Schistosoma mansoni egg-induced early IL-4 production is dependent upon IL-5 and eosinophils

doi:10.1084/jem.184.5.1871

This Article

Full Text (PDF)

Alert me when this article is cited

Citation Map

Services

Email this article

Similar articles in this journal

Similar articles in PubMed

Alert me to new content in the JEM

Download to citation manager

Citing Articles

Citing Articles via HighWire

Citing Articles via CrossRef

Citing Articles via Google Scholar

Google Scholar

Articles by Sabin, E. A.

Articles by Pearce, E. J.

Search for Related Content

PubMed

PubMed Citation

Articles by Sabin, E. A.

Articles by Pearce, E. J.

Pubmed/NCBI databases

Substance via MeSH

Social Bookmarking

What's this?

ARTICLES

Schistosoma mansoni egg-induced early IL-4 production is dependent upon IL-5 and eosinophils

EA Sabin, MA Kopf and EJ Pearce
Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853-6401, USA.

The initial immune response to Schistosoma mansoni eggs presumably results in IL-4 production, as schistosome eggs are strong Th2-inducing antigens and the differentiation of antigen-specific Th2 cells is largely dependent on the presence of IL-4 during priming of naive Th cells. Consistent with this concept, intraperitoneal injection of mice with schistosome eggs results in an upregulation of IL-4 production by peritoneal exudate cells (PECs) within 12 h. Egg-induced IL-4 is rapidly bound by its receptor, suggesting that this cytokine is utilized by a cell type present at the site of antigen deposition or is complexed to soluble receptor. The peak of early IL-4 production is accompanied by a local eosinophilia and the apparent disappearance of mast cells. Studies utilizing either IL-4, IL-5, or mast cell-deficient mice indicate that the eosinophilia is dependent on mast cells and IL-5 and independent of IL-4. Strikingly, egg-induced IL-4 production is absent in animals lacking the early peritoneal eosinophilia. Immunocytochemical analysis of PEC following egg injection indicates that the eosinophils themselves make IL-4. These data strongly suggest that egg-induced IL-5 plays an essential role in recruiting eosinophils to the site of antigen deposition and that it is these eosinophils that then directly produce early IL-4.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Wang, H.-B., Weller, P. F. (2008). Pivotal Advance: Eosinophils mediate early alum adjuvant-elicited B cell priming and IgM production. J. Leukoc. Biol. 83: 817-821 [Abstract] [Full Text]
Loke, P., Gallagher, I., Nair, M. G., Zang, X., Brombacher, F., Mohrs, M., Allison, J. P., Allen, J. E. (2007). Alternative Activation Is an Innate Response to Injury That Requires CD4+ T Cells to be Sustained during Chronic Infection. J. Immunol. 179: 3926-3936 [Abstract] [Full Text]
Xin, J., Ohmori, K., Nishida, J., Zhu, Y., Huang, H. (2007). The initial response of CD4+ IL-4-producing cells. Int Immunol 19: 305-310 [Abstract] [Full Text]
Leeto, M., Herbert, D. R., Marillier, R., Schwegmann, A., Fick, L., Brombacher, F. (2006). TH1-Dominant Granulomatous Pathology Does Not Inhibit Fibrosis or Cause Lethality during Murine Schistosomiasis. Am. J. Pathol. 169: 1701-1712 [Abstract] [Full Text]
Balic, A., Harcus, Y. M., Taylor, M. D., Brombacher, F., Maizels, R. M. (2006). IL-4R signaling is required to induce IL-10 for the establishment of Th2 dominance. Int Immunol 18: 1421-1431 [Abstract] [Full Text]
Swartz, J. M., Dyer, K. D., Cheever, A. W., Ramalingam, T., Pesnicak, L., Domachowske, J. B., Lee, J. J., Lee, N. A., Foster, P. S., Wynn, T. A., Rosenberg, H. F. (2006). Schistosoma mansoni infection in eosinophil lineage-ablated mice. Blood 108: 2420-2427 [Abstract] [Full Text]
Spencer, L. A., Melo, R. C. N., Perez, S. A. C., Bafford, S. P., Dvorak, A. M., Weller, P. F. (2006). Cytokine receptor-mediated trafficking of preformed IL-4 in eosinophils identifies an innate immune mechanism of cytokine secretion. Proc. Natl. Acad. Sci. USA 103: 3333-3338 [Abstract] [Full Text]
Mikhalkevich, N., Becknell, B., Caligiuri, M. A., Bates, M. D., Harvey, R., Zheng, W.-p. (2006). Responsiveness of Naive CD4 T Cells to Polarizing Cytokine Determines the Ratio of Th1 and Th2 Cell Differentiation. J. Immunol. 176: 1553-1560 [Abstract] [Full Text]
McKee, A. S., Pearce, E. J. (2004). CD25+CD4+ Cells Contribute to Th2 Polarization during Helminth Infection by Suppressing Th1 Response Development. J. Immunol. 173: 1224-1231 [Abstract] [Full Text]
Chen, L., Grabowski, K. A., Xin, J.-p., Coleman, J., Huang, Z., Espiritu, B., Alkan, S., Xie, H. B., Zhu, Y., White, F. A., Clancy, J. Jr, Huang, H. (2004). IL-4 Induces Differentiation and Expansion of Th2 Cytokine-Producing Eosinophils. J. Immunol. 172: 2059-2066 [Abstract] [Full Text]
Bystrom, J., Wynn, T. A., Domachowske, J. B., Rosenberg, H. F. (2004). Gene microarray analysis reveals interleukin-5-dependent transcriptional targets in mouse bone marrow. Blood 103: 868-877 [Abstract] [Full Text]
Tawill, S., Le Goff, L., Ali, F., Blaxter, M., Allen, J. E. (2004). Both Free-Living and Parasitic Nematodes Induce a Characteristic Th2 Response That Is Dependent on the Presence of Intact Glycans. Infect. Immun. 72: 398-407 [Abstract] [Full Text]
Gyetko, M. R., Sud, S., Chensue, S. W. (2004). Urokinase-Deficient Mice Fail To Generate a Type 2 Immune Response following Schistosomal Antigen Challenge. Infect. Immun. 72: 461-467 [Abstract] [Full Text]
Saeftel, M., Arndt, M., Specht, S., Volkmann, L., Hoerauf, A. (2003). Synergism of Gamma Interferon and Interleukin-5 in the Control of Murine Filariasis. Infect. Immun. 71: 6978-6985 [Abstract] [Full Text]
Ramalingam, T., Rajan, B., Lee, J., Rajan, T. V. (2003). Kinetics of Cellular Responses to Intraperitoneal Brugia pahangi Infections in Normal and Immunodeficient Mice. Infect. Immun. 71: 4361-4367 [Abstract] [Full Text]
Bandeira-Melo, C., Woods, L. J., Phoofolo, M., Weller, P. F. (2002). Intracrine Cysteinyl Leukotriene Receptor-mediated Signaling of Eosinophil Vesicular Transport-mediated Interleukin-4 Secretion. J. Exp. Med. 196: 841-850 [Abstract] [Full Text]
Rao, K. V. N., Chen, L., Gnanasekar, M., Ramaswamy, K. (2002). Cloning and Characterization of a Calcium-binding, Histamine-releasing Protein from Schistosoma mansoni. J. Biol. Chem. 277: 31207-31213 [Abstract] [Full Text]
Balmer, P., Devaney, E. (2002). NK T Cells Are a Source of Early Interleukin-4 following Infection with Third-Stage Larvae of the Filarial Nematode Brugia pahangi. Infect. Immun. 70: 2215-2219 [Abstract] [Full Text]
Campbell, S. B., Komata, T., Kelso, A. (2001). CD4 Ligation Promotes the IL-4-Independent Development of IL-4-Producing Clones from Naive CD4+ T Cells. J. Immunol. 167: 5610-5619 [Abstract] [Full Text]
MacKenzie, J. R., Mattes, J., Dent, L. A., Foster, P. S. (2001). Eosinophils Promote Allergic Disease of the Lung by Regulating CD4+ Th2 Lymphocyte Function. J. Immunol. 167: 3146-3155 [Abstract] [Full Text]
Tesciuba, A. G., Subudhi, S., Rother, R. P., Faas, S. J., Frantz, A. M., Elliot, D., Weinstock, J., Matis, L. A., Bluestone, J. A., Sperling, A. I. (2001). Inducible Costimulator Regulates Th2-Mediated Inflammation, but Not Th2 Differentiation, in a Model of Allergic Airway Disease. J. Immunol. 167: 1996-2003 [Abstract] [Full Text]
Hall, L. R., Diaconu, E., Pearlman, E. (2001). A Dominant Role for Fc{{gamma}} Receptors in Antibody-Dependent Corneal Inflammation. J. Immunol. 167: 919-925 [Abstract] [Full Text]
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]
Nickdel, M. B., Roberts, F., Brombacher, F., Alexander, J., Roberts, C. W. (2001). Counter-Protective Role for Interleukin-5 during Acute Toxoplasma gondii Infection. Infect. Immun. 69: 1044-1052 [Abstract] [Full Text]
Noben-Trauth, N., Hu-Li, J., Paul, W. E. (2000). Conventional, Naive CD4+ T Cells Provide an Initial Source of IL-4 During Th2 Differentiation. J. Immunol. 165: 3620-3625 [Abstract] [Full Text]
Vos, Q., Snapper, C. M., Mond, J. J. (2000). Th1 versus Th2 cytokine profile determines the modulation of in vitro T cell-independent type 2 responses by IL-4. Int Immunol 12: 1337-1345 [Abstract] [Full Text]
Cai, G., Radzanowski, T., Villegas, E. N., Kastelein, R., Hunter, C. A. (2000). Identification of STAT4-Dependent and Independent Mechanisms of Resistance to Toxoplasma gondii. J. Immunol. 165: 2619-2627 [Abstract] [Full Text]
Webb, D. C., McKenzie, A. N. J., Koskinen, A. M. L., Yang, M., Mattes, J., Foster, P. S. (2000). Integrated Signals Between IL-13, IL-4, and IL-5 Regulate Airways Hyperreactivity. J. Immunol. 165: 108-113 [Abstract] [Full Text]
Hoffmann, K. F., Cheever, A. W., Wynn, T. A. (2000). IL-10 and the Dangers of Immune Polarization: Excessive Type 1 and Type 2 Cytokine Responses Induce Distinct Forms of Lethal Immunopathology in Murine Schistosomiasis. J. Immunol. 164: 6406-6416 [Abstract] [Full Text]
Al-Qaoud, K. M., Pearlman, E., Hartung, T., Klukowski, J., Fleischer, B., Hoerauf, A. (2000). A new mechanism for IL-5-dependent helminth control: neutrophil accumulation and neutrophil-mediated worm encapsulation in murine filariasis are abolished in the absence of IL-5. Int Immunol 12: 899-908 [Abstract] [Full Text]
Jankovic, D., Kullberg, M. C., Noben-Trauth, N., Caspar, P., Paul, W. E., Sher, A. (2000). Single Cell Analysis Reveals That IL-4 Receptor/Stat6 Signaling Is Not Required for the In Vivo or In Vitro Development of CD4+ Lymphocytes with a Th2 Cytokine Profile. J. Immunol. 164: 3047-3055 [Abstract] [Full Text]
Finkelman, F. D., Morris, S. C., Orekhova, T., Mori, M., Donaldson, D., Reiner, S. L., Reilly, N. L., Schopf, L., Urban, J. F. Jr. (2000). Stat6 Regulation of In Vivo IL-4 Responses. J. Immunol. 164: 2303-2310 [Abstract] [Full Text]
La Flamme, A. C., MacDonald, A. S., Pearce, E. J. (2000). Role of IL-6 in Directing the Initial Immune Response to Schistosome Eggs. J. Immunol. 164: 2419-2426 [Abstract] [Full Text]
Mould, A. W., Ramsay, A. J., Matthaei, K. I., Young, I. G., Rothenberg, M. E., Foster, P. S. (2000). The Effect of IL-5 and Eotaxin Expression in the Lung on Eosinophil Trafficking and Degranulation and the Induction of Bronchial Hyperreactivity. J. Immunol. 164: 2142-2150 [Abstract] [Full Text]
Martin, D. L., King, C. L., Pearlman, E., Strine, E., Heinzel, F. P. (2000). IFN-{gamma} Is Necessary But Not Sufficient for Anti-CD40 Antibody-Mediated Inhibition of the Th2 Response to Schistosoma mansoni Eggs. J. Immunol. 164: 779-785 [Abstract] [Full Text]
Brewer, J. M., Conacher, M., Hunter, C. A., Mohrs, M., Brombacher, F., Alexander, J. (1999). Aluminium Hydroxide Adjuvant Initiates Strong Antigen-Specific Th2 Responses in the Absence of IL-4- or IL-13-Mediated Signaling. J. Immunol. 163: 6448-6454 [Abstract] [Full Text]
Hayashi, N., Matsui, K., Tsutsui, H., Osada, Y., Mohamed, R. T., Nakano, H., Kashiwamura, S.-i., Hyodo, Y., Takeda, K., Akira, S., Hada, T., Higashino, K., Kojima, S., Nakanishi3, K. (1999). Kupffer Cells from Schistosoma mansoni-Infected Mice Participate in the Prompt Type 2 Differentiation of Hepatic T Cells in Response to Worm Antigens. J. Immunol. 163: 6702-6711 [Abstract] [Full Text]
Chen, Y.-T., Chen, F.-L., Kung, J. T. (1999). Age-Associated Rapid and Stat6-Independent IL-4 Production by NK1-CD4+8- Thymus T Lymphocytes. J. Immunol. 163: 4747-4753 [Abstract] [Full Text]
Caamano, J., Alexander, J., Craig, L., Bravo, R., Hunter, C. A. (1999). The NF-{kappa}B Family Member RelB Is Required for Innate and Adaptive Immunity to Toxoplasma gondii. J. Immunol. 163: 4453-4461 [Abstract] [Full Text]
Rosa Brunet, L., Sabin, E. A., Cheever, A. W., Kopf, M. A., Pearce, E. J. (1999). Interleukin 5�(IL-5) Is Not Required for Expression of a Th2 Response or Host Resistance Mechanisms during Murine Schistosomiasis Mansoni but Does Play a Role in Development of IL-4-Producing Non-T, Non-B Cells. Infect. Immun. 67: 3014-3018 [Abstract] [Full Text]
Giembycz, M. A., Lindsay, M. A. (1999). Pharmacology of the Eosinophil. Pharmacol. Rev. 51: 213-340 [Abstract] [Full Text]
La Flamme, A. C., Pearce, E. J. (1999). The Absence of IL-6 Does Not Affect Th2 Cell Development In Vivo, But Does Lead to Impaired Proliferation, IL-2 Receptor Expression, and B Cell Responses. J. Immunol. 162: 5829-5837 [Abstract] [Full Text]
Boros, D. L., Whitfield, J. R. (1999). Enhanced Th1 and Dampened Th2 Responses Synergize To Inhibit Acute Granulomatous and Fibrotic Responses in Murine Schistosomiasis Mansoni. Infect. Immun. 67: 1187-1193 [Abstract] [Full Text]
Chiaramonte, M. G., Schopf, L. R., Neben, T. Y., Cheever, A. W., Donaldson, D. D., Wynn, T. A. (1999). IL-13 Is a Key Regulatory Cytokine for Th2 Cell-Mediated Pulmonary Granuloma Formation and IgE Responses Induced by Schistosoma mansoni Eggs. J. Immunol. 162: 920-930 [Abstract] [Full Text]
Rumbley, C. A., Zekavat, S. A., Sugaya, H., Perrin, P. J., Ramadan, M. A., Phillips, S. M. (1998). The Schistosome Granuloma: Characterization of Lymphocyte Migration, Activation, and Cytokine Production. J. Immunol. 161: 4129-4137 [Abstract] [Full Text]
Hoffmann, K. F., Caspar, P., Cheever, A. W., Wynn, T. A. (1998). IFN-{gamma}, IL-12, and TNF-{alpha} Are Required to Maintain Reduced Liver Pathology in Mice Vaccinated with Schistosoma mansoni Eggs and IL-12. J. Immunol. 161: 4201-4210 [Abstract] [Full Text]
Chen, Y., Boros, D. L. (1998). Identification of the Immunodominant T Cell Epitope of p38, a Major Egg Antigen, and Characterization of the Epitope-Specific Th Responsiveness During Murine Schistosomiasis Mansoni. J. Immunol. 160: 5420-5427 [Abstract] [Full Text]
Hultgren, O., Kopf, M., Tarkowski, A. (1998). Staphylococcus aureus-Induced Septic Arthritis and Septic Death Is Decreased in IL-4-Deficient Mice: Role of IL-4 as Promoter for Bacterial Growth. J. Immunol. 160: 5082-5087 [Abstract] [Full Text]
Lange, C., Schuler, T., Blankenstein, T. (1998). Interleukin 4�Gene-defective Mice Reconstituted with Wild-type Bone Marrow Fail to Produce Normal Immunoglobulin E Levels. J. Exp. Med. 187: 1487-1493 [Abstract] [Full Text]
MacDonald, A. S., Maizels, R. M., Lawrence, R. A., Dransfield, I., Allen, J. E. (1998). Requirement for In Vivo Production of IL-4, But Not IL-10, in the Induction of Proliferative Suppression by Filarial Parasites. J. Immunol. 160: 4124-4132 [Abstract] [Full Text]
Morris, S. C., Coffman, R. L., Finkelman, F. D. (1998). In Vivo IL-4 Responses to Anti-IgD Antibody Are MHC Class II Dependent and {beta}2-Microglobulin Independent and Develop Normally in the Absence of IL-4 Priming of T Cells. J. Immunol. 160: 3299-3304 [Abstract] [Full Text]
Langhorne, J., Cross, C., Seixas, E., Li, C., von der Weid, T. (1998). A role for B cells in the development of T cell helper function in a malaria infection in�mice. Proc. Natl. Acad. Sci. USA 95: 1730-1734 [Abstract] [Full Text]
MacDonald, A. S., Maizels, R. M., Lawrence, R. A., Dransfield, I., Allen, J. E. (1998). Requirement for In Vivo Production of IL-4, But Not IL-10, in the Induction of Proliferative Suppression by Filarial Parasites. J. Immunol. 160: 1304-1312 [Abstract] [Full Text]
Lee, J. J., McGarry, M. P., Farmer, S. C., Denzler, K. L., Larson, K. A., Carrigan, P. E., Brenneise, I. E., Horton, M. A., Haczku, A., Gelfand, E. W., Leikauf, G. D., Lee, N. A. (1997). Interleukin-5 Expression in the Lung Epithelium of Transgenic Mice Leads to Pulmonary Changes Pathognomonic of Asthma. J. Exp. Med. 185: 2143-2156 [Abstract] [Full Text]
Coffman, R. L., Weid, T. (1997). Multiple Pathways for the Initiation of T Helper 2�(Th2) Responses. J. Exp. Med. 185: 373-376 [Full Text]