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Chapter 18 : Innate Immunity to Parasitic Infections

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Innate Immunity to Parasitic Infections, Page 1 of 2

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Abstract:

The highly divergent lifestyles and patterns of adaptive immune responses associated with control of helminth and protozoan parasites are reflected in the distinct innate responses they trigger and in their consequences for the pathogen. In the case of protozoa, innate immunity has an important role in limiting early parasite replication until cognitive T- and B-lymphocyte responses can dominate. Alternatively, the innate recognition of helminths may function to limit the number of invading larvae and perhaps slow their development prior to the onset of adaptive immunity. Consequently, in order to be successful, parasites have to survive the innate response and this hard-wired system provides a powerful selective pressure on host and microorganism. This is evident from the numerous strategies employed by protozoa and helminths to evade these antimicrobial mechanisms and underscores the importance of studying innate immunity in order to understand the host/parasite adaptation. Perhaps the simplest forms of innate immunity are represented by the presence of preexisting, soluble factors that can recognize and destroy invading parasites. In addition to complement, there are other soluble factors that mediate innate immunity to parasitic infections. Natural killer (NK) cells can produce IL-5, this may represent a mechanism whereby NK cells can influence the development of effector mechanisms required for resistance to worms. Although innate immunity has an important role in resistance to acute infections, it is the adaptive response, characterized by the selective expansion of T and B cells, that is required to provide long-term immunological control of many chronic parasitic infections.

Citation: Hunter C, Sher A. 2011. Innate Immunity to Parasitic Infections, p 225-236. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch18

Key Concept Ranking

Innate Immune System
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Adaptive Immune System
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Parasitic Diseases
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MHC Class II
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Complement System
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0.47297648
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References

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1. Afonso, L. C. C.,, T. M. Scharton,, L. Q. Vieira,, M. Wysocka,, G. Trinchieri, and, P. Scott. 1994. The adjuvant effect of interleukin-12 in a vaccine against Leishmania major. Science 263:235237.
2. Andrade, L. O., and, N. W. Andrews. 2004. Lysosomal fusion is essential for the retention of Trypanosoma cruzi inside host cells. J. Exp. Med. 200:11351143.
3. Andrews, N. W.,, C. K. Abrams,, S. L. Slatin, and, G. Griffiths. 1990. A T. cruzi-secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH. Cell 61:12771287.
4. Artavanis-Tsakonas, K.,, K. Eleme,, K. L. McQueen,, N. W. Cheng,, P. Parham,, D. M. Davis, and, E. M. Riley. 2003. Activation of a subset of human NK cells upon contact with Plasmodium falciparummfected erythrocytes. J. Immunol. 171:53965405.
5. Artavanis-Tsakonas, K., and, E. M. Riley. 2002. Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J. Immunol. 169:29562963.
6. Babu, S.,, C. P. Blauvelt,, V. Kumaraswami, and, T. B. Nutman. 2005. Diminished expression and function of TLR in lymphatic filariasis: a novel mechanism of immune dysregulation. J. Immunol. 175:11701176.
7. Babu, S.,, P. Porte,, T. R. Klei,, L. D. Shultz, and, T. V. Rajan. 1998. Host NK cells are required for the growth of the human filarial parasite Brugia malayi in mice. J. Immunol. 161:14281432.
8. Bafica, A.,, H. C. Santiago,, R. Goldszmid,, C. Ropert,, R. T. Gazzinelli, and, A. Sher. 2006. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J. Immunol. 177:35153519.
9. Benson, A.,, R. Pifer,, C. L. Behrendt,, L. V. Hooper, and, F. Yarovinsky. 2009. Gut commensal bacteria direct a protective immune response against Toxoplasma gondii. Cell Host Microbe 6:187196.
10. Braga, L. L.,, H. Ninomiya,, J. J. McCoy,, S. Eacker,, T. Wiedmer,, C. Pham,, S. Wood,, P. J. Sims, and, W. A. Petri, Jr. 1992. Inhibition of the complement membrane attack complex by the galactose-specific adhesion of Entamoeba histolytica. J. Clin. Invest. 90:11311137.
11. Brannstrom, K.,, M. E. Sellin,, P. Holmfeldt,, M. Brattsand, and, M. Gullberg. 2009. The Schistosoma mansoni protein Sm16/SmSLP/SmSPO-1 assembles into a nine-subunit oligomer with potential to inhibit Toll-like receptor signaling. Infect. Immun. 77:11441154.
12. Brittingham, A.,, C. J. Morrison,, W. R. McMaster,, B. S. McGwire,, K. P. Chang, and, D. M. Mosser. 1995. Role of the Leishmania surface protease gp63 in complement fixation, cell adhesion, and resistance to complement-mediated lysis. J. Immunol. 155:31023111.
13. Campino, S.,, J. Forton,, S. Auburn,, A. Fry,, M. Diakite,, A. Richardson,, J. Hull,, M. Jallow,, F. Sisay-Joof,, M. Pinder,, M. E. Molyneux,, T. E. Taylor,, K. Rockett,, T. G. Clark, and, D. P. Kwiatkowski. 2009. TLR9 polymorphisms in African populations: no association with severe malaria, but evidence of cis-variants acting on gene expression. Malar. J. 8:44.
14. Campos, M. A.,, I. C. Almeida,, O. Takeuchi,, S. Akira,, E. P. Valente,, D. O. Procopio,, L. R. Travassos,, J. A. Smith,, D. T. Golenbock, and, R. T. Gazzinelli. 2001. Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J. Immunol. 167:416423.
15. Capin, R.,, N. R. Capin,, M. Carmona, and, L. Ortiz-Ortiz. 1980. Effect of complement depletion on the induction of amebic liver abscess in the hamster. Arch. Invest. Med. (Mex.) 11:173180.
16. Carter, T.,, M. Sumiya,, K. Reilly,, R. Ahmed,, P. Sobieszczuk,, J. A. Summerfield, and, R. A. Lawrence. 2007. Mannose-binding lectin A-deficient mice have abrogated antigen-specific IgM responses and increased susceptibility to a nematode infection. J. Immunol. 178:51165123.
17. Catto, B. A.,, F. A. Lewis, and, E. A. Ottesen. 1980. Cercaria-induced histamine release: a factor in the pathogenesis of schistosome dermatitis? Am. J. Trop. Med. Hyg. 29:886889.
18. Chessler, A. D.,, L. R. Ferreira,, T. H. Chang,, K. A. Fitzgerald, and, B. A. Burleigh. 2008. A novel IFN regulatory factor 3-dependent pathway activated by trypanosomes triggers IFN-beta in macrophages and fibroblasts. J. Immunol. 181:79177924.
19. Cliffe, L. J.,, N. E. Humphreys,, T. E. Lane,, C. S. Potten,, C. Booth, and, R. K. Grencis. 2005. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308:14631465.
20. Coban, C.,, K. J. Ishii,, T. Kawai,, H. Hemmi,, S. Sato,, S. Uematsu,, M. Yamamoto,, O. Takeuchi,, S. Itagaki,, N. Kumar,, T. Horii, and, S. Akira. 2005. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J. Exp. Med. 201:1925.
21. Couper, K. N.,, D. G. Blount, and, E. M. Riley. 2008. IL-10: the master regulator of immunity to infection. J. Immunol. 180:57715777.
22. de Veer, M. J.,, J. M. Curtis,, T. M., Baldwin, J. A. DiDonato, A. Sexton, M. J. McConville, E. Handman, and, L. Schofield. 2003. MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signaling. Eur.J. Immunol. 33:28222831.
23. Diaz, A.,, A. Ferreira, and, R. B. Sim. 1997. Complement evasion by Echinococcus granulosus: sequestration of host factor H in the hydatid cyst wall. J. Immunol. 158:37793786.
24. Dostert, C.,, G. Guarda,, J. F. Romero,, P. Menu,, O. Gross,, A. Tardivel,, M. L. Suva,, J. C. Stehle,, M. Kopf,, I. Stamenkovic,, G. Corradin, and, J. Tschopp. 2009. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS ONE 4:e6510.
25. Ferrante, A., and, A. C. Allison. 1983. Alternative pathway activation of complement by African trypanosomes lacking a glycoprotein coat. Parasite Immunol. 5:491498.
26. Finkelman, F. D.,, T. Shea-Donohue, S. C. Morris,, L. Gildea,, R. Strait,, K. B. Madden,, L. Schopf, and, J. F. Urban, Jr. 2004. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 201:139155.
27. Fishelson, Z. 1995. Novel mechanisms of immune evasion by Schistosoma mansoni. Mem. Inst. Oswaldo Cruz 90:289292.
28. Garcia-Hernandez, P.,, M. Rodero, and, C. Cuellar. 2009. Study of the effect of Anisakis simplex larval products on the early and late components in the classical complement pathway. J. Parasitol. 95:240241.
29. Gazzinelli, R. T., and, E. Y. Denkers. 2006. Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nat. Rev. Immunol. 6:895906.
30. Giacomin, P. R.,, D. L. Gordon,, M. Botto,, M. R. Daha,, S. D. Sanderson,, S. M. Taylor, and, L. A. Dent. 2008. The role of complement in innate, adaptive and eosinophil-dependent immunity to the nematode Nippostrongylus brasiliensis. Mol. Immunol. 45:446455.
31. Gomez-Garcia, L.,, L. M. Lopez-Marin,, R. Saavedra,, J. L. Reyes,, M. Rodriguez-Sosa, and, L. I. Terrazas. 2005. Intact glycans from cestode antigens are involved in innate activation of myeloid suppressor cells. Parasite Immunol. 27:395405.
32. Goodridge, H. S.,, S. McGuiness,, K. M. Houston,, C. A. Egan,, L. Al-Riyami,, M. J. Alcocer,, M. M. Harnett, and, W. Harnett. 2007. Phosphorylcholine mimics the effects of ES-62 on macrophages and dendritic cells. Parasite Immunol. 29:127137.
33. Gutierrez-Kobeh, L.,, N. Cabrera, and, R. Perez-Montfort. 1997. A mechanism of acquired resistance to complement-mediated lysis by Entamoeba histolytica. J. Parasitol. 83:234241.
34. Hager, K. M., and, S. L. Hajduk. 1997. Mechanism of resistance of African trypanosomes to cytotoxic human HDL. Nature 385:823826.
35. Himmelrich, H.,, C. Parra-Lopez,, F. Tacchini-Cottier, J. A. Louis, and, P. Launois. 1998. The IL-4 rapidly produced in BALB/c mice after infection with Leishmania major downregulates IL-12 receptor beta 2-chain expression on CD4+ T cells resulting in a state of unresponsiveness to IL-12. J. Immunol. 161:61566163.
36. Hise, A. G.,, K. Daehnel,, I. Gillette-Ferguson,, E. Cho,, H. F. McGarry,, M. J. Taylor,, D. T. Golenbock,, K. A. Fitzgerald,, J. W. Kazura, and, E. Pearlman. 2007. Innate immune responses to endosymbiotic Wolbachia bacteria in Brugia malayi and Onchocerca volvulus are dependent on TLR2, TLR6, MyD88, and Mal, but not TLR4, TRIF, or TRAM. J. Immunol. 178:10681076.
37. Hunter, C. A.,, L. Bermudez,, H. Beernink,, W. Waegell, and, J. S. Remington. 1995. Transforming growth factor-β inhibits interleukin-12-induced production of interferon-γ by natural killer cells: A role for transforming growth factor-β in the regulation of T-cell independent resistance to Toxoplasma gondii. Eur. J. Immunol. 25:9941000.
38. Hunter, C. A.,, L. Ellis-Neyer, K. Gabriel,, M. Kennedy,, P. Linsley, and, J. S. Remington. 1997. The role of the CD28/B7 interaction in the regulation of NK cell responses during infection with Toxoplasma gondii. J. Immunol. 158:22852293.
39. Ilg, T. 2000. Lipophosphoglycan is not required for infection of macrophages or mice by Leishmania mexicana. EMBO J. 19:19531962.
40. Imrie, H.,, D. J. Ferguson,, M. Carter,, J. Drain,, A. Schiflett,, S. L. Hajduk, and, K. P. Day. 2004. Light and electron microscopical observations of the effects of high-density lipoprotein on growth of Plasmodium falciparum in vitro. Parasitology 128:577584.
41. Joiner, K. A.,, S. A. Fuhrman,, H. M. Miettinen,, L. H. Kasper, and, I. Mellman. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249:641646.
42. Kane, C. M.,, L. Cervi,, J. Sun,, A. S. McKee,, K. S. Masek,, S. Shapira,, C. A. Hunter, and, E. J. Pearce. 2004. Helminth antigens modulate TLR-initiated dendritic cell activation. J. Immunol. 173:74547461.
43. Kane, C. M.,, E. Jung, and, E. J. Pearce. 2008. Schistosoma mansoni egg antigen-mediated modulation of Toll-like receptor (TLR)-induced activation occurs independently of TLR2, TLR4, and MyD88. Infect. Immun. 76:57545759.
44. Kayama, H.,, R. Koga,, K. Atarashi,, M. Okuyama,, T. Kimura,, T. W. Mak,, S. Uematsu,, S. Akira,, H. Takayanagi,, K. Honda,, M. Yamamoto, and, K. Takeda. 2009. NFATc1 mediates Toll-like receptor-independent innate immune responses during Trypanosoma cruzi infection. PLoS Pathog. 5:e1000514.
45. Kaye, P. M.,, N. J. Rogers,, A. J. Curry, and, J. C. Scott. 1994. Deficient expression of co-stimulatory molecules on Leishmania-infected macrophages. Eur. J. Immunol. 24:28502854.
46. Kelly, P.,, D. L. Jack,, A. Naeem,, B. Mandanda,, R. C. Pollok,, N. J. Klein,, M. W. Turner, and, M. J. Farthing. 2000. Mannose-binding lectin is a component of innate mucosal defense against Cryptosporidium parvum in AIDS. Gastroenterology 119:12361242.
47. Kerepesi, L. A.,, J. A. Hess,, T. J. Nolan,, G. A. Schad, and, D. Abraham. 2006. Complement component C3 is required for protective innate and adaptive immunity to larval Strongyloides stercoralis in mice. J. Immunol. 176:43154322.
48. Koga, R.,, S. Hamano,, H. Kuwata,, K. Atarashi,, M. Ogawa,, H. Hisaeda,, M. Yamamoto,, S. Akira,, K. Himeno,, M. Matsumoto, and, K. Takeda. 2006. TLR-dependent induction of IFN-beta mediates host defense against Trypanosoma cruzi. J. Immunol. 177:70597066.
49. Korbel, D. S.,, O. C. Finney, and, E. M. Riley. 2004. Natural killer cells and innate immunity to protozoan pathogens. Int. J. Parasitol. 34:15171528.
50. Koyama, K., and, Y. Ito. 2000. Mucosal mast cell responses are not required for protection against infection with the murine nematode parasite Trichuris muris. Parasite Immunol. 22:1320.
51. Lambert, H., and, A. Barragan. 2009. Modelling parasite dissemination: host cell subversion and immune evasion by Toxoplasma gondii. Cell Microbiol. 12:292300.
52. Lambert, H.,, N. Hitziger,, I., Dellacasa,, M. Svensson, and, A. Barragan. 2006. Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell. Microbiol. 8:16111623.
53. Laouar, Y.,, F. S. Sutterwala,, L. Gorelik, and, R. A. Flavell. 2005. Transforming growth factor-beta controls T helper type 1 cell development through regulation of natural killer cell interferon-gamma. Nat. Immunol. 6:600607.
54. Laskay, T.,, G. van Zandbergen, and, W. Solbach. 2008. Neutrophil granulocytes as host cells and transport vehicles for intracellular pathogens: apoptosis as infection-promoting factor. Immunobiology 213:183191.
55. Layland, L. E.,, R. Rad,, H. Wagner, and, C. U. da Costa. 2007. Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur. J. Immunol. 37:21742184.
56. Liu, C. H.,, Y. T. Fan,, A. Dias,, L. Esper,, R. A. Corn,, A. Bafica,, F. S. Machado, and, J. Aliberti. 2006. Cutting edge: dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice. J. Immunol. 177:3135.
57. Lodge, R., and, A. Descoteaux. 2005. Modulation of phagolysosome biogenesis by the lipophosphoglycan of Leishmania. Clin. Immunol. 114:256265.
58. MacDonald, A. S., and, E. J. Pearce. 2002. Cutting edge: polarized Th cell response induction by transferred antigen-pulsed dendritic cells is dependent on IL-4 or IL-12 production by recipient cells. J. Immunol. 168:31273130.
59. Maroof, A.,, L. Beattie,, S. Zubairi,, M. Svensson,, S. Stager, and, P. M. Kaye. 2008. Posttranscriptional regulation of il10 gene expression allows natural killer cells to express immunoregulatory function. Immunity 29:295305.
60. Marshall, F. A., and, E. J. Pearce. 2008. Uncoupling of induced protein processing from maturation in dendritic cells exposed to a highly antigenic preparation from a helminth parasite. J. Immunol. 181:75627570.
61. McConville, J.,, S. T. Turco,, M. A. J. Ferguson, and, D. L. Sacks. 1992. Developmental modification of lipophosphoglycan during the differentiation of Leishmania major promastigotes to an infectious stage. EMBO J. 11:35933600.
62. McDermott, J. R.,, R. E. Bartram,, P. A. Knight,, H. R. Miller,, D. R. Garrod, and, R. K. Grencis. 2003. Mast cells disrupt epithelial barrier function during enteric nematode infection. Proc. Natl. Acad. Sci. USA. 100:77617766.
63. McDermott, J. R.,, N. E. Humphreys,, S. P. Forman,, D. D. Donaldson, and, R. K. Grencis. 2005. Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection. J. Immunol. 175:32073213.
64. McKenzie, A. N. 2000. Regulation of T helper type 2 cell immunity by interleukin-4 and interleukin-13. Pharmacol. Ther. 88:143151.
65. Molina-Portela, M. P.,, M. Samanovic, and, J. Raper. 2008. Distinct roles of apolipoprotein components within the trypanosome lytic factor complex revealed in a novel transgenic mouse model. J. Exp. Med. 205:17211728.
66. Norris, K. A. 1998. Stable transfection of Trypanosoma cruzi epimastigotes with the trypomastigote-specific complement regulatory protein cDNA confers complement resistance. Infect. Immun. 66:24602465.
67. Norris, K. A., and, J. E. Schrimpf. 1994. Biochemical analysis of the membrane and soluble forms of the complement regulatory protein of Trypanosoma cruzi. Infect. Immun. 62:236243.
68. Olivier, M.,, D. J. Gregory, and, G. Forget. 2005. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin. Microbiol. Rev. 18:293305.
69. Padigel, U. M.,, J. A. Hess,, J. J. Lee,, J. B. Lok,, T. J. Nolan,, G. A. Schad, and, D. Abraham. 2007. Eosinophils act as antigen-presenting cells to induce immunity to Strongyloides stercoralis in mice. J. Infect. Dis. 196:18441851.
70. Padilla, A. M.,, L. J. Simpson, and, R. L. Tarleton. 2009. Insufficient TLR activation contributes to the slow development of CD8+ T cell responses in Trypanosoma cruzi infection. J. Immunol. 183:12451252.
71. Parroche, P.,, F. N. Lauw,, N. Goutagny,, E. Latz,, B. G. Monks,, A. Visintin,, K. A. Halmen,, M. Lamphier,, M. Olivier,, D. C. Bartholomeu,, R. T. Gazzinelli, and, D. T. Golenbock. 2007. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc. Natl. Acad. Sci. U.S.A. 104:19191924.
72. Passos, S. T.,, J. S. Silver,, A. O’Hara, D. Sehy, J. S. Stumhofer, and, C. A. Hunter. 2010. IL-6 promotes NK cell production of IL-17 during toxoplasmosis. J. Immunol. 184:17761783.
73. Pepper, M.,, F. Dzierszinski,, E. Wilson,, E. Tait,, Q. Fang,, F. Yarovinsky,, T. M. Laufer,, D. Roos, and, C. A. Hunter. 2008. Plasmacytoid dendritic cells are activated by Toxoplasma gondii to present antigen and produce cytokines. J. Immunol. 180:62296236.
74. Perez-Morga, D.,, B. Vanhollebeke,, F. Paturiaux-Hanocq, D. P. Nolan,, L. Lins,, F. Homble,, L. Vanhamme,, P. Tebabi,, A. Pays,, P. Poelvoorde,, A. Jacquet,, R. Brasseur, and, E. Pays. 2005. Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 309;469472.
75. Perrigoue, J. G.,, S. A. Saenz,, M. C. Siracusa,, E. J. Allenspach,, B. C. Taylor,, P. R. Giacomin,, M. G. Nair,, Y. Du,, C. Zaph,, N. van Rooijen,, M. R. Comeau,, E. J. Pearce,, T. M. Laufer, and, D. Artis. 2009. MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokine-dependent immunity. Nat. Immunol. 10:697705.
76. Peters, N. C.,, J. G. Egen,, N. Secundino,, A. Debrabant,, N. Kimblin,, S. Kamhawi,, P. Lawyer,, M. P. Fay,, R. N. Germain, and, D. Sacks. 2008. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321:970974.
77. Plattner, F.,, F. Yarovinsky,, S. Romero,, D. Didry,, M. F. Carlier,, A. Sher, and, D. Soldati-Favre. 2008. Toxoplasma profilin is essential for host cell invasion and TLR11-dependent induction of an interleukin-12 response. Cell Host Microbe 3:7787.
78. Ramasawmy, R.,, E. Cunha-Neto,, K. C. Fae,, S. C. Borba,, P. C. Teixeira,, S. C. Ferreira,, A. C. Goldberg,, B. Ianni,, C. Mady, and, J. Kalil. 2009. Heterozygosity for the S180L variant of MAL/TIRAP, a gene expressing an adaptor protein in the Toll-like receptor pathway, is associated with lower risk of developing chronic Chagas’cardiomyopathy. J. Infect. Dis. 199:18381845.
79. Raper, J.,, R. Fung,, J. Ghiso,, V. Nussenzweig, and, S. Tomlinson. 1999. Characterization of a novel trypanosome lytic factor from human serum. Infect. Immun. 67:19101916.
80. Reed, S. L.,, W. E. Keene,, J. H. McKerrow, and, I. Gigli. 1989. Cleavage of C3 by a neutral cysteine proteinase of Entamoeba histolytica. J. Immunol. 143:189195.
81. Reise Sousa, C.,, 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. 186:18191829.
82. Samanovic, M.,, M. P. Molina-Portela,, A. D. Chessler,, B. A. Burleigh, and, J. Raper. 2009. Trypanosome lytic factor, an antimicrobial high-density lipoprotein, ameliorates Leishmania infection. PLoS Pathog. 5:e1000276.
83. Scharton-Kersten, T.,, L. C. C. Afonso,, M. Wysocka,, G. Trinchieri, and, P. Scott. 1995. IL-12 is required for natural killer cell activation and subsequent T helper 1 cell development in experimental leishmaniasis. J. Immunol. 154:53205330.
84. Schleicher, U.,, J. Liese,, I. Knippertz,, C. Kurzmann,, A. Hesse,, A. Heit,, J. A. Fischer,, S. Weiss,, U. Kalinke,, S. Kunz, and, C. Bogdan. 2007. NK cell activation in visceral leishmaniasis requires TLR9, myeloid DCs, and IL-12, but is independent of plasmacytoid DCs. J. Exp. Med. 204:893906.
85. Scott, P., and, C. A. Hunter. 2002. Dendritic cells and immunity to leishmaniasis and toxoplasmosis. Curr. Opin. Immunol. 14:466470.
86. Scott, P., and, G. Trinchieri. 1995. The role of natural killer cells in host-parasite interactions. Curr. Opin. Immunol. 7:3440.
87. Sharma, S. D., J. Verhoef, and, J. S. Remington. 1984. Enhancement of human natural killer cell activity by subcellular components of Toxoplasma gondii. Cell. Immunol. 86:317326.
88. Shoda, L. K.,, K. A. Kegerreis,, C. E. Suarez,, I. Roditi,, R. S. Corral,, G. M. Bertot,, J. Norimine, and, W. C. Brown. 2001. DNA from protozoan parasites Babesia bovis, Trypanosoma cruzi, and T. brucei is mitogenic for B lymphocytes and stimulates macrophage expression of interleukin-12, tumor necrosis factor alpha, and nitric oxide. Infect. Immun. 69:21622171.
89. Sibley, L. D.,, W. Qiu,, S. Fentress,, S. J. Taylor,, A. Khan, and, R. Hui. 2009. Forward genetics in Toxoplasma gondii reveals a family of rhoptry kinases that mediates pathogenesis. Eukaryot. Cell 8:10851093.
90. Smith, A. B.,, J. D. Esko, and, S. L. Hajduk. 1995. Killing of trypanosomes by the human haptoglobin-related protein. Science 268:284286.
91. Spath, G. F.,, L. Epstein,, B. Leader,, S. M. Singer,, H. A. Avila,, S. J. Turco, and, S. M. Beverley. 2000. Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proc. Natl. Acad. Sci. USA 97:92589263.
92. Steinfelder, S.,, J. F. Andersen,, J. L. Cannons,, C. G. Feng,, M. Joshi,, D. Dwyer,, P. Caspar,, P. L. Schwartzberg,, A. Sher, and, D. Jankovic. 2009. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J. Exp. Med. 206:16811690.
93. Stumhofer, J. S., and, C. A. Hunter. 2008. Advances in understanding the anti-inflammatory properties of IL-27. Immunol. Lett. 117:123130.
94. Summerfield, J. A.,, S. Ryder,, M., Sumiya,, M. Thursz,, A. Gorchein,, M. A. Monteil, and, M. W. Turner. 1995. Mannose binding protein gene mutations associated with unusual and severe infections in adults. Lancet 345:886889.
95. Svetic, A.,, K. B. Madden,, X. D. Zhou,, P. Lu,, I. M. Katona,, F. D. Finkelman,, J. F. Urban, Jr., and, W. C. Gause. 1993. A primary intestinal helminthic infection rapidly induces a gut-associated elevation of Th2-associated cytokines and IL-3. J. Immunol. 150:34343441.
96. Tait, E. D.,, K. A. Jordan,, T. H. Harris,, B. Gregg,, C. D. Dupont,, E. H. Wilson,, M. Pepper,, F. Dzierszinski,, D. S. Roos, and, C. A. Hunter. 2010. Virulence of Toxoplasma gondii is associated with distinct dendritic cell responses and reduced numbers of activated CD8+ T cells. J. Immunol., 185:15021512.
97. Takamoto, M.,, K. S. Ovington,, C. A., Behm,, K. Sugane,, I. G. Young, and, K. I. Matthaei. 1997. Eosinophilia, parasite burden and lung damage in Toxocara canis infection in C57BL/6 mice genetically deficient in IL-5. Immunology 90:511517.
98. Taylor, G. A.,, C. G. Feng, and, A. Sher. 2007. Control of IFN-gamma-mediated host resistance to intracellular pathogens by immunity-related GTPases (p47 GTPases). Microbes Infect. 9:16441651.
99. Tiemi Shio, M.,, S. C. Eisenbarth,, M. Savaria,, A. F. Vinet,, M. J. Bellemare,, K. W. Harder,, F. S. Sutterwala,, D. S. Bohle,, A. Descoteaux,, R. A. Flavell, and, M. Olivier. 2009. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog. 5:e1000559.
100. Turner, J. D.,, R. S. Langley,, K. L. Johnston,, G. Egerton,, S. Wanji, and, M. J. Taylor. 2006. Wolbachia endosymbiotic bacteria of Brugia malayi mediate macrophage tolerance to TLR- and CD40-specific stimuli in a MyD88/TLR2-dependent manner. J. Immunol. 177:12401249.
101. van der Kleij, D.,, E. Latz,, J. F. Brouwers,, Y. C. Kruize,, M. Schmitz,, E. A. Kurt-Jones,, T. Espevik,, E. C. de Jong,, M. L. Kapsenberg,, D. T. Golenbock,, A. G. Tielens, and, M. Yazdanbakhsh. 2002. A novel host-parasite lipid crosstalk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277:4812248129.
102. Vannier-Santos, M. A.,, A. Martiny, and, W. de Souza. 2002. Cell biology of Leishmania spp.: invading and evading. Curr. Pharm. Des. 8:297318.
103. Vargas-Inchaustegui, D. A.,, W. Tai,, L. Xin,, A. E. Hogg,, D. B. Corry, and, L. Soong. 2009. Distinct roles for MyD88 and Toll-like receptor 2 during Leishmania braziliensis infection in mice. Infect. Immun. 77:29482956.
104. Wynn, T. A.,, A. W. Cheever,, D. Jankovic,, R. W. Poindexter,, P., Caspar,, F. A. Lewis, and, A. Sher. 1995. An IL-12 based vaccination method for preventing fibrosis induced by schistosome infection. Nature 376:594596.
105. Xong, H. V.,, L. Vanhamme,, M. Chamekh,, C. E. Chimfwembe,, J. Van Den Abbeele,, A. Pays,, N. Van Meirvenne,, R. Hamers,, P. De Baetselier, and, E. Pays. 1998. A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 95:839846.
106. Zaph, C.,, A. E. Troy,, B. C. Taylor,, L. D. Berman-Booty,, K. J. Guild,, Y. Du,, E. A. Yost,, A. D. Gruber,, M. J. May,, F. R. Greten,, L. Eckmann,, M. Karin, and, D. Artis. 2007. Epithelial-cell-intrinsic IKK-beta expression regulates intestinal immune homeostasis. Nature 446:552556.
107. Zhao, Y.,, D. J. Ferguson,, D. C. Wilson,, J. C. Howard,, L. D. Sibley, and, G. S. Yap. 2009a. Virulent Toxoplasma gondii evade immunity-related GTPase-mediated parasite vacuole disruption within primed macrophages. J. Immunol. 182:37753781.
108. Zhao, Y. O.,, A. Khaminets,, J. P. Hunn, and, J. C. Howard. 2009b. Disruption of the Toxoplasma gondii parasitophorous vacuole by IFN-gamma-inducible immunity-related GTPases (IRG proteins) triggers necrotic cell death. PLoS Pathog. 5:e1000288.

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