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Homeostatic Regulation of Intestinal Villous Epithelia by B Lymphocytes¹

Yasuhiro Nishiyama^*,, Hiromasa Hamada^*,¶, Satoshi Nonaka^*, Hiroshi Yamamoto^¶, Masanobu Nanno, Yasuo Katayama, Hidemi Takahashi and Hiromichi Ishikawa^2,*

^* Department of Microbiology, Keio University School of Medicine, Department of Microbiology and Immunology and Second Department of Internal Medicine, Nippon Medical School, and Yakult Central Institute for Microbiological Research, Tokyo, Japan; and ^¶ Department of Immunology, Graduate School of Pharmaceutical Science, Osaka University, Osaka, Japan

The epithelial cell of the small intestine is one of the most rapidly regenerating cells in the body. However, the cellular mechanism and biological significance underlying this rapid regeneration remain elusive. In this study we examined the intestinal epithelia of mutant mice that lack B and/or T cells and those of normal littermates. The absence of B cells in Ig µ-chain mutant mice or B and T cells in recombination-activating gene (RAG)-2^-/- as well as SCID mutant mice was associated with a marked acceleration of epithelial cell turnover and an up-regulation of the expression of MHC class II molecules. No such effects were observed in T cell-deficient TCR- and - double-mutant mice. As far as the goblet cells of villous epithelium are concerned, absolute numbers of them remained the same among these mutant mice that have no B and/or T cells. Alymphoplasia (aly/aly) mutant mice that lacked Peyer’s patches and Ig-producing cells in the lamina propria, but harbored a large number of intestinal mucosal T cells, also displayed a significant acceleration of epithelial cell turnover and, to some extent, up-regulated expression of MHC class II molecules. Notably, the accelerated epithelial cell turnover was not observed and returned to normalcy in the Ig µ-chain mutant mice that had been given antibiotic-containing water. These findings indicate that B cells down-regulate the generation and differentiation of intestinal epithelial cells in the normal wild-type condition and suggest that enteric microorganisms are implicated in the accelerated generation of epithelial cells in mice that have no B cells.

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