Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-06T01:08:42.341Z Has data issue: false hasContentIssue false
  • English
  • Français

Different protein of Echinococcus granulosus stimulates dendritic induced immune response

Published online by Cambridge University Press:  25 February 2015

YANA WANG ,
QIANG WANG ,
SHIYU LV  and
SHENGXIANG ZHANG
YANA WANG
Affiliation:
Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, School of Life Sciences, Lanzhou University, 222 South Tianshui Road, Lanzhou, Gansu 730000, China Echinococcosis Laboratory, Ningxia Medical University, Yinchun 750004, China
QIANG WANG
Affiliation:
Echinococcosis Laboratory, Ningxia Medical University, Yinchun 750004, China
SHIYU LV
Affiliation:
School of Laboratory Medicine, Ningxia Medical University, Yinchuan 750004, China
SHENGXIANG ZHANG*
Affiliation:
Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, School of Life Sciences, Lanzhou University, 222 South Tianshui Road, Lanzhou, Gansu 730000, China
*
*Corresponding author. School of Life Sciences, Lanzhou University, 222 South Tianshui Road, Lanzhou, Gansu 730000, China. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Cystic echinococcosis is a chronic infectious disease that results from a host/parasite interaction. Vaccination with ferritin derived from Echinococcus granulosus is a potential preventative treatment. To understand whether ferritin is capable of inducing a host immune response, we investigated the response of dendritic cells (DCs) to both recombinant ferritin protein and the hydatid fluid (HF) of E. granulosus. We evaluated the immunomodulatory potential of these antigens by performing, immunocytochemistry, electron microscopy and in vivo imaging of monocyte-derived murine DCs. During antigen stimulation of DCs, ferritin cause DCs maturation and induced higher levels of surface marker expression and activated T-cell proliferation and migration. On contrary, HF failed to induce surface marker expression and to stimulate T-cell proliferation. In response to HF, DCs produced interleukin-6 (IL-6), but no IL-12 and IL-10. DCs stimulated with ferritin produced high levels of cytokines. Overall, HF appears to induce host immunosuppression in order to ensure parasite survival via inhibits DC maturation and promotes Th2-dependent secretion of cytokines. Although ferritin also promoted DC maturation and cytokine release, it also activates CD4+T-cell proliferation, but regard of the mechanism of the Eg.ferritin induce host to eradicate E. granulosus were not clear.

Keywords

dendritic cellrecombinant ferritinEchinococcus granulosushydatid fluidimmune response
Type
Research Article
Information
Parasitology , Volume 142 , Issue 7 , June 2015 , pp. 879 - 889
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Banchereau, J. and Steinman, R. M. (1998). Dendritic cells and the control of immunity. Nature 392, 245–252.CrossRefGoogle ScholarPubMed
Chemale, G., Ferreira, H. B., Barrett, J., Brophy, P. M. and Zaha, A. (2005). Echinococcus granulosus antigen B hydrophobic ligand binding properties. Biochimica et Biophysica Acta 1747, 189–194.Google Scholar
Clarke, T. E., Tari, L. W. and Vogel, H. J. (2001). Structural biology of bacterial iron uptake systems. Current Topics in Medicinal Chemistry 1, 7–30.Google Scholar
Clemens, L. E. and Basch, P. F. (1989). Schistosoma mansoni: effect of transferrin and growth factors on development of schistosomula in vitro. Journal of Parasitology 75, 417–421.CrossRefGoogle ScholarPubMed
Demeure, C. E., Tanaka, H., Mateo, V., Rubio, M., Delespesse, G. and Sarfati, M. (2000). CD47 engagement inhibits cytokine production and maturation of human dendritic cells. Journal of Immunology 164, 2193–2199.CrossRefGoogle ScholarPubMed
Ermann, J. and Fathman, C. G. (2003). Costimulatory signals controlling regulatory T cells. Proceedings of National Academy of Science of the United States of America 100, 15292–15293.Google Scholar
Ersfeld, K. and Craig, P. S. (1995). Cloning and immunological characterisation of Echinococcus granulosus ferritin. Parasitology Research 81, 382–387.Google Scholar
Fukao, T., Tanabe, M., Terauchi, Y., Ota, T., Matsuda, S., Asano, T., Kadowaki, T., Takeuchi, T. and Koyasu, S. (2002). PI3 K-mediated negative feedback regulation of IL-12 production in DCs. Nature Immunology 3, 875–881.Google Scholar
Gottstein, B., Haag, K., Walker, M., Matsumoto, J., Mejri, N. and Hemphill, A. (2006). Molecular survival strategies of Echinococcus multilocularis in the murine host. Parasitology International 55 (Suppl), S45–49.Google Scholar
Guermonprez, P., Valladeau, J., Zitvogel, L., Thery, C. and Amigorena, S. (2002). Antigen presentation and T cell stimulation by dendritic cells. Annual Review of Immunology 20, 621–667.Google Scholar
Hanig, J. and Lutz, M. B. (2008). Suppression of mature dendritic cell function by regulatory T cells in vivo is abrogated by CD40 licensing. Journal of Immunology 180, 1405–1413.Google Scholar
Harnett, W. (2005). Parasite modulation of the immune response. Parasite Immunology 27, 357–359.Google Scholar
Hawiger, D., Inaba, K., Dorsett, Y., Guo, M., Mahnke, K., Rivera, M., Ravetch, J. V., Steinman, R. M. and Nussenzweig, M. C. (2001). Dendritic cells induce peripheral cell unresponsiveness under steady state conditions in vivo. Journal of Experimental Medicine 194, 769–779.Google Scholar
He, J., Gurunathan, S., Iwasaki, A., Ash-Shaheed, B. and Kelsall, B. L. (2000). Primary role for Gi protein signaling in the regulation of interleukin 12 production and the induction of T helper cell type 1 responses. Journal of Experimental Medicine 191, 1605–1610.Google Scholar
Jankovic, D., Steinfelder, S., Kullberg, M. C. and Sher, A. (2006). Mechanisms underlying helminth-induced Th2 polarization: default, negative or positive pathways? Chemical Immunology and Allergy 90, 65–81.Google Scholar
Jenne, L., Arrighi, J. F., Sauter, B. and Kern, P. (2001). Dendritic cells pulsed with unfractionated helminthic proteins to generate antiparasitic cytotoxic T lymphocyte. Parasite Immunology 23, 195–201.Google Scholar
Kanan, J. H. and Chain, B. M. (2006). Modulation of dendritic cell differentiation and cytokine secretion by the hydatid cyst fluid of Echinococcus granulosus . Immunology 118, 271–278.Google Scholar
Latour, S., Tanaka, H., Demeure, C., Mateo, V., Rubio, M., Brown, E. J., Maliszewski, C., Lindberg, F. P., Oldenborg, A., Ullrich, A., Delespesse, G. and Sarfati, M. (2001). Bidirectional negative regulation of human T and dendritic cells by CD47 and its cognate receptor signal-regulator protein-alpha: down-regulation of IL-12 responsiveness and inhibition of dendritic cell activation. Journal of Immunology 167, 2547–2554.Google Scholar
Liu, Y. J. (2001). Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 106, 259–262.Google Scholar
Lorenzo, C., Last, J. A. and Gonzalez-Sapienza, G. G. (2005). The immunogenicity of Echinococcus granulosus antigen 5 is determined by its post-translational modifications. Parasitology 131, 669–677.Google Scholar
Lutz, M. B., Kukutsch, N., Ogilvie, A. L., Rossner, S., Koch, F., Romani, N. and Schuler, G. (1999). An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. Journal of Immunological Methods 223, 77–92.Google Scholar
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. (2004). Helminth parasites – masters of regulation. Immunology Review 201, 89–116.CrossRefGoogle ScholarPubMed
Mamuti, W., Sako, Y., Nakao, M., Xiao, N., Nakaya, K., Ishikawa, Y., Yamasaki, H., Lightowlers, M. W. and Ito, A. (2006). Recent advances in characterization of Echinococcus antigen B. Parasitology International 55 (Suppl), S57–62.Google Scholar
Margos, M. C., Grandgirard, D., Leib, S. and Gottstein, B. (2011). In vitro induction of lymph node cell proliferation by mouse bone marrow dendritic cells following stimulation with different Echinococcus multilocularis antigens. Journal of Helminthology 1–10.Google Scholar
McManus, D. P., Zhang, W., Li, J. and Bartley, P. B. (2003). Echinococcosis. Lancet 362, 1295–1304.Google Scholar
Moro, P. and Schantz, P. M. (2009). Echinococcosis: a review. International Journal of Infectious Disease 13, 125–133.Google Scholar
Moser, M. and Murphy, K. M. (2000). Dendritic cell regulation of TH1-TH2 development. Nature Immunology 1, 199–205.Google Scholar
Naik, S. H. (2008). Demystifying the development of dendritic cell subtypes, a little. Immunology and Cell Biology 86, 439–452.Google Scholar
O'Sullivan, B. and Thomas, R. (2003). CD40 and dendritic cell function. Critical Review in Immunology 23, 83–107.CrossRefGoogle ScholarPubMed
Rescigno, M. and Borrow, P. (2001). The host-pathogen interaction: new themes from dendritic cell biology. Cell 106, 267–270.Google Scholar
Rigano, R., Buttari, B., De Falco, E., Profumo, E., Ortona, E., Margutti, P., Scotta, C., Teggi, A. and Siracusano, A. (2004). Echinococcus granulosus-specific T-cell lines derived from patients at various clinical stages of cystic echinococcosis. Parasite Immunology 26, 45–52.Google Scholar
Rigano, R., Buttari, B., Profumo, E., Ortona, E., Delunardo, F., Margutti, P., Mattei, V., Teggi, A., Sorice, M. and Siracusano, A. (2007). Echinococcus granulosus Antigen B impairs human dendritic cell differentiation and polarizes immature dendritic cell maturation towards a Th2 cell response. Infection and Immunity 75, 1667–1678.Google Scholar
Rosenzvit, M. C., Camicia, F., Kamenetzky, L., Muzulin, P. M. and Gutierrez, A. M. (2006). Identification and intra-specific variability analysis of secreted and membrane-bound proteins from Echinococcus granulosus . Parasitology International 55 (Suppl), S63–67.Google Scholar
Schussler, P., Potters, E., Winnen, R., Bottke, W. and Kunz, W. (1995). An isoform of ferritin as a component of protein yolk platelets in Schistosoma mansoni . Molecular Reproduction and Development 41, 325–330.Google Scholar
Steinman, R. M. (2003). Some interfaces of dendritic cell biology. APMIS 111, 675–697.Google Scholar
Steinman, R. M. (2007). Dendritic cells: understanding immunogenicity. European Journal of Immunology 37 (Suppl 1), S53–60.Google Scholar
Steinman, R. M. and Nussenzweig, M. C. (2002). Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proceedings of National Academy of Science of the United States of America 99, 351–358.Google Scholar
Steinman, R. M., Hawiger, D. and Nussenzweig, M. C. (2003). Tolerogenic dendritic cells. Annual Review of Immunology 21, 685–711.CrossRefGoogle ScholarPubMed
Thery, C. and Amigorena, S. (2001). The cell biology of antigen presentation in dendritic cells. Current Opinion in Immunology 13, 45–51.Google Scholar
Thomson, A. W. and Robbins, P. D. (2008). Tolerogenic dendritic cells for autoimmune disease and transplantation. Annals of the Rheumatic Disease 67 (Suppl 3), iii90–96.Google Scholar
Varol, C., Vallon-Eberhard, A., Elinav, E., Aychek, T., Shapira, Y., Luche, H., Fehling, H. J., Hardt, W. D., Shakhar, G. and Jung, S. (2009). Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31, 502–512.Google Scholar
Vuitton, D. A., Zhang, S. L., Yang, Y., Godot, V., Beurton, I., Mantion, G. and Bresson-Hadni, S. (2006). Survival strategy of Echinococcus multilocularis in the human host. Parasitology International 55 (Suppl), S51–55.Google Scholar
Williams, P. (1988). Role of the cell envelope in bacterial adaptation to growth in vivo in infections. Biochimie 70, 987–1011.Google Scholar
Wang, Y., Li, Z., Bo, Y. and Zhao, W. (2009). Recombinant ferritin protects mice against challenge with Echinococcus granulosus? Acta Parasitologica 54, 335–340.Google Scholar
Zhang, W., Zhang, Z., Shi, B., Li, J., You, H., Tulson, G., Dang, X., Song, Y., Yimiti, T., Wang, J., Jones, M. K. and McManus, D. P. (2006). Vaccination of dogs against Echinococcus granulosus, the cause of cystic hydatid disease in humans. Journal of Infectious Disease 194, 966–74.Google Scholar