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Journal of Histochemistry and Cytochemistry, Vol. 51, 1225-1235, September 2003, Copyright © 2003, The Histochemical Society, Inc.

ARTICLE

Development of Thymic Microenvironments In Vitro Is Oxygen-dependent and Requires Permanent Presence of T-cell Progenitors

Wilfred T.V. Germeraada, Hiroshi Kawamotob, Manami Itoic, Yufei Jiangd, Takashi Amagaic, Yoshimoto Katsurae, and Willem van Ewijkf
a Department of Internal Medicine, Academic Hospital Maastricht, Maastricht, The Netherlands
b Laboratory for Lymphocyte Development, RIKEN Research Center for Allergy and Immunology, Yokohama, Japan
c Department of Immunology and Microbiology, Meiji University of Oriental Medicine, Kyoto, Japan
d Department of Molecular Biology, Princeton University, Princeton, New Jersey
e Department of Cell Regeneration and Transplantation, Nihon University School of Medicine, Tokyo, Japan
f Departments of Immunology and Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands

Correspondence to: Willem van Ewijk, Dept. of Molecular Cell Biology, Center for Electron Microscopy, Leiden University Medical Center, Wassenaarse weg 72, 2333 AL Leiden, The Netherlands. E-mail: vanewijk@lumc.nl

Development of a mature T-cell repertoire in the thymus depends on lympho–stromal interaction between thymocytes and stromal cells. To facilitate intercellular contact, the epithelium in the thymus has differentiated into a unique three-dimensionally (3D)-oriented network. Here we analyze factors influencing induction and maintenance of the 3D configuration of the epithelial network in fetal thymic lobes in vitro. We show that the 3D configuration of the thymic stroma depends on (a) the oxygen pressure in vitro and (b) permanent physical contact between stromal cells and developing thymocytes. This latter feature is demonstrated by incubation of fetal thymic lobes with deoxyguanosine (d-Guo), inducing a 2D-organized thymic stroma, with thymic cysts appearing. Reconstitution of d-Guo-treated lobes with a limited number of flow-sorted T-cell progenitors restores the 3D configuration of the thymic epithelium, but only at high oxygen pressure. This study underlines the plasticity of thymic epithelium and shows that the unique organization of the thymic epithelium is dependent on both oxygen and crosstalk signals derived from developing thymocytes. (J Histochem Cytochem 51:1225–1235, 2003)

Key Words: T-cell development, lympho–stromal interaction, crosstalk, fetal thymic organ culture, thymic epithelium


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