Caspase-11 attenuates gastrointestinal inflammation and experimental colitis pathogenesis

Am J Physiol Gastrointest Liver Physiol. 2015 Jan 15;308(2):G139-50. doi: 10.1152/ajpgi.00234.2014. Epub 2014 Nov 20.

Abstract

Nucleotide-binding domain and leucine-rich repeat containing protein inflammasome formation plays an essential role in modulating immune system homeostasis in the gut. Recently, a caspase-11 noncanonical inflammasome has been characterized and appears to modulate many biological functions that were previously considered to be solely dependent on caspase-1 and the canonical inflammasome. To better elucidate the function of this noncanonical inflammasome during inflammatory bowel disease, experimental colitis was induced in wild-type and Casp11(-/-) mice utilizing dextran sulfate sodium (DSS). Here, we report that caspase-11 attenuates acute experimental colitis pathogenesis. Casp11(-/-) mice showed significantly increased morbidity and colon inflammation following DSS exposure. Subsequent cytokine analysis revealed that IL-1β and IL-18 levels in the colon were significantly reduced in the Casp11(-/-) mice compared with the wild-type animals. Additional mechanistic studies utilizing IL-1β and IL-18 reconstitution revealed that Casp11(-/-) hypersensitivity was associated with the loss of both of these cytokines. Bone marrow reconstitution experiments further revealed that caspase-11 gene expression and function in both hematopoietic- and nonhematopoietic-derived cells contribute to disease attenuation. Interestingly, unlike caspase-1, caspase-11 does not appear to influence relapsing remitting disease progression or the development of colitis-associated tumorigenesis. Together, these data identify caspase-11 as a critical factor protecting the host during acute DSS-induced colonic injury and inflammation but not during chronic inflammation and tumorigenesis.

Keywords: colitis-associated cancer; inflammasome; inflammatory bowel disease; noncanonical inflammasome; nucleotide-binding domain and leucine-rich repeat containing protein.

Publication types

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

MeSH terms

  • Animals
  • Carcinogenesis / chemically induced
  • Carcinogenesis / metabolism
  • Caspase 1 / metabolism
  • Caspases / genetics*
  • Caspases, Initiator
  • Colitis / chemically induced
  • Colitis / genetics
  • Colitis / metabolism*
  • Dextran Sulfate / adverse effects
  • Disease Models, Animal
  • Gastrointestinal Tract / metabolism*
  • Gene Expression / physiology
  • Homeostasis / genetics
  • Inflammation / metabolism
  • Mice
  • Mice, Knockout

Substances

  • Dextran Sulfate
  • Casp4 protein, mouse
  • Caspases
  • Caspases, Initiator
  • Caspase 1