Brugia malayi microfilariae induce cell death in human dendritic cells, inhibit their ability to make IL-12 and IL-10, and reduce their capacity to activate CD4+ T cells

Journal of Immunology

Volumn 171, Issue 4, 2003, Pages 1950-1960

  Semnani, Roshanak Tolouei ^a   Liu, Anne Y ^a,b   Sabzevari, Helen ^c   Kubofcik, Joseph ^a   Zhou, Jun ^c   Gilden, Julia K ^a   Nutman, Thomas B ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1ALPHA; INTERLEUKIN 5; INTERLEUKIN 8; MESSENGER RNA; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; BRUGIA MALAYI; CELL FUNCTION; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FILARIA; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MICROFILARIA; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION; UPREGULATION;

EID: 0042635842     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.4.1950     Document Type: Article

References (42)

1. Maizels, R. M., J. E. Allen, and M. Yaszdanbakhsh. 2000. Immunology of lymphatic filariasis: current controversies. In Lymphatic Filariasis. Nutman, T. B., ed. Imperial College Press, London, p. 217.
2. Mahanty, S., H. E. Luke, V. Kumaraswami, P. R. Narayanan, V. Vijayshekaran, and T. B. Nutman. 1996. Stage-specific induction of cytokines regulates the immune response in lymphatic filariasis. Exp. Parasitol. 84:282.
3. Mountford, A. P., and E. Pearlman. 1998. Interleukin-12 and the host response to parasitic helminths: the paradoxical effect on protective immunity and immunopathology. Parasite Immunol. 20:509.
4. Candolfi, E., C. A. Hunter, and J. S. Remington. 1994. Mitogen- and antigen-specific proliferation of T cells in murine toxoplasmosis is inhibited by reactive nitrogen intermediates. Infect. Immun. 62:1995.
5. Dai, W. J., and B. Gottstein. 1999. Nitric oxide-mediated immunosuppression following murine Echinococcus multilocularis infection. Immunology. 97:107.
6. Schleifer, K. W., and J. M. Mansfield. 1993. Suppressor macrophages in African trypanosomiasis inhibit T cell proliferative responses by nitric oxide and prostaglandins. J. Immunol. 151:5492.
7. King, C. L., S. Mahanty, V. Kumaraswami, J. S. Abrams, J. Regunathan, K. Jayaraman, E. A. Ottesen, and T. B. Nutman. 1993. Cytokine control of parasite-specific anergy in human lymphatic filariasis: preferential induction of a regulatory T helper type 2 lymphocyte subset. J. Clin. Invest. 92:1667.
8. Loke, P., A. A. MacDonald, A. Robb, R. M. Maizels, and J. E. Allen. 2000. Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. Eur. J. Immunol. 30:2669.
9. Whelan, M., M. M. Harnett, K. M. Houston, V. Patel, W. Harnett, and K. P. Rigley. 2000. A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J. Immunol. 164:6453.
10. Semnani, R. T., H. Sabzevari, R. Iyer, and T. B. Nutman. 2001. Filarial antigens impair the function of human dendritic cells during differentiation. Infect. Immun. 69:5813.
11. + T lymphocytes: a mechanism of immune unresponsiveness in filariasis. Eur. J. Immunol. 32:858.
12. Mabbott, N. A., I. A. Sutherland, and J. M. Sternberg. 1995. Suppressor macrophages in Trypanosoma brucei infection: nitric oxide is related to both suppressive activity and lifespan in vivo. Parasite Immunol. 17:143.
13. Mahanty, S., M. Ravichandran, U. Raman, K. Jayaraman, V. Kumaraswami, and T. B. Nutman. 1997. Regulation of parasite antigen-driven immune responses by interleukin-10 (IL-10) and IL-12 in lymphatic filariasis. Infect. Immun. 65:1742.
14. Dieu, M. C., B. Vanbervliet, A. Vicari, J. M. Bridon, E. Oldham, S. Ait-Yahia, F. Briere, A. Zlotnik, S. Lebecque, and C. Caux. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 188:373.
15. Gusmao, R. D., A. M. Stanley, and E. A. Ottesen. 1981. Brugia pahangi: immunologic evaluation of the differential susceptibility to filarial infection in inbred Lewis rats. Exp. Parasitol. 52:147.
16. Horgan, K. J., and S. Shaw. 1991. Immunomagnetic purification of T cell populations. In Current Protocols in Immunology. Coligan, J. E., A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober, eds. Wiley Interscience, New York, p. 7.4.1.
17. + T cells. J. Exp. Med. 180:2125.
18. Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad Sci. USA 95:14863.
19. Taylor, M. J. 2002. A new insight into the pathogenesis of filarial disease. Curr. Mol. Med. 2:299.
20. Jeffers, G. W., T. R. Klei, and F. M. Enright. 1984. Activation of jird (Meriones unguiculatus) macrophages by the filarial parasite Brugia pahangi. Infect. Immun. 43:43.
21. Springer, T. A. 1990. Adhesion receptors of the immune system. Nature 346:425.
22. Ritter, D. M., and J. H. McKerrow. 1996. Intercellular adhesion molecule 1 is the major adhesion molecule expressed during schistosome granuloma formation. Infect. Immun. 64:4706.
23. Kaifi, J. T., E. Diaconu, and E. Pearlman. 2001. Distinct roles for PECAM-1, ICAM-1, and VCAM-1 in recruitment of neutrophils and eosinophils to the cornea in ocular onchocerciasis (river blindness). J. Immunol. 166:6795.
24. Kim, P. K., Y. G. Kwon, H. T. Chung, and Y. M. Kim. 2002. Regulation of caspases by nitric oxide. Ann. NY Acad. Sci. 962:42.
25. Ashany, D., A. Savir, N. Bhardwaj, and K. B. Elkon. 1999. Dendritic cells are resistant to apoptosis through the Fas (CD95/APO-1) pathway. J. Immunol. 163:5303.
26. Krishnamoorthy, B., K. Narayanan, S. Miyamoto, and A. Balakrishnan. 2000. Epithelial cells release proinflammatory cytokines and undergo c-Myc-induced apoptosis on exposure to filarial parasitic sheath protein: Bcl2 mediates rescue by activating c-H-Ras. In Vitro Cell. Dev. Biol. Anim. 36:532.
27. Taylor, M. J., H. F. Cross, and K. Bilo. 2000. Inflammatory responses induced by the filarial nematode Brugia malayi are mediated by lipopolysaccharide-like activity from endosymbiotic Wolbachia bacteria. J. Exp. Med. 191:1429.
28. McRae, B. L., B. A. Beilfuss, and G. A. van Seventer. 2000. IFN-β differentially regulates CD40-induced cytokine secretion by human dendritic cells. J. Immunol. 164:23.
29. Ottesen, E. A. 1992. The Wellcome Trust Lecture: Infection and disease in lymphatic filariasis: an immunological perspective. Parasitology 104:S71.
30. Vincent, A. L., A. C. Vickery, M. J. Lotz, and U. Desai. 1984. The lymphatic pathology of Brugia pahangi in nude (athymic) and thymic mice C3H/HeN. J. Parasitol. 70:48.
31. Rao, U. R., A. C. Vickery, B. H. Kwa, and J. K. Nayar. 1996. Regulatory cytokines in the lymphatic pathology of athymic mice infected with Brugia malayi. Int. J. Parasitol. 26:561.
32. Pastrana, D. V., N. Raghavan, P. FitzGerald, S. W. Eisinger, C. Metz, R. Bucala, R. P. Schleimer, C. Bickel, and A. L. Scott. 1998. Filarial nematode parasites secrete a homologue of the human cytokine macrophage migration inhibitory factor. Infect. Immun. 66:5955.
33. Zang, X., P. Taylor, J. M. Wang, D. J. Meyer, A. L. Scott, M. D. Walkinshaw, and R. M. Maizels. 2002. Homologues of human macrophage migration inhibitory factor from a parasitic nematode: gene cloning, protein activity and crystal structure. J. Biol. Chem. 277:44261.
34. Hilkens, C. M., P. Kalinski, M. de Boer, and M. L. Kapsenberg. 1997. Human dendritic cells require exogenous interleukin-12-inducing factors to direct the development of naive T-helper cells toward the Thl phenotype. Blood 90:1920.
35. Kalinski, P., C. M. Hilkens, A. Snijders, F. G. Snijdewint, and M. L. Kapsenberg. 1997. IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J. Immunol. 159:28.
36. Sousa, C. R., S. Hieny, T. Scharton-Kersten, D. Jankovic, H. Charest, R. N. Germain, and A. Sher. 1997. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med 186:1819.
37. Verhasselt, V., C. Buelens, F. Willems, D. De Groote, N. Haeffner-Cavaillon, and M. Goldman. 1997. Bacterial lipopolysaccharide stimulates the production of cytokines and the expression of costimulatory molecules by human peripheral blood dendritic cells: evidence for a soluble CD14-dependent pathway. J. Immunol. 158:2919.
38. Koch, F., U. Stanzl, P. Jennewein, K. Janke, C. Heufler, E. Kampgen, N. Romani, and G. Schuler. 1996. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J. Exp. Med. 184:741.
39. Snijders, A., P. Kalinski, C. M. Hilkens, and M. L. Kapsenberg. 1998. High-level IL-12 production by human dendritic cells requires two signals. Int. Immunol. 10:1593.
40. + human T cells in vitro. J. Immunol. 160:351.
41. Ottesen, E. A., F. Skvaril, S. P. Tripathy, R. W. Poindexter, and R. Hussain. 1985. Prominence of IgG4 in the IgG antibody response to human filariasis. J. Immunol. 134:2707.
42. Kumiawan, A., M. Yazdanbakhsh, R. van Ree, R. Aalberse, M. E. Selkirk, F. Partono, and R. M. Maizels. 1993. Differential expression of IgE and IgG4 specific antibody responses in asymptomatic and chronic human filariasis. J. Immunol. 150:3941.