in the mechanism of TJ disruption in the intestinal epithelium by different types of cellular stress in vitro and bio behavioral stress in vivo.

Keywords: ROS; adherens junction; barrier function; epithelium; intestine; tight junction.

MeSH terms

  • Animals
  • CSK Tyrosine-Protein Kinase
  • Caco-2 Cells
  • Calcium / metabolism*
  • Calcium Channels / genetics
  • Calcium Channels / metabolism
  • Calcium Channels, L-Type / genetics
  • Calcium Channels, L-Type / metabolism
  • Chelating Agents / pharmacology
  • Colon / cytology
  • Colon / drug effects
  • Colon / metabolism*
  • Corticosterone / pharmacology
  • Cyclosporine / pharmacology
  • Dextran Sulfate / pharmacology
  • Egtazic Acid / analogs & derivatives
  • Egtazic Acid / pharmacology
  • Gene Expression Regulation
  • Humans
  • JNK Mitogen-Activated Protein Kinases / genetics
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Male
  • Mechanotransduction, Cellular
  • Mice
  • Mice, Inbred C57BL
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Osmotic Pressure / drug effects
  • Oxidative Stress / drug effects
  • Reactive Oxygen Species / agonists
  • Reactive Oxygen Species / metabolism*
  • Stress, Mechanical
  • Stress, Psychological / genetics
  • Stress, Psychological / metabolism*
  • Stress, Psychological / physiopathology
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism
  • Tight Junctions / drug effects
  • Tight Junctions / metabolism*
  • Tight Junctions / pathology
  • src-Family Kinases / genetics
  • src-Family Kinases / metabolism

Substances

  • Cacna1d protein, mouse
  • Calcium Channels
  • Calcium Channels, L-Type
  • Chelating Agents
  • Reactive Oxygen Species
  • TRPV Cation Channels
  • Trpv6 protein, mouse
  • 1,2-bis(2-aminophenoxy)ethane N,N,N',N'-tetraacetic acid acetoxymethyl ester
  • Egtazic Acid
  • Cyclosporine
  • Dextran Sulfate
  • CSK Tyrosine-Protein Kinase
  • src-Family Kinases
  • CSK protein, human
  • JNK Mitogen-Activated Protein Kinases
  • Calcium
  • NG-Nitroarginine Methyl Ester
  • Corticosterone