Interferon-γ - Central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria

Journal of Leukocyte Biology

Volumn 88, Issue 6, 2010, Pages 1131-1143

  McCall, Matthew B B ^a   Sauerwein, Robert W ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Adaptive; Cytokine; Falciparum; Human; Innate; Vaccine

Indexed keywords

CYTOKINE; GAMMA INTERFERON; MALARIA VACCINE;

ADAPTIVE IMMUNITY; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; ERYTHROCYTE; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOPATHOLOGY; INNATE IMMUNITY; MALARIA; NONHUMAN; OUTCOME ASSESSMENT; PLASMODIUM; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVIEW;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; ERYTHROCYTES; HUMANS; INFLAMMATION; INTERFERON-GAMMA; MALARIA; MALARIA VACCINES;

PLASMODIUM PARASITES;

EID: 78649736819     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0310137     Document Type: Review

References (232)

1. Schroder, K., Hertzog, P. J., Ravasi, T., Hume, D. A. (2004) Interferon-γ: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 75, 163-189.
2. Gessani, S., Belardelli, F. (1998) IFN-γ expression in macrophages and its possible biological significance. Cytokine Growth Factor Rev. 9, 117-123.
3. Frucht, D. M., Fukao, T., Bogdan, C., Schindler, H., O'Shea, J. J., Koyasu, S. (2001) IFN-γ production by antigen-presenting cells: mechanisms emerge. Trends Immunol. 22, 556-560.
4. Munder, M., Mallo, M., Eichmann, K., Modolell, M. (1998) Murine macrophages secrete interferon γ upon combined stimulation with interleukin (IL)-12 and IL-18: a novel pathway of autocrine macrophage activation. J. Exp. Med. 187, 2103-2108.
5. Otani, T., Nakamura, S., Toki, M., Motoda, R., Kurimoto, M., Orita, K. (1999) Identification of IFN-γ-producing cells in IL-12/IL-18-treated mice. Cell. Immunol. 198, 111-119.
6. Buchmeier, N. A., Schreiber, R. D. (1985) Requirement of endogenous interferon-γ production for resolution of Listeria monocytogenes infection. Proc. Natl. Acad. Sci. USA 82, 7404-7408.
7. Huang, S., Hendriks, W., Althage, A., Hemmi, S., Bluethmann, H., Kamijo, R., Vilcek, J., Zinkernagel, R. M., Aguet, M. (1993) Immune response in mice that lack the interferon-γ receptor. Science 259, 1742-1745.
8. Van den Broek, M. F., Muller, U., Huang, S., Zinkernagel, R. M., Aguet, M. (1995) Immune defense in mice lacking type I and/or type II interferon receptors. Immunol. Rev. 148, 5-18.
9. Murray, H. W., Rubin, B. Y., Rothermel, C. D. (1983) Killing of intracellular Leishmania donovani by lymphokine-stimulated human mononuclear phagocytes. Evidence that interferon-γ is the activating lymphokine. J. Clin. Invest. 72, 1506-1510.
10. Torrico, F., Heremans, H., Rivera, M. T., Van, M. E., Billiau, A., Carlier, Y. (1991) Endogenous IFN-γ is required for resistance to acute Trypanosoma cruzi infection in mice. J. Immunol. 146, 3626-3632.
11. Scharton-Kersten, T. M., Wynn, T. A., Denkers, E. Y., Bala, S., Grunvald, E., Hieny, S., Gazzinelli, R. T., Sher, A. (1996) In the absence of endogenous IFN-γ, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J. Immunol. 157, 4045-4054.
12. Miller, L. H., Howard, R. J., Carter, R., Good, M. F., Nussenzweig, V., Nussenzweig, R. S. (1986) Research toward malaria vaccines. Science 234, 1349-1356.
13. Kuvin, S. F., Tobie, J. E., Evans, C. B., Coatney, G. R., Contacos, P. G. (1962) Antibody production in human malaria as determined by the fluorescent antibody technique. Science 135, 1130-1131.
14. Clyde, D. F., McCarthy, V. C., Miller, R. M., Hornick, R. B. (1973) Specificity of protection of man immunized against sporozoite-induced falciparum malaria. Am. J. Med. Sci. 266, 398-403.
15. Doolan, D. L., Martinez-Alier, N. (2006) Immune response to pre-erythrocytic stages of malaria parasites. Curr. Mol. Med. 6, 169-185.
16. Perrin, L. H., Dayal, R. (1982) Immunity to asexual erythrocytic stages of Plasmodium falciparum: role of defined antigens in the humoral response. Immunol. Rev. 61, 245-269.
17. Yazdani, S. S., Mukherjee, P., Chauhan, V. S., Chitnis, C. E. (2006) Immune responses to asexual blood-stages of malaria parasites. Curr. Mol. Med. 6, 187-203.
18. Beeson, J. G., Osier, F. H., Engwerda, C. R. (2008) Recent insights into humoral and cellular immune responses against malaria. Trends Parasitol. 24, 578-584.
19. Pombo, D. J., Lawrence, G., Hirunpetcharat, C., Rzepczyk, C., Bryden, M., Cloonan, N., Anderson, K., Mahakunkijcharoen, Y., Martin, L. B., Wilson, D., Elliott, S., Elliott, S., Eisen, D. P., Weinberg, J. B., Saul, A., Good, M. F. (2002) Immunity to malaria after administration of ultralow doses of red cells infected with Plasmodium falciparum. Lancet 360, 610-617.
20. Roestenberg, M., McCall, M., Hopman, J., Wiersma, J., Luty, A. J., van Gemert, G. J., van de Vegte-Bolmer, M., van Schaijk, B., Teelen, K., Arens, T., Spaarman, L., de Mast, Q., Roeffen, W., Snounou, G., Rénia, L., van der Ven, A., Hermsen, C. C., Sauerwein, R. (2009) Protection against a malaria challenge by sporozoite inoculation. N. Engl. J. Med. 361, 468-477.
21. Kumaratilake, L. M., Ferrante, A. (1994) T-cell cytokines in malaria: their role in the regulation of neutrophil- and macrophage-mediated killing of Plasmodium falciparum asexual blood forms. Res. Immunol. 145, 423-429.
22. Bouharoun-Tayoun, H., Oeuvray, C., Lunel, F., Druilhe, P. (1995) Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J. Exp. Med. 182, 409-418.
23. Nussler, A. K., Renia, L., Pasquetto, V., Miltgen, F., Matile, H., Mazier, D. (1993) In vivo induction of the nitric oxide pathway in hepatocytes after injection with irradiated malaria sporozoites, malaria blood parasites or adjuvants. Eur. J. Immunol. 23, 882-887.
24. Seguin, M. C., Klotz, F. W., Schneider, I., Weir, J. P., Goodbary, M., Slayter, M., Raney, J. J., Aniagolu, J. U., Green, S. J. (1994) Induction of nitric oxide synthase protects against malaria in mice exposed to irradiated Plasmodium berghei infected mosquitoes: involvement of interferon γ and CD8+T cells. J. Exp. Med. 180, 353-358.
25. Tsuji, M., Miyahira, Y., Nussenzweig, R. S., Aguet, M., Reichel, M., Zavala, F. (1995) Development of antimalaria immunity in mice lacking IFN-γ receptor. J. Immunol. 154, 5338-5344.
26. Ockenhouse, C. F., Schulman, S., Shear, H. L. (1984) Induction of crisis forms in the human malaria parasite Plasmodium falciparum by γ-interferon-activated, monocyte-derived macrophages. J. Immunol. 133, 1601-1608.
27. Shear, H. L., Srinivasan, R., Nolan, T., Ng, C. (1989) Role of IFN-γ in lethal and nonlethal malaria in susceptible and resistant murine hosts. J. Immunol. 143, 2038-2044.
28. Su, Z., Stevenson, M. M. (2000) Central role of endogenous γ interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect. Immun. 68, 4399-4406.
29. Wang, Q. H., Liu, Y. J., Liu, J., Chen, G., Zheng, W., Wang, J. C., Cao, Y. M. (2009) Plasmodium yoelii: assessment of production and role of nitric oxide during the early stages of infection in susceptible and resistant mice. Exp. Parasitol. 121, 268-273.
30. Kumaratilake, L. M., Ferrante, A. (2000) Opsonization and phagocytosis of Plasmodium falciparum merozoites measured by flow cytometry. Clin. Diagn. Lab. Immunol. 7, 9-13.
31. Yoneto, T., Waki, S., Takai, T., Tagawa, Y., Iwakura, Y., Mizuguchi, J., Nariuchi, H., Yoshimoto, T. (2001) A critical role of Fc receptor-mediated antibody-dependent phagocytosis in the host resistance to blood-stage Plasmodium berghei XAT infection. J. Immunol. 166, 6236-6241.
32. Su, Z., Fortin, A., Gros, P., Stevenson, M. M. (2002) Opsonin-independent phagocytosis: an effector mechanism against acute blood-stage Plasmodium chabaudi AS infection. J. Infect. Dis. 186, 1321-1329.
33. Naotunne, T. S., Karunaweera, N. D., Del, G. G., Kularatne, M. U., Grau, G. E., Carter, R., Mendis, K. N. (1991) Cytokines kill malaria parasites during infection crisis: extracellular complementary factors are essential. J. Exp. Med. 173, 523-529.
34. McCall, M. B., Netea, M. G., Hermsen, C. C., Jansen, T., Jacobs, L., Golenbock, D., van der Ven, A. J., Sauerwein, R. W. (2007) Plasmodium falciparum infection causes proinflammatory priming of human TLR responses. J. Immunol. 179, 162-171.
35. Adegnika, A. A., Kohler, C., Agnandji, S. T., Chai, S. K., Labuda, L., Breitling, L. P., Schonkeren, D., Weerdenburg, E., Issifou, S., Luty, A. J., Kremsner, P. G., Yazdanbakhsh, M. (2008) Pregnancy-associated malaria affects Toll-like receptor ligand-induced cytokine responses in cord blood. J. Infect. Dis. 198, 928-936.
36. Hartgers, F. C., Obeng, B. B., Voskamp, A., Larbi, I. A., Amoah, A. S., Luty, A. J., Boakye, D., Yazdanbakhsh, M. (2008) Enhanced Toll-like receptor responsiveness associated with mitogen-activated protein kinase activation in Plasmodium falciparum-infected children. Infect. Immun. 76, 5149-5157.
37. Franklin, B. S., Parroche, P., Ataide, M. A., Lauw, F., Ropert, C., de Oliveira, R. B., Pereira, D., Tada, M. S., Nogueira, P., da Silva, L. H., Bjorkbacka, H., Golenbock, D. T., Gazzinelli, R. T. (2009) Malaria primes the innate immune response due to interferon-γ induced enhancement of Toll-like receptor expression and function. Proc. Natl. Acad. Sci. USA 106, 5789-5794.
38. Brustoski, K., Moller, U., Kramer, M., Petelski, A., Brenner, S., Palmer, D. R., Bongartz, M., Kremsner, P. G., Luty, A. J., Krzych, U. (2005) IFN-γ and IL-10 mediate parasite-specific immune responses of cord blood cells induced by pregnancy-associated Plasmodium falciparum malaria. J. Immunol. 174, 1738-1745.
39. Winkler, S., Willheim, M., Baier, K., Schmid, D., Aichelburg, A., Graninger, W., Kremsner, P. G. (1998) Reciprocal regulation of Th1- and Th2-cytokine-producing T cells during clearance of parasitemia in Plasmodium falciparum malaria. Infect. Immun. 66, 6040-6044.
40. Tongren, J. E., Corran, P. H., Jarra, W., Langhorne, J., Riley, E. M. (2005) Epitope-specific regulation of immunoglobulin class switching in mice immunized with malarial merozoite surface proteins. Infect. Immun. 73, 8119-8129.
41. Bejon, P., Keating, S., Mwacharo, J., Kai, O. K., Dunachie, S., Walther, M., Berthoud, T., Lang, T., Epstein, J., Carucci, D., Moris, P., Cohen, J., Gilbert, S. C., Peshu, N., Marsh, K., Hill, A. V. (2006) Early γ interferon and interleukin-2 responses to vaccination predict the late resting memory in malaria-naive and malaria-exposed individuals. Infect. Immun. 74, 6331-6338.
42. Todryk, S. M., Walther, M., Bejon, P., Hutchings, C., Thompson, F. M., Urban, B. C., Porter, D. W., Hill, A. V. (2009) Multiple functions of human T cells generated by experimental malaria challenge. Eur. J. Immunol. 39, 3042-3051.
43. Schofield, L., Villaquiran, J., Ferreira, A., Schellekens, H., Nussenzweig, R., Nussenzweig, V. (1987) γ Interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330, 664-666.
44. Hoffman, S. L., Isenbarger, D., Long, G. W., Sedegah, M., Szarfman, A., Waters, L., Hollingdale, M. R., van der Meide, P. H., Finbloom, D. S., Ballou, W. R. (1989) Sporozoite vaccine induces genetically restricted T cell elimination of malaria from hepatocytes. Science 244, 1078-1081.
45. Doolan, D. L., Sedegah, M., Hedstrom, R. C., Hobart, P., Charoenvit, Y., Hoffman, S. L. (1996) Circumventing genetic restriction of protection against malaria with multigene DNA immunization: CD8+ cell-, interferon γ-, and nitric oxide-dependent immunity. J. Exp. Med. 183, 1739-1746.
46. Wang, R., Charoenvit, Y., Corradin, G., De La Vega, P., Franke, E. D., Hoffman, S. L. (1996) Protection against malaria by Plasmodium yoelii sporozoite surface protein 2 linear peptide induction of CD4+ T cell- and IFN-γ-dependent elimination of infected hepatocytes. J. Immunol. 157, 4061-4067.
47. Doolan, D. L., Hoffman, S. L. (1999) IL-12 and NK cells are required for antigen-specific adaptive immunity against malaria initiated by CD8+ T cells in the Plasmodium yoelii model. J. Immunol. 163, 884-892.
48. Belnoue, E., Voza, T., Costa, F. T., Gruner, A. C., Mauduit, M., Rosa, D. S., Depinay, N., Kayibanda, M., Vigario, A. M., Mazier, D., Snounou, G., Sinnis, P., Renia, L. (2008) Vaccination with live Plasmodium yoelii blood stage parasites under chloroquine cover induces cross-stage immunity against malaria liver stage. J. Immunol. 181, 8552-8558.
49. Ferreira, A., Schofield, L., Enea, V., Schellekens, H., van der Meide, P., Collins, W. E., Nussenzweig, R. S., Nussenzweig, V. (1986) Inhibition of development of exoerythrocytic forms of malaria parasites by γ-interferon. Science 232, 881-884. (Pubitemid 16117400)
50. Sedegah, M., Finkelman, F., Hoffman, S. L. (1994) Interleukin 12 induction of interferon γ-dependent protection against malaria. Proc. Natl. Acad. Sci. USA 91, 10700-10702.
51. Hoffman, S. L., Crutcher, J. M., Puri, S. K., Ansari, A. A., Villinger, F., Franke, E. D., Singh, P. P., Finkelman, F., Gately, M. K., Dutta, G. P., Sedegah, M. (1997) Sterile protection of monkeys against malaria after administration of interleukin-12. Nat. Med. 3, 80-83.
52. Walther, M., Woodruff, J., Edele, F., Jeffries, D., Tongren, J. E., King, E., Andrews, L., Bejon, P., Gilbert, S. C., De Souza, J. B., Sinden, R., Hill, A. V., Riley, E. M. (2006) Innate immune responses to human malaria: heterogeneous cytokine responses to blood-stage Plasmodium falciparum correlate with parasitological and clinical outcomes. J. Immunol. 177, 5736-5745.
53. Hoffman, S. L., Goh, L. M., Luke, T. C., Schneider, I., Le, T. P., Doolan, D. L., Sacci, J., de la Vega, P., Dowler, M., Paul, C., Gordon, D. M., Stoute, J. A., Church, L. W., Sedegah, M., Heppner, D. G., Ballou, W. R., Richie, T. L. (2002) Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J. Infect. Dis. 185, 1155-1164.
54. Egan, J. E., Hoffman, S. L., Haynes, J. D., Sadoff, J. C., Schneider, I., Grau, G. E., Hollingdale, M. R., Ballou, W. R., Gordon, D. M. (1993) Humoral immune responses in volunteers immunized with irradiated Plasmodium falciparum sporozoites. Am. J. Trop. Med. Hyg. 49, 166-173.
55. Malik, A., Egan, J. E., Houghten, R. A., Sadoff, J. C., Hoffman, S. L. (1991) Human cytotoxic T lymphocytes against the Plasmodium falciparum circumsporozoite protein. Proc. Natl. Acad. Sci. USA 88, 3300-3304.
56. Moreno, A., Clavijo, P., Edelman, R., Davis, J., Sztein, M., Herrington, D., Nardin, E. (1991) Cytotoxic CD4+ T cells from a sporozoite-immunized volunteer recognize the Plasmodium falciparum CS protein. Int. Immunol. 3, 997-1003.
57. Nardin, E. H., Herrington, D. A., Davis, J., Levine, M., Stuber, D., Takacs, B., Caspers, P., Barr, P., Altszuler, R., Clavijo, P. (1989) Conserved repetitive epitope recognized by CD4+ clones from a malariaimmunized volunteer. Science 246, 1603-1606.
58. Doolan, D. L., Southwood, S., Chesnut, R., Appella, E., Gomez, E., Richards, A., Higashimoto, Y. I., Maewal, A., Sidney, J., Gramzinski, R. A., Mason, C., Koech, D., Hoffman, S. L., Sette, A. (2000) HLA-DR-promiscuous T cell epitopes from Plasmodium falciparum pre-erythrocytic-stage antigens restricted by multiple HLA class II alleles. J. Immunol. 165, 1123-1137.
59. Bejon, P., Mwacharo, J., Kai, O., Todryk, S., Keating, S., Lowe, B., Lang, T., Mwangi, T. W., Gilbert, S. C., Peshu, N., Marsh, K., Hill, A. V. (2007) The induction and persistence of T cell IFN-γ responses after vaccination or natural exposure is suppressed by Plasmodium falciparum. J. Immunol. 179, 4193-4201.
60. Dent, A. E., Chelimo, K., Sumba, P. O., Spring, M. D., Crabb, B. S., Moormann, A. M., Tisch, D. J., Kazura, J. W. (2009) Temporal stability of naturally acquired immunity to merozoite surface protein-1 in Kenyan adults. Malar. J. 8, 162.
61. Moormann, A. M., Sumba, P. O., Tisch, D. J., Embury, P., King, C. H., Kazura, J. W., John, C. C. (2009) Stability of interferon-γ and interleukin-10 responses to Plasmodium falciparum liver stage antigen 1 and thrombospondin-related adhesive protein immunodominant epitopes in a highland population from Western Kenya. Am. J. Trop. Med. Hyg. 81, 489-495.
62. Deloron, P., Chougnet, C., Lepers, J. P., Tallet, S., Coulanges, P. (1991) Protective value of elevated levels of γ interferon in serum against exoerythrocytic stages of Plasmodium falciparum. J. Clin. Microbiol. 29, 1757-1760.
63. Riley, E. M., Allen, S. J., Bennett, S., Thomas, P. J., O'Donnell, A., Lindsay, S. W., Good, M. F., Greenwood, B. M. (1990) Recognition of dominant T cell-stimulating epitopes from the circumsporozoite protein of Plasmodium falciparum and relationship to malaria morbidity in Gambian children. Trans. R. Soc. Trop. Med. Hyg. 84, 648-657.
64. Kurtis, J. D., Lanar, D. E., Opollo, M., Duffy, P. E. (1999) Interleukin-10 responses to liver-stage antigen 1 predict human resistance to Plasmodium falciparum. Infect. Immun. 67, 3424-3429.
65. Migot-Nabias, F., Deloron, P., Ringwald, P., Dubois, B., Mayombo, J., Minh, T. N., Fievet, N., Millet, P., Luty, A. (2000) Immune response to Plasmodium falciparum liver stage antigen-1: geographical variations within Central Africa and their relationship with protection from clinical malaria. Trans. R. Soc. Trop. Med. Hyg. 94, 557-562.
66. Luty, A. J., Lell, B., Schmidt-Ott, R., Lehman, L. G., Luckner, D., Greve, B., Matousek, P., Herbich, K., Schmid, D., Migot-Nabias, F., Deloron, P., Nussenzweig, R. S., Kremsner, P. G. (1999) Interferon-γ responses are associated with resistance to reinfection with Plasmodium falciparum in young African children. J. Infect. Dis. 179, 980-988.
67. May, J., Lell, B., Luty, A. J., Meyer, C. G., Kremsner, P. G. (2001) HLA-DQB1*0501-restricted Th1 type immune responses to Plasmodium falciparum liver stage antigen 1 protect against malaria anemia and reinfections. J. Infect. Dis. 183, 168-172.
68. John, C. C., Moormann, A. M., Sumba, P. O., Ofulla, A. V., Pregibon, D. C., Kazura, J. W. (2004) γ Interferon responses to Plasmodium falciparum liver-stage antigen 1 and thrombospondin-related adhesive protein and their relationship to age, transmission intensity, and protection against malaria. Infect. Immun. 72, 5135-5142.
69. Reece, W. H., Pinder, M., Gothard, P. K., Milligan, P., Bojang, K., Doherty, T., Plebanski, M., Akinwunmi, P., Everaere, S., Watkins, K. R., Voss, G., Tornieporth, N., Alloueche, A., Greenwood, B. M., Kester, K. E., McAdam, K. P., Cohen, J., Hill, A. V. (2004) A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Nat. Med. 10, 406-410.
70. Flanagan, K. L., Mwangi, T., Plebanski, M., Odhiambo, K., Ross, A., Sheu, E., Kortok, M., Lowe, B., Marsh, K., Hill, A. V. (2003) Ex vivo interferon-γ immune response to thrombospondin-related adhesive protein in coastal Kenyans: longevity and risk of Plasmodium falciparum infection. Am. J. Trop. Med. Hyg. 68, 421-430.
71. Todryk, S. M., Bejon, P., Mwangi, T., Plebanski, M., Urban, B., Marsh, K., Hill, A. V., Flanagan, K. L. (2008) Correlation of memory T cell responses against TRAP with protection from clinical malaria, and CD4 CD25 high T cells with susceptibility in Kenyans. PLoS One 3, e2027.
72. Vekemans, J., Leach, A., Cohen, J. (2009) Development of the RTS,S/AS malaria candidate vaccine. Vaccine 27 (Suppl. 6), G67-G71.
73. Sun, P., Schwenk, R., White, K., Stoute, J. A., Cohen, J., Ballou, W. R., Voss, G., Kester, K. E., Heppner, D. G., Krzych, U. (2003) Protective immunity induced with malaria vaccine, RTS,S, is linked to Plasmodium falciparum circumsporozoite protein-specific CD4+ and CD8+ T cells producing IFN-γ. J. Immunol. 171, 6961-6967.
74. Kester, K. E., Cummings, J. F., Ockenhouse, C. F., Nielsen, R., Hall, B. T., Gordon, D. M., Schwenk, R. J., Krzych, U., Holland, C. A., Richmond, G., Dowler, M. G., Williams, J., Wirtz, R. A., Tornieporth, N., Vigneron, L., Delchambre, M., Demoitie, M. A., Ballou, W. R., Cohen, J., Heppner Jr., D. G. (2008) Phase 2a trial of 0, 1, and 3 month and 0, 7, and 28 day immunization schedules of malaria vaccine RTS,S/AS02 in malaria-naive adults at the Walter Reed Army Institute of Research. Vaccine 26, 2191-2202.
75. Kester, K. E., Cummings, J. F., Ofori-Anyinam, O., Ockenhouse, C. F., Krzych, U., Moris, P., Schwenk, R., Nielsen, R. A., Debebe, Z., Pinelis, E., Juompan, L., Williams, J., Dowler, M., Stewart, V. A., Wirtz, R. A., Dubois, M. C., Lievens, M., Cohen, J., Ballou, W. R., Heppner Jr., D. G. (2009) Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J. Infect. Dis. 200, 337-346.
76. Barbosa, A., Naniche, D., Aponte, J. J., Manaca, M. N., Mandomando, I., Aide, P., Sacarlal, J., Renom, M., Lafuente, S., Ballou, W. R., Alonso, P. L. (2009) Plasmodium falciparum-specific cellular immune responses after immunization with the RTS,S/AS02D candidate malaria vaccine in infants living in an area of high endemicity in Mozambique. Infect. Immun. 77, 4502-4509.
77. Cummings, J. F., Spring, M. D., Schwenk, R. J., Ockenhouse, C. F., Kester, K. E., Polhemus, M. E., Walsh, D. S., Yoon, I. K., Prosperi, C., Juompan, L. Y., Lanar, D. E., Krzych, U., Hall, B. T., Ware, L. A., Stewart, V. A., Williams, J., Dowler, M., Nielsen, R. K., Hillier, C. J., Giersing, B. K., Dubovsky, F., Malkin, E., Tucker, K., Dubois, M. C., Cohen, J. D., Ballou, D. R., Heppner, D. G. Jr. (2009) Recombinant liver stage antigen-1 (LSA-1) formulated with AS01 or AS02 is safe, elicits high titer antibody and induces IFN-γ/IL-2 CD4+ T cells but does not protect against experimental Plasmodium falciparum infection. Vaccine , Epub ahead of print.
78. Keating, S. M., Bejon, P., Berthoud, T., Vuola, J. M., Todryk, S., Webster, D. P., Dunachie, S. J., Moorthy, V. S., McConkey, S. J., Gilbert, S. C., Hill, A. V. (2005) Durable human memory T cells quantifiable by cultured enzyme-linked immunospot assays are induced by heterologous prime boost immunization and correlate with protection against malaria. J. Immunol. 175, 5675-5680.
79. Webster, D. P., Dunachie, S., Vuola, J. M., Berthoud, T., Keating, S., Laidlaw, S. M., McConkey, S. J., Poulton, I., Andrews, L., Andersen, R. F., Bejon, P., Butcher, G., Sinden, R., Skinner, M. A., Gilbert, S. C., Hill, A. V. (2005) Enhanced T cell-mediated protection against malaria in human challenges by using the recombinant poxviruses FP9 and modified vaccinia virus Ankara. Proc. Natl. Acad. Sci. USA 102, 4836-4841.
80. Good, M. F., Xu, H., Wykes, M., Engwerda, C. R. (2005) Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annu. Rev. Immunol. 23, 69-99.
81. Urban, B. C., Ing, R., Stevenson, M. M. (2005) Early interactions between blood-stage Plasmodium parasites and the immune system. Curr. Top. Microbiol. Immunol. 297, 25-70.
82. van der Heyde, H. C., Pepper, B., Batchelder, J., Cigel, F., Weidanz, W. P. (1997) The time course of selected malarial infections in cytokine-deficient mice. Exp. Parasitol. 85, 206-213.
83. Amani, V., Vigario, A. M., Belnoue, E., Marussig, M., Fonseca, L., Mazier, D., Renia, L. (2000) Involvement of IFN-γ receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur. J. Immunol. 30, 1646-1655.
84. Favre, N., Ryffel, B., Bordmann, G., Rudin, W. (1997) The course of Plasmodium chabaudi chabaudi infections in interferon-γ receptor deficient mice. Parasite Immunol. 19, 375-383.
85. Meding, S. J., Cheng, S. C., Simon-Haarhaus, B., Langhorne, J. (1990) Role of γ interferon during infection with Plasmodium chabaudi chabaudi. Infect. Immun. 58, 3671-3678.
86. Stevenson, M. M., Tam, M. F., Belosevic, M., van der Meide, P. H., Podoba, J. E. (1990) Role of endogenous γ interferon in host response to infection with blood-stage Plasmodium chabaudi AS. Infect. Immun. 58, 3225-3232.
87. Yoneto, T., Yoshimoto, T., Wang, C. R., Takahama, Y., Tsuji, M., Waki, S., Nariuchi, H. (1999) γ Interferon production is critical for protective immunity to infection with blood-stage Plasmodium berghei XAT but neither NO production nor NK cell activation is critical. Infect. Immun. 67, 2349-2356.
88. Edstein, M. D., Kotecka, B. M., Anderson, K. L., Pombo, D. J., Kyle, D. E., Rieckmann, K. H., Good, M. F. (2005) Lengthy antimalarial activity of atovaquone in human plasma following atovaquone-proguanil administration. Antimicrob. Agents Chemother. 49, 4421-4422.
89. Ramharter, M., Kremsner, P. G., Willheim, M., Winkler, H., Graninger, W., Winkler, S. (2004) Plasmodium falciparum-specific interleukin-2 and tumor necrosis factor-α expressing-T cells are associated with resistance to reinfection and severe malaria in healthy African children. Eur. Cytokine Netw. 15, 189-196.
90. Dodoo, D., Omer, F. M., Todd, J., Akanmori, B. D., Koram, K. A., Riley, E. M. (2002) Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to Plasmodium falciparum malaria. J. Infect. Dis. 185, 971-979.
91. D'Ombrain, M. C., Robinson, L. J., Stanisic, D. I., Taraika, J., Bernard, N., Michon, P., Mueller, I., Schofield, L. (2008) Association of early interferon-γ production with immunity to clinical malaria: a longitudinal study among Papua New Guinean children. Clin. Infect. Dis. 47, 1380-1387.
92. Robinson, L. J., D'Ombrain, M. C., Stanisic, D. I., Taraika, J., Bernard, N., Richards, J. S., Beeson, J. G., Tavul, L., Michon, P., Mueller, I., Schofield, L. (2009) Cellular tumor necrosis factor, γ interferon, and interleukin-6 responses as correlates of immunity and risk of clinical Plasmodium falciparum malaria in children from Papua New Guinea. Infect. Immun. 77, 3033-3043.
93. McCall, M. B., Hopman, J., Daou, M., Maiga, B., Dara, V., Ploemen, I., Nganou-Makamdop, K., Niangaly, A., Tolo, Y., Arama, C., Bousema, J. T., van der Meer, J. W., van der Ven, A. J., Troye-Blomberg, M., Dolo, A., Doumbo, O. K., Sauerwein, R. W. (2010) Early interferon-γ response against Plasmodium falciparum correlates with interethnic differences in susceptibility to parasitemia between sympatric Fulani and Dogon in Mali. J. Infect. Dis. 201, 142-152.
94. Riley, E. M., Allen, S. J., Troye-Blomberg, M., Bennett, S., Perlmann, H., Andersson, G., Smedman, L., Perlmann, P., Greenwood, B. M. (1991) Association between immune recognition of the malaria vaccine candidate antigen Pf155/RESA and resistance to clinical disease: a prospective study in a malaria-endemic region of West Africa. Trans. R. Soc. Trop. Med. Hyg. 85, 436-443.
95. Riley, E. M., Jakobsen, P. H., Allen, S. J., Wheeler, J. G., Bennett, S., Jepsen, S., Greenwood, B. M. (1991) Immune response to soluble exoantigens of Plasmodium falciparum may contribute to both pathogenesis and protection in clinical malaria: evidence from a longitudinal, prospective study of semi-immune African children. Eur. J. Immunol. 21, 1019-1025.
96. Al-Yaman, F., Genton, B., Taraika, J., Anders, R., Alpers, M. P. (1997) Association between cellular response (IL-4) to RESA/Pf155 and protection from clinical malaria among Papua New Guinean children living in a malaria endemic area. Parasite Immunol. 19, 249-254.
97. al-Yaman, F., Genton, B., Taraika, J., Anders, R., Alpers, M. P. (1997) Cellular immunity to merozoite surface protein 2 (FC27 and 3D7) in Papua New Guinean children. Temporal variation and relation to clinical and parasitological status. Parasite Immunol. 19, 207-214.
98. Luty, A. J., Lell, B., Schmidt-Ott, R., Lehman, L. G., Luckner, D., Greve, B., Matousek, P., Herbich, K., Schmid, D., Ulbert, S., Migot-Nabias, F., Dubois, B., Deloron, P., Kremsner, P. G. (1998) Parasite antigen-specific interleukin-10 and antibody reponses predict accelerated parasite clearance in Plasmodium falciparum malaria. Eur. Cytokine Netw. 9, 639-646.
99. Migot-Nabias, F., Luty, A. J., Ringwald, P., Vaillant, M., Dubois, B., Renaut, A., Mayombo, R. J., Minh, T. N., Fievet, N., Mbessi, J. R., Millet, P., Deloron, P. (1999) Immune responses against Plasmodium falciparum asexual blood-stage antigens and disease susceptibility in Gabonese and Cameroonian children. Am. J. Trop. Med. Hyg. 61, 488-494.
100. Riley, E. M., Allen, S. J., Wheeler, J. G., Blackman, M. J., Bennett, S., Takacs, B., Schonfeld, H. J., Holder, A. A., Greenwood, B. M. (1992) Naturally acquired cellular and humoral immune responses to the major merozoite surface antigen (PfMSP1) of Plasmodium falciparum are associated with reduced malaria morbidity. Parasite Immunol. 14, 321-337.
101. Shaffer, N., Grau, G. E., Hedberg, K., Davachi, F., Lyamba, B., Hightower, A. W., Breman, J. G., Phuc, N. D. (1991) Tumor necrosis factor and severe malaria. J. Infect. Dis. 163, 96-101.
102. Jakobsen, P. H., McKay, V., Morris-Jones, S. D., McGuire, W., van Hensbroek, M. B., Meisner, S., Bendtzen, K., Schousboe, I., Bygbjerg, I. C., Greenwood, B. M. (1994) Increased concentrations of interleukin-6 and interleukin-1 receptor antagonist and decreased concentrations of β-2-glycoprotein I in Gambian children with cerebral malaria. Infect. Immun. 62, 4374-4379.
103. McGuire, W., Hill, A. V., Allsopp, C. E., Greenwood, B. M., Kwiatkowski, D. (1994) Variation in the TNF-α promoter region associated with susceptibility to cerebral malaria. Nature 371, 508-510. (Pubitemid 24306606)
104. Wenisch, C., Linnau, K. F., Looaresuwan, S., Rumpold, H. (1999) Plasma levels of the interleukin-6 cytokine family in persons with severe Plasmodium falciparum malaria. J. Infect. Dis. 179, 747-750.
105. Lyke, K. E., Burges, R., Cissoko, Y., Sangare, L., Dao, M., Diarra, I., Kone, A., Harley, R., Plowe, C. V., Doumbo, O. K., Sztein, M. B. (2004) Serum levels of the proinflammatory cytokines interleukin-1 β (IL-1β), IL-6, IL-8, IL-10, tumor necrosis factor α, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect. Immun. 72, 5630-5637.
106. Grau, G. E., Heremans, H., Piguet, P. F., Pointaire, P., Lambert, P. H., Billiau, A., Vassalli, P. (1989) Monoclonal antibody against interferon γ can prevent experimental cerebral malaria and its associated overproduction of tumor necrosis factor. Proc. Natl. Acad. Sci. USA 86, 5572-5574.
107. De Kossodo, S., Grau, G. E. (1993) Profiles of cytokine production in relation with susceptibility to cerebral malaria. J. Immunol. 151, 4811-4820.
108. Yanez, D. M., Manning, D. D., Cooley, A. J., Weidanz, W. P., van der Heyde, H. C. (1996) Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J. Immunol. 157, 1620-1624.
109. Haque, A., Echchannaoui, H., Seguin, R., Schwartzman, J., Kasper, L. H., Haque, S. (2001) Cerebral malaria in mice: interleukin-2 treatment induces accumulation of γδ T cells in the brain and alters resistant mice to susceptible-like phenotype. Am. J. Pathol. 158, 163-172.
110. Curfs, J. H., van der Meide, P. H., Billiau, A., Meuwissen, J. H., Eling, W. M. (1993) Plasmodium berghei: recombinant interferon-γ and the development of parasitemia and cerebral lesions in malaria-infected mice. Exp. Parasitol. 77, 212-223.
111. Singh, R. P., Kashiwamura, S., Rao, P., Okamura, H., Mukherjee, A., Chauhan, V. S. (2002) The role of IL-18 in blood-stage immunity against murine malaria Plasmodium yoelii 265 and Plasmodium berghei ANKA. J. Immunol. 168, 4674-4681.
112. Bullen, D. V., Hansen, D. S., Siomos, M. A., Schofield, L., Alexander, W. S., Handman, E. (2003) The lack of suppressor of cytokine signaling-1 (SOCS1) protects mice from the development of cerebral malaria caused by Plasmodium berghei ANKA. Parasite Immunol. 25, 113-118.
113. Hanum, P. S., Hayano, M., Kojima, S. (2003) Cytokine and chemokine responses in a cerebral malaria-susceptible or -resistant strain of mice to Plasmodium berghei ANKA infection: early chemokine expression in the brain. Int. Immunol. 15, 633-640.
114. Kremsner, P. G., Neifer, S., Chaves, M. F., Rudolph, R., Bienzle, U. (1992) Interferon-γ induced lethality in the late phase of Plasmodium vinckei malaria despite effective parasite clearance by chloroquine. Eur. J. Immunol. 22, 2873-2878.
115. Yap, G. S., Stevenson, M. M. (1994) Inhibition of in vitro erythropoiesis by soluble mediators in Plasmodium chabaudi AS malaria: lack of a major role for interleukin 1, tumor necrosis factor α, and γ interferon. Infect. Immun. 62, 357-362.
116. Cross, C. E., Langhorne, J. (1998) Plasmodium chabaudi chabaudi (AS): inflammatory cytokines and pathology in an erythrocytic-stage infection in mice. Exp. Parasitol. 90, 220-229.
117. Harpaz, R., Edelman, R., Wasserman, S. S., Levine, M. M., Davis, J. R., Sztein, M. B. (1992) Serum cytokine profiles in experimental human malaria. Relationship to protection and disease course after challenge. J. Clin. Invest. 90, 515-523.
118. Ringwald, P., Peyron, F., Vuillez, J. P., Touze, J. E., Le Bras, J., Deloron, P. (1991) Levels of cytokines in plasma during Plasmodium falciparum malaria attacks. J. Clin. Microbiol. 29, 2076-2078.
119. Mshana, R. N., Boulandi, J., Mshana, N. M., Mayombo, J., Mendome, G. (1991) Cytokines in the pathogenesis of malaria: levels of IL-I β, IL-4, IL-6, TNF-α and IFN-γ in plasma of healthy individuals and malaria patients in a holoendemic area. J. Clin. Lab. Immunol. 34, 131-139.
120. Mordmuller, B. G., Metzger, W. G., Juillard, P., Brinkman, B. M., Verweij, C. L., Grau, G. E., Kremsner, P. G. (1997) Tumor necrosis factor in Plasmodium falciparum malaria: high plasma level is associated with fever, but high production capacity is associated with rapid fever clearance. Eur. Cytokine Netw. 8, 29-35.
121. Torre, D., Speranza, F., Giola, M., Matteelli, A., Tambini, R., Biondi, G. (2002) Role of Th1 and Th2 cytokines in immune response to uncomplicated Plasmodium falciparum malaria. Clin. Diagn. Lab. Immunol. 9, 348-351.
122. Ho, M., Sexton, M. M., Tongtawe, P., Looareesuwan, S., Suntharasamai, P., Webster, H. K. (1995) Interleukin-10 inhibits tumor necrosis factor production but not antigen-specific lymphoproliferation in acute Plasmodium falciparum malaria. J. Infect. Dis. 172, 838-844.
123. Al-Yaman, F. M., Genton, B., Clark, I. A. (1998) The ratio of reactive nitrogen intermediates to tumor necrosis factor and clinical outcome of falciparum malaria disease. Trans. R. Soc. Trop. Med. Hyg. 92, 417-420.
124. Nagamine, Y., Hayano, M., Kashiwamura, S., Okamura, H., Nakanishi, K., Krudsod, S., Wilairatana, P., Looareesuwan, S., Kojima, S. (2003) Involvement of interleukin-18 in severe Plasmodium falciparum malaria. Trans. R. Soc. Trop. Med. Hyg. 97, 236-241.
125. Wroczynska, A., Nahorski, W., Bakowska, A., Pietkiewicz, H. (2005) Cytokines and clinical manifestations of malaria in adults with severe and uncomplicated disease. Int. Marit. Health 56, 103-114.
126. Walther, M., Jeffries, D., Finney, O. C., Njie, M., Ebonyi, A., Deininger, S., Lawrence, E., Ngwa-Amambua, A., Jayasooriya, S., Cheeseman, I. H., Gomez-Escobar, N., Okebe, J., Conway, D. J., Riley, E. M. (2009) Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog. 5, e1000364.
127. Kern, P., Hemmer, C. J., Van, D. J., Gruss, H. J., Dietrich, M. (1989) Elevated tumor necrosis factor α and interleukin-6 serum levels as markers for complicated Plasmodium falciparum malaria. Am. J. Med. 87, 139-143.
128. Kwiatkowski, D., Hill, A. V., Sambou, I., Twumasi, P., Castracane, J., Manogue, K. R., Cerami, A., Brewster, D. R., Greenwood, B. M. (1990) TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336, 1201-1204.
129. Yamada-Tanaka, M. S., Ferreira-da-Cruz, M. F., Alecrim, M. G., Mascarenhas, L. A., Daniel-Ribeiro, C. T. (1995) Tumor necrosis factor α interferon γ and macrophage stimulating factor in relation to the severity of Plasmodium falciparum malaria in the Brazilian Amazon. Trop. Geogr. Med. 47, 282-285.
130. Prakash, D., Fesel, C., Jain, R., Cazenave, P. A., Mishra, G. C., Pied, S. (2006) Clusters of cytokines determine malaria severity in Plasmodium falciparum-infected patients from endemic areas of Central India. J. Infect. Dis. 194, 198-207.
131. Jakobsen, P. H., Morris-Jones, S., Theander, T. G., Hviid, L., Hansen, M. B., Bendtzen, K., Ridley, R. G., Greenwood, B. M. (1994) Increased plasma levels of soluble IL-2R are associated with severe Plasmodium falciparum malaria. Clin. Exp. Immunol. 96, 98-103.
132. Baptista, J. L., Vanham, G., Wery, M., Van, M. E. (1997) Cytokine levels during mild and cerebral falciparum malaria in children living in a mesoendemic area. Trop. Med. Int. Health 2, 673-679.
133. Luty, A. J., Perkins, D. J., Lell, B., Schmidt-Ott, R., Lehman, L. G., Luckner, D., Greve, B., Matousek, P., Herbich, K., Schmid, D., Weinberg, J. B., Kremsner, P. G. (2000) Low interleukin-12 activity in severe Plasmodium falciparum malaria. Infect. Immun. 68, 3909-3915.
134. Malaguarnera, L., Pignatelli, S., Musumeci, M., Simpore, J., Musumeci, S. (2002) Plasma levels of interleukin-18 and interleukin-12 in Plasmodium falciparum malaria. Parasite Immunol. 24, 489-492.
135. Chaisavaneeyakorn, S., Othoro, C., Shi, Y. P., Otieno, J., Chaiyaroj, S. C., Lal, A. A., Udhayakumar, V. (2003) Relationship between plasma interleukin-12 (IL-12) and IL-18 levels and severe malarial anemia in an area of holoendemicity in Western Kenya. Clin. Diagn. Lab. Immunol. 10, 362-366.
136. Chaiyaroj, S. C., Rutta, A. S., Muenthaisong, K., Watkins, P., Na, U. M., Looareesuwan, S. (2004) Reduced levels of transforming growth factor-β1, interleukin-12 and increased migration inhibitory factor are associated with severe malaria. Acta Trop. 89, 319-327. (Pubitemid 38117068)
137. Deloron, P., Dumont, N., Nyongabo, T., Aubry, P., Astagneau, P., Ndarugirire, F., Menetrier-Caux, C., Burdin, N., Brelivet, J. C., Peyron, F. (1994) Immunologic and biochemical alterations in severe falciparum malaria: relation to neurological symptoms and outcome. Clin. Infect. Dis. 19, 480-485.
138. Maneerat, Y., Pongponratn, E., Viriyavejakul, P., Punpoowong, B., Looareesuwan, S., Udomsangpetch, R. (1999) Cytokines associated with pathology in the brain tissue of fatal malaria. Southeast Asian J. Trop. Med. Public Health 30, 643-649.
139. Armah, H. B., Wilson, N. O., Sarfo, B. Y., Powell, M. D., Bond, V. C., Anderson, W., Adjei, A. A., Gyasi, R. K., Tettey, Y., Wiredu, E. K., Tongren, J. E., Udhayakumar, V., Stiles, J. K. (2007) Cerebrospinal fluid and serum biomarkers of cerebral malaria mortality in Ghanaian children. Malar. J. 6, 147.
140. Day, N. P., Hien, T. T., Schollaardt, T., Loc, P. P., Chuong, L. V., Chau, T. T., Mai, N. T., Phu, N. H., Sinh, D. X., White, N. J., Ho, M. (1999) The prognostic and pathophysiologic role of pro- and antiinflammatory cytokines in severe malaria. J. Infect. Dis. 180, 1288-1297.
141. Bream, J. H., Ping, A., Zhang, X., Winkler, C., Young, H. A. (2002) A single nucleotide polymorphism in the proximal IFN-γ promoter alters control of gene transcription. Genes Immun. 3, 165-169.
142. Chevillard, C., Henri, S., Stefani, F., Parzy, D., Dessein, A. (2002) Two new polymorphisms in the human interferon γ (IFN-γ) promoter. Eur. J. Immunogenet. 29, 53-56.
143. Cabantous, S., Poudiougou, B., Traore, A., Keita, M., Cisse, M. B., Doumbo, O., Dessein, A. J., Marquet, S. (2005) Evidence that interferon-γ plays a protective role during cerebral malaria. J. Infect. Dis. 192, 854-860.
144. Jason, J., Archibald, L. K., Nwanyanwu, O. C., Bell, M., Jensen, R. J., Gunter, E., Buchanan, I., Larned, J., Kazembe, P. N., Dobbie, H., Jarvis, W. R. (2001) The effects of iron deficiency on lymphocyte cytokine production and activation: preservation of hepatic iron but not at all cost. Clin. Exp. Immunol. 126, 466-473.
145. Perkmann, T., Winkler, H., Graninger, W., Kremsner, P. G., Winkler, S. (2005) Circulating levels of the interleukin (IL)-4 receptor and of IL-18 in patients with Plasmodium falciparum malaria. Cytokine 29, 153-158.
146. Othoro, C., Lal, A. A., Nahlen, B., Koech, D., Orago, A. S., Udhayakumar, V. (1999) A low interleukin-10 tumor necrosis factor-α ratio is associated with malaria anemia in children residing in a holoendemic malaria region in Western Kenya. J. Infect. Dis. 179, 279-282.
147. Ong'echa, J. M., Lal, A. A., Terlouw, D. J., Ter Kuile, F. O., Kariuki, S. K., Udhayakumar, V., Orago, A. S., Hightower, A. W., Nahlen, B. L., Shi, Y. P. (2003) Association of interferon-γ responses to pre-erythrocytic stage vaccine candidate antigens of Plasmodium falciparum in young Kenyan children with improved hemoglobin levels: XV. Asembo Bay Cohort Project. Am. J. Trop. Med. Hyg. 68, 590-597.
148. Fried, M., Muga, R. O., Misore, A. O., Duffy, P. E. (1998) Malaria elicits type 1 cytokines in the human placenta: IFN-γ and TNF-α associated with pregnancy outcomes. J. Immunol. 160, 2523-2530.
149. Kabyemela, E. R., Fried, M., Kurtis, J. D., Mutabingwa, T. K., Duffy, P. E. (2008) Fetal responses during placental malaria modify the risk of low birth weight. Infect. Immun. 76, 1527-1534.
150. Rogerson, S. J., Brown, H. C., Pollina, E., Abrams, E. T., Tadesse, E., Lema, V. M., Molyneux, M. E. (2003) Placental tumor necrosis factor α but not γ interferon is associated with placental malaria and low birth weight in Malawian women. Infect. Immun. 71, 267-270.
151. Suguitan Jr., A. L., Cadigan, T. J., Nguyen, T. A., Zhou, A., Leke, R. J., Metenou, S., Thuita, L., Megnekou, R., Fogako, J., Leke, R. G., Taylor, D. W. (2003) Malaria-associated cytokine changes in the placenta of women with pre-term deliveries in Yaounde, Cameroon. Am. J. Trop. Med. Hyg. 69, 574-581.
152. Bongfen, S. E., Torgler, R., Romero, J. F., Renia, L., Corradin, G. (2007) Plasmodium berghei-infected primary hepatocytes process and present the circumsporozoite protein to specific CD8+ T cells in vitro. J. Immunol. 178, 7054-7063.
153. Plebanski, M., Hannan, C. M., Behboudi, S., Flanagan, K. L., Apostolopoulos, V., Sinden, R. E., Hill, A. V. (2005) Direct processing and presentation of antigen from malaria sporozoites by professional antigen-presenting cells in the induction of CD8 T-cell responses. Immunol. Cell Biol. 83, 307-312.
154. Chakravarty, S., Cockburn, I. A., Kuk, S., Overstreet, M. G., Sacci, J. B., Zavala, F. (2007) CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat. Med. 13, 1035-1041.
155. Del Giudice, G., Grillot, D., Renia, L., Muller, I., Corradin, G., Louis, J. A., Mazier, D., Lambert, P. H. (1990) Peptide-primed CD4+ cells and malaria sporozoites. Immunol. Lett. 25, 59-63.
156. Tsuji, M., Romero, P., Nussenzweig, R. S., Zavala, F. (1990) CD4+ cytolytic T cell clone confers protection against murine malaria. J. Exp. Med. 172, 1353-1357.
157. Tsuji, M., Mombaerts, P., Lefrancois, L., Nussenzweig, R. S., Zavala, F., Tonegawa, S. (1994) γ δ T cells contribute to immunity against the liver stages of malaria in α β T-cell-deficient mice. Proc. Natl. Acad. Sci. USA 91, 345-349.
158. Pied, S., Roland, J., Louise, A., Voegtle, D., Soulard, V., Mazier, D., Cazenave, P. A. (2000) Liver CD4-CD8- NK1.1+ TCR α β intermediate cells increase during experimental malaria infection and are able to exhibit inhibitory activity against the parasite liver stage in vitro. J. Immunol. 164, 1463-1469.
159. Ojo-Amaize, E. A., Vilcek, J., Cochrane, A. H., Nussenzweig, R. S. (1984) Plasmodium berghei sporozoites are mitogenic for murine T cells, induce interferon, and activate natural killer cells. J. Immunol. 133, 1005-1009.
160. Roland, J., Soulard, V., Sellier, C., Drapier, A. M., Di Santo, J. P., Cazenave, P. A., Pied, S. (2006) NK cell responses to Plasmodium infection and control of intrahepatic parasite development. J. Immunol. 177, 1229-1239.
161. Lundie, R. J., de Koning-Ward, T. F., Davey, G. M., Nie, C. Q., Hansen, D. S., Lau, L. S., Mintern, J. D., Belz, G. T., Schofield, L., Carbone, F. R., Villadangos, J. A., Crabb, B. S., Heath, W. R. (2008) Blood-stage Plasmodium infection induces CD8+ T lymphocytes to parasite-expressed antigens, largely regulated by CD8α+ dendritic cells. Proc. Natl. Acad. Sci. USA 105, 14509-14514.
162. Miyakoda, M., Kimura, D., Yuda, M., Chinzei, Y., Shibata, Y., Honma, K., Yui, K. (2008) Malaria-specific and nonspecific activation of CD8+ T cells during blood stage of Plasmodium berghei infection. J. Immunol. 181, 1420-1428.
163. Sinigaglia, F., Richard, J., Pink, L. (1985) Human T lymphocyte clones specific for malaria (Plasmodium falciparum) antigens. EMBO J. 4, 3819-3822.
164. Behr, C., Dubois, P. (1992) Preferential expansion of V γ 9 V δ 2 T cells following stimulation of peripheral blood lymphocytes with extracts of Plasmodium falciparum. Int. Immunol. 4, 361-366.
165. Goodier, M., Fey, P., Eichmann, K., Langhorne, J. (1992) Human peripheral blood γ δ T cells respond to antigens of Plasmodium falciparum. Int. Immunol. 4, 33-41.
166. Jones, S. M., Goodier, M. R., Langhorne, J. (1996) The response of γ δ T cells to Plasmodium falciparum is dependent on activated CD4+ T cells and the recognition of MHC class. Immunology 89, 405-412.
167. Goodier, M. R., Lundqvist, C., Hammarstrom, M. L., Troye-Blomberg, M., Langhorne, J. (1995) Cytokine profiles for human V γ 9+ T cells stimulated by Plasmodium falciparum. Parasite Immunol. 17, 413-423.
168. Hensmann, M., Kwiatkowski, D. (2001) Cellular basis of early cytokine response to Plasmodium falciparum. Infect. Immun. 69, 2364-2371.
169. D'Ombrain, M. C., Hansen, D. S., Simpson, K. M., Schofield, L. (2007) γδ-T cells expressing NK receptors predominate over NK cells and conventional T cells in the innate IFN-γ response to Plasmodium falciparum malaria. Eur. J. Immunol. 37, 1864-1873.
170. Rzepczyk, C. M., Stamatiou, S., Anderson, K., Stowers, A., Cheng, Q., Saul, A., Allworth, A., McCormack, J., Whitby, M., Olive, C., Lawrence, G. (1996) Experimental human Plasmodium falciparum infections: longitudinal analysis of lymphocyte responses with particular reference to γ δ T cells. Scand. J. Immunol. 43, 219-227.
171. Waterfall, M., Black, A., Riley, E. (1998) γδ+ T cells preferentially respond to live rather than killed malaria parasites. Infect. Immun. 66, 2393-2398.
172. Behr, C., Poupot, R., Peyrat, M. A., Poquet, Y., Constant, P., Dubois, P., Bonneville, M., Fournie, J. J. (1996) Plasmodium falciparum stimuli for human γδT cells are related to phosphorylated antigens of mycobacteria. Infect. Immun. 64, 2892-2896.
173. Pichyangkul, S., Saengkrai, P., Yongvanitchit, K., Stewart, A., Heppner, D. G. (1997) Activation of γδ T cells in malaria: interaction of cytokines and a schizont-associated Plasmodium falciparum antigen. J. Infect. Dis. 176, 233-241.
174. Dieli, F., Troye-Blomberg, M., Farouk, S. E., Sireci, G., Salerno, A. (2001) Biology of γδ T cells in tuberculosis and malaria. Curr. Mol. Med. 1, 437-446.
175. Vivier, E., Tomasello, E., Baratin, M., Walzer, T., Ugolini, S. (2008) Functions of natural killer cells. Nat. Immunol. 9, 503-510.
176. Artavanis-Tsakonas, K., Riley, E. M. (2002) Innate immune response to malaria: rapid induction of IFN-γ from human NK cells by live Plasmodium falciparum-infected erythrocytes. J. Immunol. 169, 2956-2963.
177. Baratin, M., Roetynck, S., Lepolard, C., Falk, C., Sawadogo, S., Uematsu, S., Akira, S., Ryffel, B., Tiraby, J. G., Alexopoulou, L., Kirschning, C. J., Gysin, J., Vivier, E., Ugolini, S. (2005) Natural killer cell and macrophage cooperation in MyD88-dependent innate responses to Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 102, 14747-14752.
178. Newman, K. C., Korbel, D. S., Hafalla, J. C., Riley, E. M. (2006) Crosstalk with myeloid accessory cells regulates human natural killer cell interferon-γ responses to malaria. PLoS Pathog. 2, e118.
179. Artavanis-Tsakonas, K., Eleme, K., McQueen, K. L., Cheng, N. W., Parham, P., Davis, D. M., Riley, E. M. (2003) Activation of a subset of human NK cells upon contact with Plasmodium falciparum-infected erythrocytes. J. Immunol. 171, 5396-5405.
180. Korbel, D. S., Newman, K. C., Almeida, C. R., Davis, D. M., Riley, E. M. (2005) Heterogeneous human NK cell responses to Plasmodium falciparum-infected erythrocytes. J. Immunol. 175, 7466-7473. (Pubitemid 41713444)
181. Korbel, D. S., Norman, P. J., Newman, K. C., Horowitz, A., Gendzekhadze, K., Parham, P., Riley, E. M. (2009) Killer Ig-like receptor (KIR) genotype predicts the capacity of human KIR-positive CD56dim NK cells to respond to pathogen-associated signals. J. Immunol. 182, 6426-6434.
182. Mavoungou, E., Held, J., Mewono, L., Kremsner, P. G. (2007) A Duffy binding-like domain is involved in the NKp30-mediated recognition of Plasmodium falciparum-parasitized erythrocytes by natural killer cells. J. Infect. Dis. 195, 1521-1531.
183. Coban, C., Igari, Y., Yagi, M., Reimer, T., Koyama, S., Aoshi, T., Ohata, K., Tsukui, T., Takeshita, F., Sakurai, K., Ikegami, T., Nakagawa, A., Horii, T., Nunez, G., Ishii, K. J., Akira, S. (2010) Immunogenicity of whole-parasite vaccines against Plasmodium falciparum involves malarial hemozoin and host TLR9. Cell Host Microbe 7, 50-61.
184. Parroche, P., Lauw, F. N., Goutagny, N., Latz, E., Monks, B. G., Visintin, A., Halmen, K. A., Lamphier, M., Olivier, M., Bartholomeu, D. C., Gazzinelli, R. T., Golenbock, D. T. (2007) Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc. Natl. Acad. Sci. USA 104, 1919-1924.
185. Currier, J., Sattabongkot, J., Good, M. F. (1992) "Natural" T cells responsive to malaria: evidence implicating immunological cross-reactivity in the maintenance of TCR α β+ malaria-specific responses from non-exposed donors. Int. Immunol. 4, 985-994.
186. Hermsen, C. C., Konijnenberg, Y., Mulder, L., Loé, C., van Deuren, M., van der Meer, J. W., van Mierlo, G. J., Eling, W. M., Hack, C. E., Sauerwein, R. W. (2003) Circulating concentrations of soluble granzyme A and B increase during natural and experimental Plasmodium falciparum infections. Clin. Exp. Immunol. 132, 467-472.
187. Zevering, Y., Amante, F., Smillie, A., Currier, J., Smith, G., Houghten, R. A., Good, M. F. (1992) High frequency of malaria-specific T cells in non-exposed humans. Eur. J. Immunol. 22, 689-696.
188. Dick, S., Waterfall, M., Currie, J., Maddy, A., Riley, E. (1996) Naive human α β T cells respond to membrane-associated components of malaria-infected erythrocytes by proliferation and production of interferon-γ. Immunology 88, 412-420.
189. Scragg, I. G., Hensmann, M., Bate, C. A., Kwiatkowski, D. (1999) Early cytokine induction by Plasmodium falciparum is not a classical endotoxin-like process. Eur. J. Immunol. 29, 2636-2644.
190. Ndungu, F. M., Sanni, L., Urban, B., Stephens, R., Newbold, C. I., Marsh, K., Langhorne, J. (2006) CD4 T cells from malaria-nonexposed individuals respond to the CD36-binding domain of Plasmodium falciparum erythrocyte membrane protein-1 via an MHC class II-TCR-independent pathway. J. Immunol. 176, 5504-5512.
191. Good, M. F. (1994) Immunological responses from non-exposed donors to malaria antigens: implications for immunity and pathology. Immunol. Lett. 41, 123-125.
192. Wyler, D. J., Oppenheim, J. J. (1974) Lymphocyte transformation in human Plasmodium falciparum malaria. J. Immunol. 113, 449-454.
193. Troye-Blomberg, M., Andersson, G., Stoczkowska, M., Shabo, R., Romero, P., Patarroyo, M. E., Wigzell, H., Perlmann, P. (1985) Production of IL 2 and IFN-γ by T cells from malaria patients in response to Plasmodium falciparum or erythrocyte antigens in vitro. J. Immunol. 135, 3498-3504.
194. Chizzolini, C., Grau, G. E., Geinoz, A., Schrijvers, D. (1990) T lymphocyte interferon-γ production induced by Plasmodium falciparum antigen is high in recently infected non-immune and low in immune subjects. Clin. Exp. Immunol. 79, 95-99.
195. Ramharter, M., Willheim, M., Winkler, H., Wahl, K., Lagler, H., Graninger, W., Winkler, S. (2003) Cytokine profile of Plasmodium falciparum-specific T cells in non-immune malaria patients. Parasite Immunol. 25, 211-219.
196. Dorfman, J. R., Bejon, P., Ndungu, F. M., Langhorne, J., Kortok, M. M., Lowe, B. S., Mwangi, T. W., Williams, T. N., Marsh, K. (2005) B cell memory to 3 Plasmodium falciparum blood-stage antigens in a malaria-endemic area. J. Infect. Dis. 191, 1623-1630.
197. Kinyanjui, S. M., Conway, D. J., Lanar, D. E., Marsh, K. (2007) IgG antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half-life. Malar. J. 6, 82.
198. Akpogheneta, O. J., Duah, N. O., Tetteh, K. K., Dunyo, S., Lanar, D. E., Pinder, M., Conway, D. J. (2008) Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infect. Immun. 76, 1748-1755.
199. Achtman, A. H., Bull, P. C., Stephens, R., Langhorne, J. (2005) Longevity of the immune response and memory to blood-stage malaria infection. Curr. Top. Microbiol. Immunol. 297, 71-102.
200. Migot, F., Chougnet, C., Raharimalala, L., Astagneau, P., Lepers, J. P., Deloron, P. (1993) Human immune responses to the Plasmodium falciparum ring-infected erythrocyte surface antigen (Pf155/RESA) after a decrease in malaria transmission in Madagascar. Am. J. Trop. Med. Hyg. 48, 432-439.
201. Zevering, Y., Khamboonruang, C., Rungruengthanakit, K., Tungviboonchai, L., Ruengpipattanapan, J., Bathurst, I., Barr, P., Good, M. F. (1994) Life-spans of human T-cell responses to determinants from the circumsporozoite proteins of Plasmodium falciparum and Plasmodium vivax. Proc. Natl. Acad. Sci. USA 91, 6118-6122.
202. Rhee, M. S., Akanmori, B. D., Waterfall, M., Riley, E. M. (2001) Changes in cytokine production associated with acquired immunity to Plasmodium falciparum malaria. Clin. Exp. Immunol. 126, 503-510.
203. Chizzolini, C., Geinoz, A., Schrijvers, D. (1990) Interleukin-2 reverses T cell unresponsiveness to Plasmodium falciparum-antigen in malaria immune subjects. Cell. Immunol. 128, 1-10.
204. Torcia, M. G., Santarlasci, V., Cosmi, L., Clemente, A., Maggi, L., Mangano, V. D., Verra, F., Bancone, G., Nebie, I., Sirima, B. S., Liotta, F., Frosali, F., Angeli, R., Severini, C., Sannella, A. R., Bonini, P., Lucibello, M., Maggi, E., Garaci, E., Coluzzi, M., Cozzolino, F., Annunziato, F., Romagnani, S., Modiano, D. (2008) Functional deficit of T regulatory cells in Fulani, an ethnic group with low susceptibility to Plasmodium falciparum malaria. Proc. Natl. Acad. Sci. USA 105, 646-651.
205. Finney, O. C., Nwakanma, D., Conway, D. J., Walther, M., Riley, E. M. (2009) Homeostatic regulation of T effector to Treg ratios in an area of seasonal malaria transmission. Eur. J. Immunol. 39, 1288-1300.
206. Finney, O. C., Riley, E. M., Walther, M. (2010) Regulatory T cells in malaria - friend or foe? Trends Immunol. 31, 63-70.
207. Casares, S., Richie, T. L. (2009) Immune evasion by malaria parasites: a challenge for vaccine development. Curr. Opin. Immunol. 21, 321-330.
208. Troye-Blomberg, M., Perlmann, H., Patarroyo, M. E., Perlmann, P. (1983) Regulation of the immune response in Plasmodium falciparum malaria. II. Antigen specific proliferative responses in vitro. Clin. Exp. Immunol. 53, 345-353.
209. Theander, T. G., Bygbjerg, I. C., Andersen, B. J., Jepsen, S., Kharazmi, A., Odum, N. (1986) Suppression of parasite-specific response in Plasmodium falciparum malaria. A longitudinal study of blood mononuclear cell proliferation and subset composition. Scand. J. Immunol. 24, 73-81.
210. Riley, E. M., Andersson, G., Otoo, L. N., Jepsen, S., Greenwood, B. M. (1988) Cellular immune responses to Plasmodium falciparum antigens in Gambian children during and after an acute attack of falciparum malaria. Clin. Exp. Immunol. 73, 17-22.
211. Luty, A. J., Bongartz, M., Rezbach, P., Faucher, J. F., Hollingdale, M. R., Kremsner, P. G. (2001) Plasmodium falciparum liver-stage antigen-1 peptide-specific interferon-γ responses are not suppressed during uncomplicated malaria in African children. Eur. Cytokine Netw. 12, 647-653.
212. Otoo, L. N., Riley, E. M., Menon, A., Byass, P., Greenwood, B. M. (1989) Cellular immune responses to Plasmodium falciparum antigens in children receiving long term anti-malarial chemoprophylaxis. Trans. R. Soc. Trop. Med. Hyg. 83, 778-782.
213. O'Leary, J. G., Goodarzi, M., Drayton, D. L., von Andrian, U. H. (2006) T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat. Immunol. 7, 507-516.
214. Long, B. R., Michaelsson, J., Loo, C. P., Ballan, W. M., Vu, B. A., Hecht, F. M., Lanier, L. L., Chapman, J. M., Nixon, D. F. (2008) Elevated frequency of γ interferon-producing NK cells in healthy adults vaccinated against influenza virus. Clin. Vaccine Immunol. 15, 120-130.
215. Graves, P., Gelband, H. (2006) Vaccines for preventing malaria (blood-stage). Cochrane Database Syst. Rev. CD006199.
216. Graves, P., Gelband, H. (2006) Vaccines for preventing malaria (pre-erythrocytic). Cochrane Database Syst. Rev. CD006198.
217. Graves, P., Gelband, H. (2006) Vaccines for preventing malaria (SPf66). Cochrane Database Syst. Rev. CD005966.
218. Remarque, E. J., Faber, B. W., Kocken, C. H., Thomas, A. W. (2008) Apical membrane antigen 1: a malaria vaccine candidate in review. Trends Parasitol. 24, 74-84.
219. Doolan, D. L., Dobano, C., Baird, J. K. (2009) Acquired immunity to malaria. Clin. Microbiol. Rev. 22, 13-36 (Table.).
220. Zola, H. (1997) The development of antibody responses in the infant. Immunol. Cell Biol. 75, 587-590.
221. Lewinsohn, D. A., Gennaro, M. L., Scholvinck, L., Lewinsohn, D. M. (2004) Tuberculosis immunology in children: diagnostic and therapeutic challenges and opportunities. Int. J. Tuberc. Lung Dis. 8, 658-674.
222. Baird, J. K. (1998) Age-dependent characteristics of protection v. susceptibility to Plasmodium falciparum. Ann. Trop. Med. Parasitol. 92, 367-390.
223. Zuckerman, A., Yoeli, M. (1954) Age and sex as factors influencing Plasmodium berghei infections in intact and splenectomized rats. J. Infect. Dis. 94, 225-236.
224. Smalley, M. E. (1975) The nature of age immunity to Plasmodium berghei in the rat. Parasitology 71, 337-347.
225. Adam, E., Pierrot, C., Lafitte, S., Godin, C., Saoudi, A., Capron, M., Khalife, J. (2003) The age-related resistance of rats to Plasmodium berghei infection is associated with differential cellular and humoral immune responses. Int. J. Parasitol. 33, 1067-1078.
226. Winkler, S., Willheim, M., Baier, K., Graninger, W., Kremsner, P. G. (1999) Frequency of cytokine-producing CD4-CD8- peripheral blood mononuclear cells in patients with Plasmodium falciparum malaria. Eur. Cytokine Netw. 10, 155-160.
227. Bucci, K., Kastens, W., Hollingdale, M. R., Shankar, A., Alpers, M. P., King, C. L., Kazura, J. W. (2000) Influence of age and HLA type on interferon-γ (IFN-γ) responses to a naturally occurring polymorphic epitope of Plasmodium falciparum liver stage antigen-1 (LSA-1). Clin. Exp. Immunol. 122, 94-100.
228. Ramharter, M., Winkler, H., Kremsner, P. G., Adegnika, A. A., Willheim, M., Winkler, S. (2005) Age-dependency of Plasmodium falciparum-specific and non-specific T cell cytokine responses in individuals from a malaria-endemic area. Eur. Cytokine Netw. 16, 135-143.
229. Baird, J. K., Jones, T. R., Danudirgo, E. W., Annis, B. A., Bangs, M. J., Basri, H., Purnomo, Masbar, S. (1991) Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria. Am. J. Trop. Med. Hyg. 45, 65-76.
230. Bousema, J. T., Roeffen, W., van der Kolk, M., de Vlas, S. J., van de Vegte-Bolmer, M., Bangs, M. J., Teelen, K., Kurniawan, L., Maguire, J. D., Baird, J. K., Sauerwein, R. W. (2006) Rapid onset of transmission-reducing antibodies in Javanese migrants exposed to malaria in Papua, Indonesia. Am. J. Trop. Med. Hyg. 74, 425-431.
231. Murhandarwati, E. E., Black, C. G., Wang, L., Weisman, S., Koning-Ward, T. F., Baird, J. K., Tjitra, E., Richie, T. L., Crabb, B. S., Coppel, R. L. (2008) Acquisition of invasion-inhibitory antibodies specific for the 19-kDa fragment of merozoite surface protein 1 in a transmigrant population requires multiple infections. J. Infect. Dis. 198, 1212-1218.
232. Deloron, P., Chougnet, C. (1992) Is immunity to malaria really shortlived? Parasitol. Today 8, 375-378