Modulation of Dendritic Cell Differentiation and Cytokine Secretion by the Hydatid Cyst Fluid of Echinococcus Granulosus

Overview

Journal Immunology

Specialty Allergy & Immunology

Date 2006 Jun 15

PMID 16771863

Citations 26

Authors

Joao H C Kanan

Benjamin M Chain

Affiliations

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Abstract

Chronic infection by Echinococcus granulosus results in establishment of fluid-filled cysts (hydatid cysts) in liver or lungs of infected hosts, which can escape destruction by the host immune system for long periods. This study explores the modulation by hydatid cyst fluid of the in vitro human monocyte to dendritic cell (DC) transition induced by granulocyte-macrophage colony-stimulating factor (GM-CSF) and interleukin-4 (IL-4). Addition of the fluid to adherent peripheral blood monocytes cultured in GM-CSF/IL-4 stimulates release of prostaglandin E2 (PGE2) and IL-6. Exposure of differentiating DC to the fluid during the 7-day culture in GM-CSF/IL-4 impairs their subsequent ability to secrete IL-12, IL-6 or PGE2 in response to lipopolysaccharide (LPS) stimulation. This inhibition is not dependent on the initial release of PGE2. The presence of hydatid cyst fluid also modulates the phenotype of the cells generated during culture, resulting in increased CD14 expression and decreased expression of CD1a. Finally, hydatid fluid can stimulate predifferentiated DC to mature, as evidenced by release of IL-12 and IL-6, and by up-regulation of class II major histocompatibility complex and CD86. The possible role of dendritic cell modulation in regulating the host immune response to hydatid cysts is discussed.

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References

Dematteis S, Rottenberg M, Baz A . Cytokine response and outcome of infection depends on the infective dose of parasites in experimental infection by Echinococcus granulosus. Parasite Immunol. 2003; 25(4):189-97. DOI: 10.1046/j.1365-3024.2003.00620.x. View

Zhang W, Li J, McManus D . Concepts in immunology and diagnosis of hydatid disease. Clin Microbiol Rev. 2003; 16(1):18-36. PMC: 145297. DOI: 10.1128/CMR.16.1.18-36.2003. View

Riley E, Dixon J, Jenkins P, Ross G . Echinococcus granulosus infection in mice: host responses during primary and secondary infection. Parasitology. 1986; 92 ( Pt 2):391-403. DOI: 10.1017/s0031182000064155. View

Jenkins P, Dixon J, Ross G, Cox D . Echinococcus granulosus: changes in the transformational behaviour of murine lymph node cells during early infection. Ann Trop Med Parasitol. 1986; 80(1):43-7. DOI: 10.1080/00034983.1986.11811982. View

Judson D, Dixon J, Skerritt G . Occurrence and biochemical characteristics of cestode lymphocyte mitogens. Parasitology. 1987; 94 ( Pt 1):151-60. DOI: 10.1017/s0031182000053531. View

Riley E, Dixon J . Experimental Echinococcus granulosus infection in mice: immunocytochemical analysis of lymphocyte populations in local lymphoid infections during early infection. Parasitology. 1987; 94 ( Pt 3):523-32. DOI: 10.1017/s0031182000055864. View

Cox D, Marshall-Clarke S, Dixon J . Activation of normal murine B cells by Echinococcus granulosus. Immunology. 1989; 67(1):16-20. PMC: 1385281. View

Phipps R, Stein S, Roper R . A new view of prostaglandin E regulation of the immune response. Immunol Today. 1991; 12(10):349-52. DOI: 10.1016/0167-5699(91)90064-Z. View

Janssen D, Osuna A, Lazuen J, de Rycke P . Comparative cytotoxicity of secondary hydatid cysts, protoscoleces, and in vitro developed microcysts of Echinococcus granulosus. J Helminthol. 1992; 66(2):124-31. DOI: 10.1017/s0022149x00012700. View

10.

Maizels R, Bundy D, Selkirk M, Smith D, Anderson R . Immunological modulation and evasion by helminth parasites in human populations. Nature. 1993; 365(6449):797-805. DOI: 10.1038/365797a0. View

11.

Niiro H, Otsuka T, Kuga S, Nemoto Y, Abe M, Hara N . IL-10 inhibits prostaglandin E2 production by lipopolysaccharide-stimulated monocytes. Int Immunol. 1994; 6(4):661-4. DOI: 10.1093/intimm/6.4.661. View

12.

Rigano R, Profumo E, Di Felice G, Ortona E, Teggi A, Siracusano A . In vitro production of cytokines by peripheral blood mononuclear cells from hydatid patients. Clin Exp Immunol. 1995; 99(3):433-9. PMC: 1534218. DOI: 10.1111/j.1365-2249.1995.tb05569.x. View

13.

Hinson R, Williams J, Shacter E . Elevated interleukin 6 is induced by prostaglandin E2 in a murine model of inflammation: possible role of cyclooxygenase-2. Proc Natl Acad Sci U S A. 1996; 93(10):4885-90. PMC: 39374. DOI: 10.1073/pnas.93.10.4885. View

14.

Haralabidis S, Karagouni E, Frydas S, Dotsika E . Immunoglobulin and cytokine profile in murine secondary hydatidosis. Parasite Immunol. 1995; 17(12):625-30. DOI: 10.1111/j.1365-3024.1995.tb01008.x. View

15.

Torcal J, Navarro-Zorraquino M, Lozano R, Larrad L, Salinas J, Ferrer J . Immune response and in vivo production of cytokines in patients with liver hydatidosis. Clin Exp Immunol. 1996; 106(2):317-22. PMC: 2200592. DOI: 10.1046/j.1365-2249.1996.d01-843.x. View

16.

Holcman B, Heath D . The early stages of Echinococcus granulosus development. Acta Trop. 1997; 64(1-2):5-17. DOI: 10.1016/s0001-706x(96)00636-5. View

17.

Fauser S, Kern P . T-lymphocyte cytokine mRNA expression in cystic echinococcosis. Acta Trop. 1997; 64(1-2):35-51. DOI: 10.1016/s0001-706x(96)00638-9. View

18.

Janssen D, Rueda M, de Rycke P, Osuna A . Immunomodulation by hydatid cyst fluid toxin (Echinococcus granulosus). Parasite Immunol. 1997; 19(4):149-60. DOI: 10.1046/j.1365-3024.1997.d01-194.x. View

19.

Zhang L, McManus D . Purification and N-terminal amino acid sequencing of Echinococcus granulosus antigen 5. Parasite Immunol. 1996; 18(12):597-606. DOI: 10.1046/j.1365-3024.1996.d01-42.x. View

20.

Rogan M, Craig P . Immunology of Echinococcus granulosus infections. Acta Trop. 1997; 67(1-2):7-17. DOI: 10.1016/s0001-706x(97)00055-7. View