A role for intestinal alkaline phosphatase in the maintenance of local gut immunity

Dig Dis Sci. 2011 Apr;56(4):1020-7. doi: 10.1007/s10620-010-1396-x. Epub 2010 Sep 16.

Abstract

Background and aims: Intestinal alkaline phosphatase (IAP) is a gut mucosal defense factor known to dephosphorylate lipopolysaccharide (LPS); however, the role of IAP in the gut response to luminal bacteria remains poorly defined. We investigated immune responses of wild-type (WT) and IAP-knockout (IAP-KO) mice to LPS and Salmonella typhimurium challenges.

Methods: Cryostat sectioning and standard indirect immunohistochemical staining for major histocompatibility complex (MHC) class II molecules were performed on liver tissue from WT and IAP-KO mice. WT and IAP-KO mice were orally gavaged with S. typhimurium; bacterial translocation to mesenteric nodes, liver, and spleen was determined by tissue homogenization and plating. In other experiments, WT and IAP-KO mice received intraperitoneal injections of LPS, with subsequent quantification of complete blood counts and serum interleukin (IL)-6 by enzyme-linked immunosorbent assay (ELISA). WT and IAP-KO whole blood were plated and stimulated with LPS and Pam-3-Cys, followed by cytokine assays.

Results: Immunohistologic liver examinations showed increased expression of MHC class II molecules in IAP-KO mice. Following S. typhimurium challenge, WT mice appeared moribund compared with IAP-KO mice, with increased bacterial translocation. WT mice had >50% decrease (P<.005) in platelets and 1.8-fold (P<.05) increased serum IL-6 compared with IAP-KO mice in response to LPS injections. IAP-KO whole-blood stimulation with LPS and Pam-3-Cys resulted in increased IL-6 and tumor necrosis factor (TNF)-alpha secretion compared with WT.

Conclusions: IAP-KO mice exhibit characteristics consistent with local LPS tolerance. Whole-blood response of IAP-KO mice did not reflect systemic tolerance. These data suggest that IAP is a local immunomodulating factor, perhaps regulating LPS-toll-like receptor 4 (TLR4) interaction between commensal microflora and intestinal epithelium.

Publication types

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

MeSH terms

  • Alkaline Phosphatase / genetics
  • Alkaline Phosphatase / immunology*
  • Animals
  • Bacterial Translocation / immunology
  • Blood Platelets / immunology
  • Blood Platelets / microbiology
  • Histocompatibility Antigens Class II / immunology
  • Interleukin-6 / blood
  • Interleukin-6 / immunology
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / microbiology*
  • Intestines / enzymology
  • Intestines / immunology*
  • Intestines / microbiology*
  • Lipopolysaccharides / immunology
  • Liver / enzymology
  • Liver / immunology
  • Lymph Nodes / immunology
  • Lymph Nodes / microbiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Salmonella Infections / immunology
  • Salmonella typhimurium / immunology
  • Spleen / immunology
  • Spleen / microbiology

Substances

  • Histocompatibility Antigens Class II
  • Interleukin-6
  • Lipopolysaccharides
  • Alkaline Phosphatase