Molecular Basis for Hematopoietic/Mesenchymal Interaction during Initiation of Peyer's Patch Organogenesis

doi:10.1084/jem.193.5.621

Published online 5 March 2001.

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© The Rockefeller University Press, 0022-1007/2001/3/621/ $5.00
The Journal of Experimental Medicine, Volume 193, Number 5, March 5, 2001 621-630

Original Article

Molecular Basis for Hematopoietic/Mesenchymal Interaction during Initiation of Peyer's Patch Organogenesis

Kenya Honda^a,b, Hiroyasu Nakano^d,e, Hisahiro Yoshida^a, Satomi Nishikawa^a, Paul Rennert^f, Koichi Ikuta^c, Masakatsu Tamechika^e, Kazuhito Yamaguchi^h, Tetsuo Fukumoto^g, Tsutomu Chiba^b, and Shin-Ichi Nishikawa^a
^a Department of Molecular Genetics, Graduate School of Medicine, Kyoto University, Kyoto 606-8507, Japan
^b Department of Gastroenterology, Graduate School of Medicine, Kyoto University, Kyoto 606-8507, Japan
^c Department of Medical Chemistry, Graduate School of Medicine, Kyoto University, Kyoto 606-8507, Japan
^d Department of Immunology, Juntendo University, School of Medicine, Tokyo 113-8421, Japan
^e Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation, Tokyo 101-0062, Japan
^f Department of Immunology, Biogen, Incorporated, Cambridge, Massachusetts 02142
^g Department of Anatomy, Yamaguchi University School of Medicine, Ube 755-8505, Japan
^h Institute of Laboratory Animals, Yamaguchi University School of Medicine, Ube 755-8505, Japan

Correspondence to: Kenya Honda, the Department of Molecular Genetics, Graduate School of Medicine, Kyoto University, Syogoin-Kawaharacho 53, Sakyo-ku, Kyoto 606-8507, Japan. Tel:81-75-751-4161 Fax:81-75-751-4169 E-mail:khonda{at}virus.kyoto-u.ac.jp.

Mice deficient in lymphotoxin ß receptor (LTßR)or interleukin 7 receptor ${alpha}$ (IL-7R ${alpha}$ ) lack Peyer's patches (PPs).Deficiency in CXC chemokine receptor 5 (CXCR5) also severelyaffects the development of PPs. A molecular network involvingthese three signaling pathways has been implicated in PP organogenesis,but it remains unclear how they are connected during this process.We have shown that PP organogenesis is initiated at sites containingIL-7R ${alpha}$ ⁺ lymphoid cells and vascular cell adhesion molecule (VCAM)-1/intercellularadhesion molecule (ICAM)-1 expressing nonlymphoid elements.Here we characterize these lymphoid and nonlymphoid componentsin terms of chemokine signals. The lymphoid population expressesCXCR5 and has a strong chemotactic response to B lymphocytechemoattractant (BLC). Importantly, chemokines produced by VCAM-1⁺ICAM-1⁺nonlymphoid cells mediate the recruitment of lymphoid cells.Furthermore, we show that these VCAM-1⁺ICAM-1⁺ cells are mesenchymalcells that are activated by lymphoid cells through the LTßRto express adhesion molecules and chemokines. Thus, promotionof PP development relies on mutual interaction between mesenchymaland lymphoid cells.

Key Words: lymphoid tissue, lymphotoxin, interleukin 7, chemokines, chemotaxis

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