Calcium/calmodulin-dependent protein kinase IV (CaMKIV) activation contributes to the pathogenesis of experimental colitis via inhibition of intestinal epithelial cell proliferation

FASEB J. 2019 Jan;33(1):1330-1346. doi: 10.1096/fj.201800535R. Epub 2018 Aug 16.

Abstract

The incidence and prevalence of inflammatory bowel disease (IBD) are increasing worldwide. IBD is known to be multifactorial, but inflammatory signaling within the intestinal epithelium and a subsequent failure of the intestinal epithelial barrier have been shown to play essential roles in disease pathogenesis. CaMKIV is a multifunctional protein kinase associated with inflammation and cell cycle regulation. CaMKIV has been extensively studied in autoimmune diseases, but a role in idiopathic intestinal inflammation has not been described. In this study, active CaMKIV was highly expressed within the intestinal epithelium of humans with ulcerative colitis and wild-type (WT) mice with experimental induced colitis. Clinical disease severity directly correlates with CaMKIV activation, as does expression of proinflammatory cytokines and histologic features of colitis. In WT mice, CaMKIV activation is associated with increases in expression of 2 cell cycle proarrest signals: p53 and p21. Cell cycle arrest inhibits proliferation of the intestinal epithelium and ultimately results in compromised intestinal epithelial barrier integrity, further perpetuating intestinal inflammation during experimental colitis. Using a CaMKIV null mutant mouse, we demonstrate that a loss of CaMKIV protects against murine DSS colitis. Small molecules targeting CaMKIV activation may provide therapeutic benefit for patients with IBD.-Cunningham, K. E., Novak, E. A., Vincent, G., Siow, V. S., Griffith, B. D., Ranganathan, S., Rosengart, M. R., Piganelli, J. D., Mollen, K. P. Calcium/calmodulin-dependent protein kinase IV (CaMKIV) activation contributes to the pathogenesis of experimental colitis via inhibition of intestinal epithelial cell proliferation.

Keywords: CREB; inflammatory bowel disease; intestinal epithelial barrier; intracellular calcium signaling.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 4 / genetics
  • Calcium-Calmodulin-Dependent Protein Kinase Type 4 / metabolism*
  • Cell Proliferation*
  • Colitis / chemically induced
  • Colitis / enzymology*
  • Colitis / pathology*
  • Colitis, Ulcerative / enzymology
  • Colitis, Ulcerative / metabolism
  • Colitis, Ulcerative / pathology
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Dextran Sulfate / toxicity
  • Enzyme Activation
  • Humans
  • Intestinal Mucosa / enzymology
  • Intestinal Mucosa / pathology*
  • Mice
  • Mice, Knockout
  • Signal Transduction

Substances

  • Creb1 protein, mouse
  • Cyclic AMP Response Element-Binding Protein
  • Dextran Sulfate
  • Calcium-Calmodulin-Dependent Protein Kinase Type 4
  • Calcium