CTLA-4 in filarial infections: Implications for a role in diminished T cell reactivity

Journal of Immunology

Volumn 170, Issue 4, 2003, Pages 1930-1938

  Nutman, Cathy Steel Thomas B ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 5; MESSENGER RNA;

ADOLESCENT; ADULT; ANTIGEN SPECIFICITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; ENDEMIC DISEASE; FEMALE; FILARIASIS; FLOW CYTOMETRY; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; MICROFILARIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; SUPPRESSOR CELL; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL;

EID: 0037442134     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.170.4.1930     Document Type: Article

References (62)

1. Steel, C., A. Guinea, and E. A. Ottesen. 1996. Evidence for protective immunity to bancroftian filariasis in the Cook Islands. J. Infect. Dis. 174:598.
2. Soboslay, P. T., S. M. Geiger, N. Weiss, M. Banla, C. G. Luder, C. M. Dreweck, E. Batchassi, B. A. Boatin, A. Stadler, and H. Schulz-Key. 1997. The diverse expression of immunity in humans at distinct states of Onchocerca volvulus infection. Immunology 90:592.
3. 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 T(h)3/T(r)1-type cytokines IL-10 and transforming growth factor-β but not by a T(h)l to T(h)2 shift. Int. Immunol. 12:623.
4. 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.
5. 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.
6. Osborne, J., and E. Devaney. 1999. Interleukin-10 and antigen-presenting cells actively suppress Th1 cells in BALB/c mice infected with the filarial parasite Brugia pahangi. Infect. Immun. 67:1599.
7. 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.
8. Osborne, J., S. J. Hunter, E. Devaney, J. S. Jenson, and R. O'Connor. 1996. Anti-interleukin-4 modulation of the Th2 polarized response to the parasitic nematode Brugia pahangi. Infect. Immun. 64:3461.
9. Piessens, W. F., F. Partono, S. L. Hoffman, S. Ratiwayanto, P. W. Piessens, J. R. Palmieri, I. Koiman, D. T. Dennis, and W. P. Carney. 1982. Antigen-specific suppressor T lymphocytes in human lymphatic filariasis. N. Engl. J. Med. 307:144.
10. Piessens, W. F., S. Ratiwayanto, S. Tuti, J. H. Palmieri, P. W. Piessens, I. Koiman, and D. T. Dennis. 1980. Antigen-specific suppressor cells and suppressor factors in human filariasis with Brugia malayi. N. Engl. J. Med. 302:833.
11. Bosshardt, S. C., S. U. Coleman, C. S. McVay, K. L. Jones, and T. R. Klei. 1995. Impact of microfilaremia on maintenance of a hyporesponsive cellular immune response in Brugia-infected gerbils (Meriones unguiculatus). Infect. Immun. 63:940.
12. 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.
13. Steel, C., A. Guinea, J. S. McCarthy, and E. A. Ottesen. 1994. Long-term effect of prenatal exposure to maternal microfilaraemia on immune responsiveness to filarial parasite antigens. Lancet 343:890.
14. Elson, L. H., A. Days, M. Calvopina, W. Paredes, E. Araujo, R. H. Guderian, J. E. Bradley, and T. B. Nutman. 1996. In utero exposure to Onchocerca volvulus: relationship to subsequent infection intensity and cellular immune responsiveness. Infect. Immun. 64:5061.
15. Pit, D. S., A. M. Polderman, H. Schulz-Key, and P. T. Soboslay. 2000. Prenatal immune priming with helminth infections: parasite-specific cellular reactivity and Th1 and Th2 cytokine responses in neonates. Allergy 55:732.
16. Lammie, P. J., W. L. Hitch, E. M. Walker Allen, W. Hightower, and M. L. Eberhard. 1991. Maternal filarial infection as risk factor for infection in children. Lancet 337:1005.
17. Klei, T. R., D. P. Blanchard, and S. U. Coleman. 1986. Development of Brugia pahangi infections and lymphatic lesions in male offspring of female jirds with homologous infections. Trans. R. Soc. Trop. Med. Hyg. 80:214.
18. Schrater, A. F., A. Spielman, and W. F. Piessens. 1983. Predisposition to Brugia malayi microfilaremia in progeny of infected gerbils. Am. J. Trop. Med. Hyg. 32:1306.
19. Linsley, P. S., J. L. Greene, P. Tan, J. Bradshaw, J. A. Ledbetter, C. Anasetti, and N. K. Damle. 1992. Coexpression and functional cooperation of CTLA-4 and CD28 on activated T lymphocytes, J. Exp. Med. 176:1595.
20. Walunas, T. L., C. Y. Bakker, and J. A. Bluestone. 1996. CTLA-4 ligation blocks CD28-dependent T cell activation. J. Exp. Med. 183:2541.
21. L induction. J. Immunol. 160:12.
22. Brunner, M. C., C. A. Chambers, F. K. Chan, J. Hanke, A. Winoto, and J. P. Allison. 1999. CTLA-4-mediated inhibition of early events of T cell proliferation. J. Immunol. 162:5813.
23. Krummel, M. F., and J. P. Allison. 1996. CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J. Exp. Med. 183:2533.
24. Greenwald, R. J., V. A. Boussiotis, R. B. Lorsbach, A. K. Abbas. and A. H. Sharpe. 2001. CTLA-4 regulates induction of anergy in vivo. Immunity 14:145.
25. Gribben, J. G., G. J. Freeman, V. A. Boussiotis, P. Rennert, C. L. Jellis. E. Greenfield, M. Barber, V. A. Restivo, Jr., X. Ke, G. S. Gray, et al. 1995. CTLA-4 mediates antigen-specific apoptosis of human T cells. Proc. Natl. Acad. Sci. USA 92:811.
26. Krummel, M. F., and J. P. Allison. 1995. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J. Exp. Med. 182:459.
27. Egen, J. G., and J. P. Allison. 2002. Cytotoxic T lymphocyte antigen-4 accumulation in the immunological synapse is regulated by TCR signal strength. Immunity 16:23.
28. Anderson, D. E., K. D. Bieganowska, A. Bar-Or, E. M. Oliveira, B. Carreno, M. Collins, and D. A. Hafler. 2000. Paradoxical inhibition of T-cell function in response to CTLA-4 blockade: heterogeneity within the human T-cell population. Nat. Med. 6:211.
29. Oosterwegel, M. A., D. A. Mandelbrot, S. D. Boyd, R. B. Lorsbach, D. Y. Jarrett, A. K. Abbas, and A. H. Sharpe. 1999. The role of CTLA-4 in regulating Th2 differentiation. J. Immunol. 163:2634.
30. Khattri, R., J. A. Auger, M. D. Griffin, A. H. Sharpe, and J. A. Bluestone. 1999. Lymphoproliferative disorder in CTLA-4 knockout mice is characterized by CD28-regulated activation of Th2 responses. J. Immunol. 162:5784.
31. Saha, B., S. Chattopadhyay, R. Germond, D. M. Harlan, and P. J. Perrin. 1998. CTLA-4 (CD152) modulates the Th subset response and alters the course of experimental Leishmania major infection. Eur. J. Immunol. 28:4213.
32. McCoy, K., M. Camberis, and G. L. Gros. 1997. Protective immunity to nematode infection is induced by CTLA-4 blockade. J. Exp. Med. 186:183.
33. Borkow, G., Q. Leng, Z. Weisman, M. Stein, N. Galai, A. Kalinkovich, and Z. Bentwich. 2000. Chronic immune activation associated with intestinal helminth infections results in impaired signal transduction and anergy. J. Clin. Invest. 106:1053.
34. Gusmao, R. D., A. M. Stanley, and E. A. Ottesen. 1981. Brugia pahangi: immunologic evaluation of the differential susceptibility of filarial infection in inbred Lewis rats. Exp. Parasitol. 52:147.
35. 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.
36. Nutman. T. B., P. A. Zimmerman, J. Kubofcik, and D. D. Kostyu. 1994. A universally applicable diagnostic approach to filarial and other infections. Parasitol. Today 10:239.
37. Henry, N. L., M. Law, T. B. Nutman, and A. D. Klion. 2001. Onchocerciasis in a nonendemic population: clinical and immunologic assessment before treatment and at the time of presumed cure. J. Infect. Dis. 183:512.
38. + T cells. Proc. Natl. Acad. Sci. USA 97:12711.
39. Tivol, E. A., F. Borriello, A. N. Schweitzer, W. P. Lynch, J. A. Bluestone, and A. H. Sharpe. 1995. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3:541.
40. + regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med. 192:303.
41. Steel, C., and E. A. Ottesen. 2001. Evolution of immunologic responsiveness of persons living in an area of endemic bancroftian filariasis: a 17-year follow-up. J. Infect. Dis. 184:73.
42. Gopinath, R., L. E. Hanna, V. Kumaraswami, S. V. Pillai, V. Kavitha, V. Vijayasekaran, A. Rajasekharan, and T. B. Nutman. 1999. Long-term persistence of cellular hyporesponsiveness to filarial antigens after clearance of microfilaremia. Am. J. Trop. Med. Hyg. 60:848.
43. Klion, A. D., M. Massougbodji, B.-C. Sadeler, E. A. Ottesen, and T. B. Nutman. 1991. Loiasis in endemic and non-endemic populations: immunologically mediated differences in clinical presentation. J. Infect. Dis. 163: 1318.
44. Cooper, P. J., T. Mancero, M. Espinel, C. Sandoval, R. Lovato, R. H. Guderian, and T. B. Nutman. 2001. Early human infection with Onchocerca volvulus is associated with an enhanced parasite-specific cellular immune response. J. Infect. Dis. 183:1662.
45. + anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity. Blood 99:2468.
46. King, C. L., S. Mahanty, V. Kumaraswami, J. S. Abrams, J. Raganathan, 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 Th2 lymphocyte subset. J. Clin. Invest. 92:1667.
47. 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.
48. + T cells induced by low avidity engagement of T cell receptor. J. Exp. Med. 194:719.
49. + T cells toward the Th1 subset by CTLA-4 costimulation. J. Immunol. 164:3554.
50. Alegre, M. L., H. Shiels, C. B. Thompson, and T. F. Gajewski. 1998. Expression and function of CTLA-4 in Th1 and Th2 cells. J. Immunol. 161:3347.
51. Walunas, T. L., and J. A. Bluestone. 1998. CTLA-4 regulates tolerance induction and T cell differentiation in vivo. J. Immunol. 160:3855.
52. Folkard, S. G., M. J. Taylor, G. A. Butcher, and A. E. Bianco. 1997. Protective responses against skin-dwelling microfilariae of Onchocerca lienalis in severe combined immunodeficient mice. Infect. Immun. 65:2846.
53. Herbert, D. R., J. J. Lee, N. A. Lee, T. J. Nolan, G. A. Schad, and D. Abraham. 2000. Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. J. Immunol. 165:4544.
54. 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.
55. Taylor, M. J., R. P. van Es, K. Shay, S. G. Folkard, S. Townson, and A. E. Bianco. 1994. Protective immunity against Onchocerca volvulus and O. lienalis infective larvae in mice. Trop. Med. ParasitoL 45:17.
56. Hogarth, P. J., S. G. Folkard, M. J. Taylor, and A. E. Bianco. 1995. Accelerated clearance of Onchocerca microfilariae and resistance to reinfection in interleukin-4 gene knockout mice. Parasite Immunol. 17:653.
57. Bancroft, A. J., K. J. Else, R. K. Grencis, C. Martin, M. Saeftel, P. N. Vuong, S. Babayan, K. Fischer, O. Bain, and A. Hoerauf. 1994. Low-level infection with Trichuris muris significantly affects the polarization of the CD4 response. Eur. J. Immunol. 24:3113.
58. Volkmann, L., M. Saeftel, O. Bain, K. Fischer, B. Fleischer, and A. Hoerauf. 2001. Interleukin-4 is essential for the control of microfilariae in murine infection with the filaria Litomosoides sigmodontis. Infect. Immun. 69:2950.
59. Perez, V. L., L. Van Parijs, A. Biuckians, X. X. Zheng, T. B. Strom, and A. K. Abbas. 1997. Induction of peripheral T cell tolerance in vivo requires CTLA-4 engagement. Immunity 6:411.
60. Steel, C., and T. B. Nutman. 1993. Regulation of IL-5 in onchocerciasis: a critical role for IL-2. J. Immunol. 150:5511.
61. + regulatory cells that control intestinal inflammation. J. Exp. Med. 192:295.
62. + T regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J. Exp. Med. 193:1295.