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Role of Gut Cryptopatches in Early Extrathymic Maturation of Intestinal Intraepithelial T Cells¹

Takatoku Oida^*,, Kenji Suzuki^*, Masanobu Nanno, Yutaka Kanamori^§, Hisashi Saito^¶, Eiro Kubota^¶, Shingo Kato^*, Mamoru Itoh^||, Shuichi Kaminogawa and Hiromichi Ishikawa^2,*

^* Department of Microbiology, Keio University School of Medicine, Tokyo, Japan; Department of Applied Biological Chemistry, University of Tokyo, Tokyo, Japan; Yakult Central Institute for Microbiological Research, Tokyo, Japan; ^§ Department of Pediatric Surgery, Faculty of Medicine, University of Tokyo, Tokyo, Japan; ^¶ Second Department of Oral and Maxillofacial Surgery, Kanagawa Dental School, Kanagawa, Japan; and ^|| Central Institute for Experimental Animals, Kanagawa, Japan

Lympho-hemopoietic progenitors residing in murine gut cryptopatches (CP) have been shown to generate intestinal intraepithelial T cells (IEL). To investigate the role of CP in progenitor maturation, we analyzed IEL in male mice with a truncated mutation of common cytokine receptor -chain (CR^-/Y) in which CP were undetectable. IEL-expressing TCR- (-IEL) were absent, and a drastically reduced number of Thy-1^highCD4⁺ and Thy-1^highCD8ß⁺ ß-IEL were present in CR^-/Y mice, whereas these ß-IEL disappeared from athymic CR^-/Y littermate mice. Athymic CR^-/Y mice possessed a small TCR- and _Eß₇ integrin-negative IEL population, characterized by the disappearance of the extrathymic CD8⁺ subset, that expressed pre-T, RAG-2, and TCR-Cß but not CD3 transcripts. These TCR^- IEL from athymic CR^-/Y mice did not undergo Dß-Jß and V-J joinings, despite normal rearrangements at the TCR-ß and - loci in thymocytes from euthymic CR^-/Y mice. In contrast, athymic severe combined immunodeficient mice in which CP developed normally possessed two major TCR^-_Eß₇⁺ CD8⁺ and CD8^- IEL populations that expressed pre-T, RAG-2, TCR-Cß, and CD3 transcripts. These findings underscore the role of gut CP in the early extrathymic maturation of CD8⁺ IEL, including cell-surface expression of _Eß₇ integrin, CD3 gene transcription, and TCR gene rearrangements.