Colitis immunoregulation by CD8+ T cell requires T cell cytotoxicity and B cell peptide antigen presentation

Am J Physiol Gastrointest Liver Physiol. 2008 Sep;295(3):G485-92. doi: 10.1152/ajpgi.90221.2008. Epub 2008 Jul 10.

Abstract

Deficient immunoregulation by CD4+ T cells is an important susceptibility trait for inflammatory bowel disease, but the role of other regulatory cell types is less understood. This study addresses the role and mechanistic interaction of B cells and CD8+ T cells in controlling immune-mediated colitis. The genetic requirements for B cells and CD8+ T cells to confer protective immunoregulation were assessed by cotransfer with colitogenic Galphai2-/- T cells into immune-deficient mice. Disease activity in Galphai2-/- T cell recipients was evaluated by CD4+ T intestinal lymphocyte abundance, cytokine production levels, and large intestine histology. B cells deficient in B7.1/B7.2, CD40, major histocompatibility complex (MHC) II (Abb), or native B cell antigen receptor (MD4) were competent for colitis protection. However, transporter-1-deficient B cells failed to protect, indicating a requirement for peptide MHC I presentation to CD8+ T cells. CD8+ T cells deficient in native T cell receptor repertoire (OT-1) or cytolysis (perforin-/-) also were nonprotective. These finding reveal an integrated role for antigen-specific perforin-dependent CD8+ T cell cytotoxicity in colitis immunoregulatory and its efficient induction by a subset of mesenteric B lymphocytes.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily B, Member 2
  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism
  • Adoptive Transfer
  • Animals
  • Antigen Presentation*
  • Antigens / genetics
  • Antigens / metabolism*
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • B7-1 Antigen / metabolism
  • B7-2 Antigen / metabolism
  • CD4-Positive T-Lymphocytes / immunology
  • CD40 Antigens / metabolism
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / transplantation
  • Colitis / immunology*
  • Colitis / metabolism
  • Colitis / pathology
  • Colitis / prevention & control
  • Cytokines / metabolism
  • Cytotoxicity, Immunologic*
  • Disease Models, Animal
  • Female
  • GTP-Binding Protein alpha Subunit, Gi2 / genetics
  • GTP-Binding Protein alpha Subunit, Gi2 / metabolism
  • Histocompatibility Antigens Class II / metabolism
  • Intestine, Large / immunology*
  • Intestine, Large / metabolism
  • Intestine, Large / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Perforin / genetics
  • Perforin / metabolism
  • Receptors, Antigen, B-Cell / metabolism

Substances

  • ATP Binding Cassette Transporter, Subfamily B, Member 2
  • ATP-Binding Cassette Transporters
  • Antigens
  • B7-1 Antigen
  • B7-2 Antigen
  • CD40 Antigens
  • Cytokines
  • Histocompatibility Antigens Class II
  • Receptors, Antigen, B-Cell
  • Tap1 protein, mouse
  • Perforin
  • GTP-Binding Protein alpha Subunit, Gi2
  • Gnai2 protein, mouse