CD4pos, NK1.1pos T cells promptly produce interleukin 4 in response to in vivo challenge with anti-CD3

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CD4pos, NK1.1pos T cells promptly produce interleukin 4 in response to in vivo challenge with anti-CD3

T Yoshimoto and WE Paul
Laboratory of Immunology, National Institute of Allergy and infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892.

Injection of anti-CD3 antibodies causes prompt expression of interleukin (IL)-4, IL-2, and interferon gamma (IFN-gamma) mRNA among spleen cells. The optimal dose of anti-CD3 for such induction was 1.33 microgram/animal; lymphokine mRNA was first observed at 30 min, peaked at 90 min, and was undetectable (for IL-4) or had declined markedly by 4 h. Cells harvested from spleens of mice injected with anti-CD3 90 min earlier secreted IL-4, IL-2, and IFN-gamma without further stimulation. By contrast, in vitro stimulation with anti-CD3 of spleen cell suspensions or splenic fragments from noninjected donors failed to cause prompt production of IL-4 and, even after 24 h of stimulation, the amount of IL-4 produced in such cells was substantially less than that secreted within 1 h by spleen cell suspensions or splenic fragments from mice injected with anti-CD3 90 min earlier. Production of IL-4 by spleen cells from anti-CD3-injected mice was not inhibited by pretreatment with anti-IL-4 antibody or with IFN-gamma or tumor growth factor beta nor enhanced by treatment with IL-4. By contrast, CTLA-4 immunoglobulin (Ig) treatment clearly diminished IL-4 production in response to in vivo anti-CD3, indicating that cellular interactions involving CD28 (or related molecules) were important in stimulation. Cell sorting analysis indicated that the cells that produced IL-4 in response to in vivo injection of anti-CD3 were highly enriched in CD4pos cells with the phenotype leukocyte cell adhesion molecule-1 (LECAM-1)dull, CD44bright, CD45RBdull, NK1.1pos. Indeed, the small population of CD4pos, NK1.1pos cells had the great majority of the IL-4- producing activity of this population. Injection with Staphylococcal enterotoxin B also caused prompt induction of IL-4 mRNA; the cells that were principally responsible for production also had the phenotype of CD4pos, NK1.1pos. These results suggest that possibility that this rare population of T cells may be capable of secreting IL-4 at the outset of immune responses and thus may act to regulate the pattern of priming of naive T cells, by providing a source of IL-4 to favor the development of T cell helper 2-like IL-4-producing cells.
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Bandeira-Melo, C., Sugiyama, K., Woods, L. J., Weller, P. F. (2001). Cutting Edge: Eotaxin Elicits Rapid Vesicular Transport-Mediated Release of Preformed IL-4 from Human Eosinophils. J. Immunol. 166: 4813-4817 [Abstract] [Full Text]
Kudlacz, E. M., Andresen, C. J., Salafia, M., Whitney, C. A., Naclerio, B., Changelian, P. S. (2001). Genetic Ablation of the src Kinase p59fynT Exacerbates Pulmonary Inflammation in an Allergic Mouse Model. Am. J. Respir. Cell Mol. Bio. 24: 469-474 [Abstract] [Full Text]
Laloux, V., Beaudoin, L., Jeske, D., Carnaud, C., Lehuen, A. (2001). NK T Cell-Induced Protection Against Diabetes in V{{alpha}}14-J{{alpha}}281 Transgenic Nonobese Diabetic Mice Is Associated with a Th2 Shift Circumscribed Regionally to the Islets and Functionally to Islet Autoantigen. J. Immunol. 166: 3749-3756 [Abstract] [Full Text]
Iwabuchi, K., Iwabuchi, C., Tone, S., Itoh, D., Tosa, N., Negishi, I., Ogasawara, K., Uede, T., Onoe, K. (2001). Defective development of NK1.1+ T-cell antigen receptor {alpha}{beta}+ cells in zeta-associated protein 70 null mice with an accumulation of NK1.1+ CD3{-} NK-like cells in the thymus. Blood 97: 1765-1775 [Abstract] [Full Text]
Wu, Z., Turner, D. R., Oliveira, D. B. G. (2001). IL-4 gene expression up-regulated by mercury in rat mast cells: a role of oxidant stress in IL-4 transcription. Int Immunol 13: 297-304 [Abstract] [Full Text]
Carnaud, C., Gombert, J.-M., Donnars, O., Garchon, H.-J., Herbelin, A. (2001). Protection Against Diabetes and Improved NK/NKT Cell Performance in NOD.NK1.1 Mice Congenic at the NK Complex. J. Immunol. 166: 2404-2411 [Abstract] [Full Text]
Seino, K.-i., Fukao, K., Muramoto, K., Yanagisawa, K., Takada, Y., Kakuta, S., Iwakura, Y., Van Kaer, L., Takeda, K., Nakayama, T., Taniguchi, M., Bashuda, H., Yagita, H., Okumura, K. (2001). Requirement for natural killer T (NKT) cells in the induction of allograft tolerance. Proc. Natl. Acad. Sci. USA 10.1073/pnas.041608298v1 [Abstract] [Full Text]
Ulanova, M., Tarkowski, A., Hahn-Zoric, M., Hanson, L. A. (2001). The Common Vaccine Adjuvant Aluminum Hydroxide Up-Regulates Accessory Properties of Human Monocytes via an Interleukin-4-Dependent Mechanism. Infect. Immun. 69: 1151-1159 [Abstract] [Full Text]
Leite-de-Moraes, M. C., Hameg, A., Pacilio, M., Koezuka, Y., Taniguchi, M., Van Kaer, L., Schneider, E., Dy, M., Herbelin, A. (2001). IL-18 Enhances IL-4 Production by Ligand-Activated NKT Lymphocytes: A Pro-Th2 Effect of IL-18 Exerted Through NKT Cells. J. Immunol. 166: 945-951 [Abstract] [Full Text]
Yang, Y.-F., Tomura, M., Ono, S., Hamaoka, T., Fujiwara, H. (2000). Requirement for IFN-{gamma} in IL-12 production induced by collaboration between V{alpha}14+ NKT cells and antigen-presenting cells. Int Immunol 12: 1669-1675 [Abstract] [Full Text]
Araujo, L. M., Puel, A., Gouarin, C., Hameg, A., Mevel, J.-C., Koezuka, Y., Bach, J.-F., Mouton, D., Herbelin, A. (2000). NKT lymphocyte ontogeny and function are impaired in low antibody-producer Biozzi mice: gene mapping in the interval-specific congenic strains raised for immunomodulatory genes. Int Immunol 12: 1613-1622 [Abstract] [Full Text]
Hameg, A., Apostolou, I., Leite-de-Moraes, M., Gombert, J.-M., Garcia, C., Koezuka, Y., Bach, J.-F., Herbelin, A. (2000). A Subset of NKT Cells That Lacks the NK1.1 Marker, Expresses CD1d Molecules, and Autopresents the {alpha}-Galactosylceramide Antigen. J. Immunol. 165: 4917-4926 [Abstract] [Full Text]
Seaman, M. S., Wang, C.-R., Forman, J. (2000). MHC Class Ib-Restricted CTL Provide Protection Against Primary and Secondary Listeria monocytogenes Infection. J. Immunol. 165: 5192-5201 [Abstract] [Full Text]
Eberl, G., Brawand, P., MacDonald, H. R. (2000). Selective Bystander Proliferation of Memory CD4+ and CD8+ T Cells Upon NK T or T Cell Activation. J. Immunol. 165: 4305-4311 [Abstract] [Full Text]