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Compartments T Cell + and CD8 + Development of CD4 Comparative Contribution of CD1 On Comparative Contribution of CD1 on the Development of CD4 + and CD8+ T Cell Compartments This information is current as Bin Wang, Taehoon Chun and Chyung-Ru Wang of September 29, 2021. J Immunol 2000; 164:739-745; ; doi: 10.4049/jimmunol.164.2.739 http://www.jimmunol.org/content/164/2/739 Downloaded from References This article cites 57 articles, 36 of which you can access for free at: http://www.jimmunol.org/content/164/2/739.full#ref-list-1 Why The JI? Submit online. http://www.jimmunol.org/ • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average by guest on September 29, 2021 Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2000 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Comparative Contribution of CD1 on the Development of CD4؉ and CD8؉ T Cell Compartments1 Bin Wang, Taehoon Chun, and Chyung-Ru Wang2 CD1 molecules are MHC class I-like glycoproteins whose expression is essential for the development of a unique subset of T cells, the NK T cells. To evaluate to what extent CD1 contributes to the development of CD4؉ and CD8؉ T cells, we generated CD1oIIo and CD1oTAPo mice and compared the generation of T cells in these double-mutant mice and IIo or TAPo mice. FACS analysis showed that the number of CD4؉ T cells in CD1oIIo mice was reduced significantly compared with the corresponding population in IIo mice. Both CD4؉ NK1.1؉ and the CD4؉ NK1.1؊ population were reduced in CD1oIIo mice, suggesting that CD1 can select not only CD4؉ NK1.1؉ T cells but also some NK1.1؊ CD4؉ T cells. Functional analysis showed that the residual CD4؉ cells in CD1oIIo can secrete large amounts of IFN-␥ and a significant amount of IL-4 during primary stimulation with anti-CD3, sug- ؉ gesting that this population may be enriched for NK T cells restricted by other class I molecules. In contrast to the CD4 Downloaded from population, no significant differences in the CD8؉ T cell compartment can be detected between TAPo and CD1oTAPo mice in all lymphoid tissues tested, including intestinal intraepithelial lymphocytes. Our data suggest that, unlike other MHC class I mole- :cules, CD1 does not contribute in a major way to the development of CD8؉ T cells. The Journal of Immunology, 2000, 164 739–745. he CD1 molecules are cell surface glycoproteins that have (IEC) (20). This unique localization of hCD1d may allow recog- http://www.jimmunol.org/ been conserved throughout mammalian evolution (1–6). nition by intraepithelial lymphocytes (IEL). However, the expres- T The overall structure of CD1 resembles that of MHC class sion of CD1 on mouse IEC is still controversial, as anti-CD1 mAbs I molecules, with three extracellular domains (␣1, ␣2, and ␣3), a differ in detection of CD1 expression on mouse IEC (15–17, 21). transmembrane region, and a short cytoplasmic tail. The ␣3 do- Unlike MHC class I molecules, the expression of CD1 in both ␤ ␤ 3 main is noncovalently associated with 2-microglobulin ( 2m). human and mouse does not require functional TAP (22, 23). Unlike classical class I molecules, CD1 is relatively nonpolymor- Study of T cell development in mutant mice lacking MHC mol- phic and is expressed at lower levels (5, 7). Thus, CD1 molecules ecules revealed that MHC class I and class II molecules play a were classified as a member of MHC class Ib family. However, central role in the development of CD8ϩ and CD4ϩ T cells, re- unlike most of MHC class Ib genes, CD1 genes map outside of spectively (24–28). Recent studies using CD1-deficient mice have by guest on September 29, 2021 MHC both in humans and mice (8, 9), and they are significantly shown that CD1 is essential for the development of a major subset divergent from other class I genes. The sequence homology be- of NK1ϩ T cells (29–31), which use an invariant TCR ␣-chain in tween CD1 and other class I molecules is only 25–30% (5). The conjunction with a restricted set of TCR ␤-chains (32, 33). These same degree of homology was also detected between CD1 and NK1ϩ T cells promptly produce large amounts of cytokines, in class II molecules, suggesting that CD1 may represent a third lin- particular IL-4, upon primary stimulation by TCR engagement eage of Ag-presenting molecules (10). Consistent with this idea, (34). However, the role of CD1 in the development of other T cell CD1 molecules have been shown to present lipid and glycolipid subsets was unclear. Due to the presence of other MHC class I and Ags to T cells (11–14), while MHC class I and class II molecules class II molecules in CD1o mice, no significant changes in either present peptide Ags to T cells. CD4ϩ or CD8ϩ population were detected in CD1o mice (29–31). Mouse CD1 is encoded by two closely related genes, CD1d1 Yet, several lines of evidence suggested that CD1 might be in- and CD1d2 (7). CD1d1 is widely expressed on cells of multiple volved in the development of some CD4ϩ and CD8ϩ T cells. In hemopoietic lineages (15–17), including B and T cells, macro- MHC class II-deficient mice, a small population of CD4ϩ T cells phages, and dendritic cells, while CD1d2 can be detected only on can be detected in the periphery (26–28). Many of the hybridomas thymocytes (18, 19). Human CD1d can be detected in the apical derived from the CD4ϩ T cells of class II-deficient mice have been and lateral regions of small and large intestinal epithelial cells shown to recognize CD1, implicating a role for CD1 in the devel- opment of some CD4ϩ T cells (35). Although the expression of the ␤ o class I molecules is reduced significantly both in 2m and in Gwen Knapp Center for Lupus and Immunology Research, Committee on Immunol- o ϩ o ogy, and Department of Pathology, University of Chicago, Chicago, IL 60637 TAP mice, the residual number of CD8 T cells in TAP mice is ␤ o Received for publication July 27, 1999. Accepted for publication November 4, 1999. slightly higher than that in 2m mice (36–38). One possible source of these residual CD8ϩ T cells may be selection by TAP- The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance independent, nonclassical class I molecules, such as CD1 and TL with 18 U.S.C. Section 1734 solely to indicate this fact. molecules (22, 23, 39). 1 This work was supported by National Institutes of Health Grant R01-AI43407 (to In this report we have generated CD1oIIo and CD1oTAPo mice C.-R.W.). to directly examine the role of CD1 in the development of CD4ϩ 2 Address correspondence and reprint requests to Dr. Chyung-Ru Wang, Gwen Knapp and CD8ϩ T cells in the thymus and peripheral lymphoid organs. Center for Lupus and Immunology Research, University of Chicago, 924 East 57th ϩ Street, Chicago, IL 60637-5420. E-mail address: [email protected] In addition, the relative contributions of CD1-restricted CD4 T ϩ 3 ␤ ␤ cells and MHC class II-restricted CD4 T cells in several immune Abbreviations used in this paper: 2m, 2-microglobulin; IEL, intestinal epithelial cells; TNP, trinitrophenol. responses were analyzed. Copyright © 2000 by The American Association of Immunologists 0022-1767/00/$02.00 740 ROLE OF CD1 IN T CELL DEVELOPMENT Materials and Methods Mice CD1-deficient (CD1o) mice were established by homologous recombina- tion in our laboratory as previously described (29) and were backcrossed six generations onto B6. I-A␤-deficient (IIo) mice, provided by Dr. Steven Reiner (University of Chicago), were backcrossed five generations onto B6. TAP1o mice were on a mixed B6 ϫ 129 background (The Jackson Laboratory, Bar Harbor, ME). CD1oIIo mice were generated by crossing CD1o mice with IIo mice in B6 background. CD1oTAPo mice with a mixed B6 ϫ 129 background were established by crossing CD1o mice with TAPo mice. Pathogen-free B6 mice were purchased from The Jackson Laboratory. Flow cytometry analysis and cell preparations The Abs used in this study include FITC-conjugated mAbs specific for CD4 (RM4-5), TCR␤ (H57-597), CD69 (H1.2F3), V␤5 (MR9-4), V␤6 (RR4-7), V␤7 (TR310), V␤8 (MR5-2), V␤9 (MR10-2), V␤12 (MR11-1), ϩ o V␤14 (14-2), and V␣3 (RR3-16); PE-conjugated mAbs specific for CD8␣ FIGURE 1. Different levels of CD4 T cells in wild-type (WT), CD1 , (53-6.7), NK1.1 (PK136), CD4 (RM4-5), CD44 (IM7), V␤2 (B20.6), V␤3 IIo and CD1oIIo mice. Lymphocytes isolated from spleen, lymph nodes, (KJ25), V␤4 (KT4), V␤10 (B21.5), V␤11 (RR3-15), V␤13 (RR12-3), V␣2 and liver of the above mice were stained with mAbs against CD4 and (B20.1), V␣8 (B21.14), and V␣11 (RR8–1); biotin-conjugated mAb spe- TCR␣␤. The percentages of CD4ϩ T cells were analyzed by flow cytom- ϩ cific for CD62L(MEL-14); and Cy-Chrome-conjugated mAbs specific for etry and plotted as dots in the figure.
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