Expansion of Foxp3+ regulatory T cells in mice infected with the filarial parasite Brugia malayi

Journal of Immunology

Volumn 181, Issue 9, 2008, Pages 6456-6466

  McSorley, Henry J ^a   Harcus, Yvonne M ^a   Murray, Janice ^a   Taylor, Matthew D ^a   Maizels, Rick M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4 RECEPTOR; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; BAGG ALBINO MOUSE; BRUGIAN FILARIASIS; CD25+ T LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL MATURATION; CELL POPULATION; CONTROLLED STUDY; FLOW CYTOMETRY; HOST RESISTANCE; IMMUNE DEFICIENCY; LARVA; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PERITONEUM LAVAGE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TH2 CELL; ADOPTIVE TRANSFER; ANIMAL; BIOSYNTHESIS; BRUGIA MALAYI; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; FILARIASIS; GENETICS; GERBIL; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; PARASITOLOGY; PATHOLOGY; TRANSGENIC MOUSE; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; BRUGIA MALAYI; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; FILARIASIS; FORKHEAD TRANSCRIPTION FACTORS; GERBILLINAE; HUMANS; LYMPHOCYTE ACTIVATION; MACROPHAGE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, INTERLEUKIN-4; T-LYMPHOCYTES, REGULATORY;

EID: 57449084307     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.9.6456     Document Type: Article

References (76)

1. Nutman, T. B., ed. 1999. Lymphatic Filariasis. Imperial College Press, London.
2. Hoerauf, A. 2003. Control of filarial infections: not the beginning of the end, but more research is needed. Curr. Opin. Infect. Dis. 16: 403-410. (Pubitemid 37267259)
3. Rajan, T. V., and A. V. Gundlapalli. 1997. Lymphatic Filariasis. In Immunopathogenetic Aspects of Disease Induced by Helminth Parasites: Chemical Immunology. D. O. Freedman, ed. Karger, Basel, p. 125.
4. Dreyer, G., J. Norões, J. Figuerdo-Silva, and W. F. Piessens. 2000. Pathogenesis of lymphatic disease in Bancroftian filariasis: a clinical perspective. Parasitol. Today 16: 544-548.
5. Piessens, W. F., P. B. McGreevy, P. W. Piessens, M. McGreevy, I. Koiman, J. S. Saroso, and D. T. Dennis. 1980. Immune responses in human infections with Brugia malayi: specific cellular unresponsiveness to filarial antigens. J. Clin. Invest. 65: 172-179.
6. King, C. L., V. Kumaraswami, R. W. Poindexter, S. Kumari, K. Jayaraman, D. W. Alling, E. A. Ottesen, and T. B. Nutman. 1992. Immunologic tolerance in lymphatic filariasis: diminished parasite-specific T and B cell lymphocyte precursor frequency in the microfilaremic state. J. Clin. Invest. 89: 1403-1410.
7. Sartono, E., Y. C. M. Kruize, A. Kurniawan-Atmadja, R. M. Maizels, and M. Yazdanbakhsh. 1997. Depression of antigen-specific interleukin-5 and interferon-γ responses in human lymphatic filariasis as a function of clinical status and age. J. Infect. Dis. 175: 1276-1280. (Pubitemid 27176529)
8. Nutman, T. B., and V. Kumaraswami. 2001. Regulation of the immune response in lymphatic filariasis: perspectives on acute and chronic infection with Wuchereria bancrofti in South India. Parasite Immunol. 23: 389-399.
9. Brattig, N. W., B. Lepping, C. Timmann, D. W. Büttner, Y. Marfo, C. Hamelmann, and R. D. Horstmann. 2002. Onchocerca volvulus-exposed persons fail to produce interferon-γ in response to O. volvulus antigen but mount proliferative responses with interleukin-5 and IL-13 production that decrease with increasing microfilarial density. J. Infect. Dis. 185: 1148-1154.
10. Nutman, T. B., V. Kumaraswami, and E. A. Ottesen. 1987. Parasite-specific anergy in human filariasis: insights after analysis of parasite antigen-driven lymphokine production. J. Clin. Invest. 79: 1516-1523.
11. Sartono, E., Y. C. M. Kruize, A. Kurniawan, P. H. van der Meide, F. Partono, R. M. Maizels, and M. Yazdanbakhsh. 1995. Elevated cellular responses and interferon-γ release after long-term diethylcarbamazine treatment of patients with human lymphatic filariasis. J. Infect. Dis. 171: 1683-1687.
12. Steel, C., A. Lujan-Trangay, C. Gonzalez-Peralta, G. Zea-Flores, and T. B. Nutman. 1991. Immunologic responses to repeated ivermectin treatment in patients with onchocerciasis. J. Infect. Dis. 164: 581-587.
13. Babu, S., C. P. Blauvelt, V. Kumaraswami, and T. B. Nutman. 2006. Regulatory networks induced by live parasites impair both Th1 and Th2 pathways in patent lymphatic filariasis: implications for parasite persistence. J. Immunol. 176: 3248-3256. (Pubitemid 43306989)
14. + regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22: 531-562.
15. Fontenot, J. D., and A. Y. Rudensky. 2005. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat. Immunol. 6: 331-337.
16. Belkaid, Y. 2007. Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 7: 875-888. (Pubitemid 350006238)
17. Doetze, A., J. Satoguina, G. Burchard, T. Rau, C. Loliger, B. Fleischer, and A. Hoerauf. 2000. Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by Th3/Tr1-type cytokines IL-10 and transforming growth factor-β but not by a Th1 to Th2 shift. Int. Immunol. 12: 623-630. (Pubitemid 30248895)
18. Hoerauf, A., and N. Brattig. 2002. Resistance and susceptibility in human onchocerciasis-beyond Th1 vs. Th2. Trends Parasitol. 18: 25-31. (Pubitemid 34155307)
19. Maizels, R. M., and M. Yazdanbakhsh. 2003. Regulation of the immune response by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3: 733-743.
20. Hoerauf, A., J. Satoguina, M. Saeftel, and S. Specht. 2005. Immunomodulation by filarial nematodes. Parasite Immunol. 27: 417-429.
21. Mahanty, S., S. N. Mollis, M. Ravichandran, J. S. Abrams, V. Kumaraswami, K. Jayaraman, E. A. Ottesen, and T. B. Nutman. 1996. High levels of spontaneous and parasite antigen-driven interleukin-10 production are associated with antigen-specific hyporesponsiveness in human lymphatic filariasis. J. Infect. Dis. 173: 769-773. (Pubitemid 26064084)
22. 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: 1667-1673.
23. Satoguina, J., M. Mempel, J. Larbi, M. Badusche, C. Loliger, O. Adjei, G. Gachelin, B. Fleischer, and A. Hoerauf. 2002. Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes Infect. 4: 1291-1300. (Pubitemid 35356455)
24. Lawrence, R. A., and E. Devaney. 2001. Lymphatic filariasis: parallels between the immunology of infection in humans and mice. Parasite Immunol. 23: 353-361.
25. Taylor, M., L. Le Goff, A. Harris, E. Malone, J. E. Allen, and R. M. Maizels. 2005. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 174: 4924-4933. (Pubitemid 40504577)
26. + regulatory T cells inhibit protective immunity to filarial parasites in vivo. J. Immunol. 179: 4626-4634.
27. Dittrich, A. M., A. Erbacher, S. Specht, F. Diesner, M. Krokowski, A. Avagyan, P. Stock, B. Ahrens, W. H. Hoffmann, A. Hoerauf, and E. Hamelmann. 2008. Helminth infection with Litomosoides sigmodontis induces regulatory T cells and inhibits allergic sensitization, airway inflammation, and hyperreactivity in a murine asthma model. J. Immunol. 180: 1792-1799.
28. Wilson, E. H., M. R. Deehan, E. Katz, K. S. Brown, K. M. Houston, J. O'Grady, M. M. Harnett, and W. Harnett. 2003. Hyporesponsiveness of murine B lymphocytes exposed to the filarial nematode phosphorylcholine-containing secreted product ES-62 in vivo. Immunology 109: 238-245. (Pubitemid 36683615)
29. Marshall, F. A., A. M. Grierson, P. Garside, W. Harnett, and M. M. Harnett. 2005. ES-62, an immunomodulator secreted by filarial nematodes suppresses clonal expansion and modifies effector function of heterologous antigen-specific T cells in vivo. J. Immunol. 175: 5817-5826.
30. Gillan, V., and E. Devaney. 2005. Regulatory T cells modulate Th2 responses induced by Brugia pahangi third-stage larvae. Infect. Immun. 73: 4034-4042. (Pubitemid 40923143)
31. Lawrence, R. A. 1996. Lymphatic filariasis: what mice can tell us. Parasitol. Today 12: 267-271. (Pubitemid 26188411)
32. Balmer, P., and E. Devaney. 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. (Pubitemid 34242226)
33. Ramalingam, T., B. Rajan, J. Lee, and T. V. Rajan. 2003. Kinetics of cellular responses to intraperitoneal Brugia pahangi infections in normal and immunodeficient mice. Infect. Immun. 71: 4361-4367. (Pubitemid 36919900)
34. Suswillo, R. R., D. G. Owen, and D. A. Denham. 1980. Infections of Brugia pahangi in conventional and nude (athymic) mice. Acta Trop. 37: 327-335. (Pubitemid 11165317)
35. Lawrence, R. A., J. E. Allen, W. F. Gregory, M. Kopf, and R. M. Maizels. 1995. Infection of IL-4 deficient mice with the parasitic nematode Brugia malayi demonstrates that host resistance is not dependent on a Th2 dominated immune response. J. Immunol. 154: 5995-6001.
36. MacDonald, A. S., R. M. Maizels, R. A. Lawrence, I. Dransfield, and J. E. Allen. 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.
37. + Treg and control of Leishmania major infection. J. Immunol. 174: 5444-5455.
38. Lawrence, R. A., J. E. Allen, J. Osborne, and R. M. Maizels. 1994. Adult and microfilarial stages of the filarial parasite Brugia malayi stimulate contrasting cytokine and immunoglobulin isotype responses in BALB/c mice. J. Immunol. 153: 1216-1224.
39. + T cell hyporesponsiveness at sites peripheral to filarial infection. J. Immunol. 176: 6918-6927.
40. + precursors. J. Immunol. 175: 6107-6116.
41. h2 dominance. Int. Immunol. 18: 1421-1431.
42. Wilson, M. S., M. Taylor, A. Balic, C. A. M. Finney, J. R. Lamb, and R. M. Maizels. 2005. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J. Exp. Med. 202: 1199-1212. (Pubitemid 41586951)
43. + regulatory T cells in Heligmosomoides polygyrus infection. Eur. J. Immunol. 37: 1874-1886.
44. Rausch, S., J. Huehn, D. Kirchhoff, J. Rzepecka, C. Schnoeller, S. Pillai, C. Loddenkemper, A. Scheffold, A. Hamann, R. Lucius, and S. Hartmann. 2008. Functional analysis of effector and regulatory T cells in a parasitic nematode infection. Infect. Immun. 76: 1908-1919. (Pubitemid 351656124)
45. Beiting, D. P., L. F. Gagliardo, M. Hesse, S. K. Bliss, D. Meskill, and J. A. Appleton. 2007. Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-β. J. Immunol. 178: 1039-1047.
46. Hesse, M., C. A. Piccirillo, Y. Belkaid, J. Prufer, M. Mentink-Kane, M. Leusink, A. W. Cheever, E. M. Shevach, and T. A. Wynn. 2004. The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J. Immunol. 172: 3157-3166. (Pubitemid 38263706)
47. Taylor, J. J., M. Mohrs, and E. J. Pearce. 2006. Regulatory T cell responses develop in parallel to Th responses, and control the magnitude and phenotype of the Th effector population. J. Immunol. 176: 5839-5847.
48. + regulatory T cells. J. Exp. Med. 199: 303-313.
49. Steel, C., and T. B. Nutman. 2003. CTLA-4 in filarial infections: implications for a role in diminished T cell reactivity. J. Immunol. 170: 1930-1938.
50. + regulatory cells. J. Immunol. 176: 3321-3329.
51. Kilian, H. D., and G. Nielsen. 1989. Cell-mediated and humoral immune response to tetanus vaccinations in onchocerciasis patients. Trop. Med. Parasitol. 40: 285-291. (Pubitemid 19250999)
52. Kilian, H. D., and G. Nielsen. 1989. Cell-mediated and humoral immune response to BCG and rubella vaccinations and to recall antigens in onchocerciasis patients. Trop. Med. Parasitol. 40: 445-453.
53. Nookala, S., S. Srinivasan, P. Kaliraj, R. B. Narayanan, and T. B. Nutman. 2004. Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis. Infect. Immun. 72: 2598-2604. (Pubitemid 38542386)
54. Greene, B. M., M. M. Fanning, and J. J. Ellner. 1983. Non-specific suppression of antigen-induced lymphocyte blastogenesis in Onchocerca volvulus infection in man. Clin. Exp. Immunol. 52: 259-265.
55. Yazdanbakhsh, M., A. van den Biggelaar, and R. M. Maizels. 2001. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol. 22: 372-377. (Pubitemid 32673643)
56. Maizels, R. M. 2005. Infections and allergy: helminths, hygiene and host immune regulation. Curr. Opin. Immunol. 17: 656-661.
57. Saparov, A., L. A. Kraus, Y. Cong, J. Marwill, X. Y. Xu, C. O. Elson, and C. T. Weaver. 1999. Memory/effector T cells in TCR transgenic mice develop via recognition of enteric antigens by a second, endogenous TCR. Int. Immunol. 11: 1253-1264. (Pubitemid 29355665)
58. Loke, P., A. S. 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: 2669-2678.
59. Rodríguez-Sosa, M., A. R. Satoskar, R. Calderón, L. Gomez-Garcia, R. Saavedra, R. Bojalil, and L. I. Terrazas. 2002. Chronic helminth infection induces alternatively activated macrophages expressing high levels of CCR5 with low interleukin-12 production and Th2-biasing ability. Infect. Immun. 70: 3656-3664. (Pubitemid 34666004)
60. Herbert, D. R., C. Hölscher, M. Mohrs, B. Arendse, A. Schwegmann, M. Radwanska, M. Leeto, R. Kirsch, P. Hall, H. Mossmann, et al. 2004. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20: 623-635. (Pubitemid 38659504)
61. + regulatory T cells induce alternative activation of human monocytes/macrophages. Proc. Natl. Acad. Sci. USA 104: 19446-19451.
62. Hoffmann, W. H., G. Petit, H. Schulz-Key, D. W. Taylor, O. Bain, and L. Le Goff. 2000. Litomosoides sigmodontis in mice: reappraisal of an old model for filarial research. Parasitol. Today 16: 387-389.
63. Nakanishi, H., Y. Horii, and K. Fujita. 1989. The role of macrophages on the expression of sex differences in the susceptibility to Brugia pahangi infection in C57BL/6 mice. J. Helminthol. 63: 213-217. (Pubitemid 19233556)
64. Rajan, T. V., L. Ganley, N. Paciorkowski, L. Spencer, T. R. Klei, and L. D. Shultz. 2002. Brugian infections in the peritoneal cavities of laboratory mice: kinetics of infection and cellular responses. Exp. Parasitol. 100: 235-247.
65. Spencer, L., L. Shultz, and T. V. Rajan. 2001. Interleukin-4 receptor-Stat6 signaling in murine infections with a tissue-dwelling nematode parasite. Infect. Immun. 69: 7743-7752. (Pubitemid 33086605)
66. Specht, S., L. Volkmann, T. Wynn, and A. Hoerauf. 2004. Interleukin-10 (IL-10) counterregulates IL-4-dependent effector mechanisms in murine filariasis. Infect. Immun. 72: 6287-6293. (Pubitemid 39425406)
67. Martin, C., K. M. Al-Qaoud, M. N. Ungeheuer, K. Paehle, P. N. Vuong, O. Bain, B. Fleischer, and A. Hoerauf. 2000. IL-5 is essential for vaccine-induced protection and for resolution of primary infection in murine filariasis. Med. Microbiol. Immunol. 189: 67-74.
68. Martin, C., L. Le Goff, M.-N. Ungeheuer, P. N. Vuong, and O. Bain. 2000. Drastic reduction of a filarial infection in eosinophilic interleukin-5 transgenic mice. Infect. Immun. 68: 3651-3656. (Pubitemid 30340470)
69. Semnani, R. T., M. Law, J. Kubofcik, and T. B. Nutman. 2004. Filaria-induced immune evasion: suppression by the infective stage of Brugia malayi at the earliest host-parasite interface. J. Immunol. 172: 6229-6238.
70. Maizels, R. M., N. Gomez-Escobar, W. F. Gregory, J. Murray, and X. Zang. 2001. Immune evasion genes from filarial nematodes. Int. J. Parasitol. 31: 889-898. (Pubitemid 32530623)
71. Gomez-Escobar, N., W. F. Gregory, and R. M. Maizels. 2000. Identification of Bm-tgh-2, a filarial nematode homolog of C. elegans daf-7 and human TGF-β, expressed in microfilarial and adult stages of Brugia malayi. Infect. Immun. 68: 6402-6410. (Pubitemid 30800315)
72. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886.
73. Ghedin, E., S. Wang, J. M. Foster, and B. E. Slatko. 2004. First sequenced genome of a parasitic nematode. Trends Parasitol. 20: 151-153. (Pubitemid 38526124)
74. Hewitson, J. P., Y. M. Harcus, R. S. Curwen, A. A. Dowle, A. K. Atmadja, P. D. Ashton, R. A. Wilson, and R. M. Maizels. 2008. The secretome of the filarial parasite. Brugia malayi: proteomic profile of adult excretory-secretory products. Mol. Biochem. Parasitol. 160: 8-21.
75. Mucida, D., Y. Park, G. Kim, O. Turovskaya, I. Scott, M. Kronenberg, and H. Cheroutre. 2007. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317: 256-260. (Pubitemid 47076203)
76. + T cells. J. Immunol. 175: 1483-1490.