Upregulation of KCa3.1 K(+) channel in mesenteric lymph node CD4(+) T lymphocytes from a mouse model of dextran sodium sulfate-induced inflammatory bowel disease

Am J Physiol Gastrointest Liver Physiol. 2014 May 15;306(10):G873-85. doi: 10.1152/ajpgi.00156.2013. Epub 2014 Mar 27.

Abstract

The intermediate-conductance Ca(2+)-activated K(+) channel KCa3.1/KCNN4 plays an important role in the modulation of Ca(2+) signaling through the control of the membrane potential in T lymphocytes. Here, we study the involvement of KCa3.1 in the enlargement of the mesenteric lymph nodes (MLNs) in a mouse model of inflammatory bowel disease (IBD). The mouse model of IBD was prepared by exposing male C57BL/6J mice to 5% dextran sulfate sodium for 7 days. Inflammation-induced changes in KCa3.1 activity and the expressions of KCa3.1 and its regulators in MLN CD4(+) T lymphocytes were monitored by real-time PCR, Western blot, voltage-sensitive dye imaging, patch-clamp, and flow cytometric analyses. Concomitant with an upregulation of KCa3.1a and nucleoside diphosphate kinase B (NDPK-B), a positive KCa3.1 regulator, an increase in KCa3.1 activity was observed in MLN CD4(+) T lymphocytes in the IBD model. Pharmacological blockade of KCa3.1 elicited the following results: 1) a significant decrease in IBD disease severity, as assessed by diarrhea, visible fecal blood, inflammation, and crypt damage of the colon and MLN enlargement compared with control mice, and 2) the restoration of the expression levels of KCa3.1a, NDPK-B, and Th1 cytokines in IBD model MLN CD4(+) T lymphocytes. These findings suggest that the increase in KCa3.1 activity induced by the upregulation of KCa3.1a and NDPK-B may be involved in the pathogenesis of IBD by mediating the enhancement of the proliferative response in MLN CD4(+) T lymphocyte and, therefore, that the pharmacological blockade of KCa3.1 may decrease the risk of IBD.

Keywords: CD4+ T lymphocyte; KCa3.1; TRAM-34; inflammatory bowel disease; mesenteric lymph node.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / metabolism*
  • DNA-Binding Proteins / biosynthesis
  • Dextran Sulfate
  • Disease Models, Animal
  • Inflammatory Bowel Diseases / chemically induced
  • Inflammatory Bowel Diseases / drug therapy
  • Inflammatory Bowel Diseases / physiopathology*
  • Intermediate-Conductance Calcium-Activated Potassium Channels / metabolism*
  • Lymph Nodes / metabolism*
  • Lymph Nodes / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NM23 Nucleoside Diphosphate Kinases / biosynthesis*
  • Nuclear Proteins / biosynthesis
  • Pyrazoles / therapeutic use
  • Ubiquitin-Protein Ligases
  • Up-Regulation

Substances

  • DNA-Binding Proteins
  • Intermediate-Conductance Calcium-Activated Potassium Channels
  • Kcnn4 protein, mouse
  • NM23 Nucleoside Diphosphate Kinases
  • Nuclear Proteins
  • Pyrazoles
  • TRAM 34
  • Dextran Sulfate
  • Trim27 protein, mouse
  • Ubiquitin-Protein Ligases
  • Nme2 protein, mouse