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Published in: Immunologic Research 1-3/2014

01-08-2014 | IMMUNOLOGY AT THE UNIVERSITY OF IOWA

NLR proteins and parasitic disease

Authors: Gwendolyn M. Clay, Fayyaz S. Sutterwala, Mary E. Wilson

Published in: Immunologic Research | Issue 1-3/2014

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Abstract

Parasitic diseases are a serious global health concern. Many of the most common and most severe parasitic diseases, including Chagas’ disease, leishmaniasis, and schistosomiasis, are also classified as neglected tropical diseases and are comparatively less studied than infectious diseases prevalent in high income nations. The NLRs (nucleotide-binding domain leucine-rich-repeat-containing proteins) are cytosolic proteins known to be involved in pathogen detection and host response. The role of NLRs in the host response to parasitic infection is just beginning to be understood. The NLR proteins NOD1 and NOD2 have been shown to contribute to immune responses during Trypanosoma cruzi infection, Toxoplasma gondii infection, and murine cerebral malaria. The NLRP3 inflammasome is activated by T. cruzi and Leishmania amazonensis but also induces pathology during infection with schistosomes or malaria. Both the NLRP1 and NLRP3 inflammasomes respond to T. gondii infection. The NLRs may play crucial roles in human immune responses during parasitic infection, usually acting as innate immune sensors and driving the inflammatory response against invading parasites. However, this inflammatory response can either kill the invading parasite or be responsible for destructive pathology. Therefore, understanding the role of the NLR proteins will be critical to understanding the host defense against parasites as well as the fine balance between homeostasis and parasitic disease.
Literature
5.
go back to reference Wlodarska M, et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell. 2014;156(5):1045–59.PubMedCentralCrossRefPubMed Wlodarska M, et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell. 2014;156(5):1045–59.PubMedCentralCrossRefPubMed
6.
7.
go back to reference Joly S, et al. Cutting edge: Nlrp10 is essential for protective antifungal adaptive immunity against Candida albicans. J Immunol. 2012;189(10):4713–7.PubMedCentralCrossRefPubMed Joly S, et al. Cutting edge: Nlrp10 is essential for protective antifungal adaptive immunity against Candida albicans. J Immunol. 2012;189(10):4713–7.PubMedCentralCrossRefPubMed
8.
go back to reference Allen IC, et al. NLRP12 suppresses colon inflammation and tumorigenesis through the negative regulation of noncanonical NF-κB signaling. Immunity. 2012;36(5):742–54.PubMedCentralCrossRefPubMed Allen IC, et al. NLRP12 suppresses colon inflammation and tumorigenesis through the negative regulation of noncanonical NF-κB signaling. Immunity. 2012;36(5):742–54.PubMedCentralCrossRefPubMed
9.
go back to reference Arthur JC, et al. Cutting edge: NLRP12 controls dendritic and myeloid cell migration to affect contact hypersensitivity. J Immunol. 2010;185(8):4515–9.PubMedCentralCrossRefPubMed Arthur JC, et al. Cutting edge: NLRP12 controls dendritic and myeloid cell migration to affect contact hypersensitivity. J Immunol. 2010;185(8):4515–9.PubMedCentralCrossRefPubMed
11.
go back to reference Zhang L, et al. NLRC3, a member of the NLR family of proteins, is a negative regulator of innate immune signaling induced by the DNA sensor STING. Immunity. 2014;40(3):329–41.PubMedCentralCrossRefPubMed Zhang L, et al. NLRC3, a member of the NLR family of proteins, is a negative regulator of innate immune signaling induced by the DNA sensor STING. Immunity. 2014;40(3):329–41.PubMedCentralCrossRefPubMed
13.
go back to reference Faustin B, et al. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell. 2007;25(5):713–24.CrossRefPubMed Faustin B, et al. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell. 2007;25(5):713–24.CrossRefPubMed
14.
go back to reference Hsu LC, et al. A NOD2-NALP1 complex mediates caspase-1-dependent IL-1β secretion in response to Bacillus anthracis infection and muramyl dipeptide. Proc Natl Acad Sci USA. 2008;105(22):7803–8.PubMedCentralCrossRefPubMed Hsu LC, et al. A NOD2-NALP1 complex mediates caspase-1-dependent IL-1β secretion in response to Bacillus anthracis infection and muramyl dipeptide. Proc Natl Acad Sci USA. 2008;105(22):7803–8.PubMedCentralCrossRefPubMed
15.
go back to reference Terra JK, et al. Cutting edge: resistance to Bacillus anthracis infection mediated by a lethal toxin sensitive allele of Nalp1b/Nlrp1b. J Immunol. 2010;184(1):17–20.PubMedCentralCrossRefPubMed Terra JK, et al. Cutting edge: resistance to Bacillus anthracis infection mediated by a lethal toxin sensitive allele of Nalp1b/Nlrp1b. J Immunol. 2010;184(1):17–20.PubMedCentralCrossRefPubMed
16.
go back to reference Yang J, et al. Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc Natl Acad Sci USA. 2013;110(35):14408–13.PubMedCentralCrossRefPubMed Yang J, et al. Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc Natl Acad Sci USA. 2013;110(35):14408–13.PubMedCentralCrossRefPubMed
17.
go back to reference Zhao Y, et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature. 2011;477(7366):596–600.CrossRefPubMed Zhao Y, et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature. 2011;477(7366):596–600.CrossRefPubMed
18.
19.
go back to reference Miao YC, Liu CJ. ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proc Natl Acad Sci USA. 2010;107(52):22728–33.PubMedCentralCrossRefPubMed Miao YC, Liu CJ. ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proc Natl Acad Sci USA. 2010;107(52):22728–33.PubMedCentralCrossRefPubMed
20.
go back to reference Tenthorey JL, et al. Molecular basis for specific recognition of bacterial ligands by NAIP/NLRC4 inflammasomes. Mol Cell. 2014;54(1):17–29. Tenthorey JL, et al. Molecular basis for specific recognition of bacterial ligands by NAIP/NLRC4 inflammasomes. Mol Cell. 2014;54(1):17–29.
21.
go back to reference Rayamajhi M, et al. Cutting edge: mouse NAIP1 detects the type III secretion system needle protein. J Immunol. 2013;191(8):3986–9.CrossRefPubMed Rayamajhi M, et al. Cutting edge: mouse NAIP1 detects the type III secretion system needle protein. J Immunol. 2013;191(8):3986–9.CrossRefPubMed
22.
go back to reference Qu Y, et al. Phosphorylation of NLRC4 is critical for inflammasome activation. Nature. 2012;490(7421):539–42.CrossRefPubMed Qu Y, et al. Phosphorylation of NLRC4 is critical for inflammasome activation. Nature. 2012;490(7421):539–42.CrossRefPubMed
24.
25.
go back to reference Roberts TL, et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science. 2009;323(5917):1057–60.CrossRefPubMed Roberts TL, et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science. 2009;323(5917):1057–60.CrossRefPubMed
26.
go back to reference Kalantari P, et al. Dual engagement of the NLRP3 and AIM2 inflammasomes by Plasmodium-derived hemozoin and DNA during malaria. Cell Rep. 2014;6(1):196–210.PubMedCentralCrossRefPubMed Kalantari P, et al. Dual engagement of the NLRP3 and AIM2 inflammasomes by Plasmodium-derived hemozoin and DNA during malaria. Cell Rep. 2014;6(1):196–210.PubMedCentralCrossRefPubMed
27.
go back to reference Jones JW, et al. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc Natl Acad Sci USA. 2010;107(21):9771–6.PubMedCentralCrossRefPubMed Jones JW, et al. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc Natl Acad Sci USA. 2010;107(21):9771–6.PubMedCentralCrossRefPubMed
30.
go back to reference Wen H, Miao EA, Ting JP. Mechanisms of NOD-like receptor-associated inflammasome activation. Immunity. 2013;39(3):432–41.CrossRefPubMed Wen H, Miao EA, Ting JP. Mechanisms of NOD-like receptor-associated inflammasome activation. Immunity. 2013;39(3):432–41.CrossRefPubMed
31.
go back to reference Horng T. Calcium signaling and mitochondrial destabilization in the triggering of the NLRP3 inflammasome. Trends Immunol. 2014;35(6):253–61. Horng T. Calcium signaling and mitochondrial destabilization in the triggering of the NLRP3 inflammasome. Trends Immunol. 2014;35(6):253–61.
32.
go back to reference Fitzgerald KA. NLR-containing inflammasomes: central mediators of host defense and inflammation. Eur J Immunol. 2010;40(3):595–8.CrossRefPubMed Fitzgerald KA. NLR-containing inflammasomes: central mediators of host defense and inflammation. Eur J Immunol. 2010;40(3):595–8.CrossRefPubMed
33.
go back to reference Philpott DJ, et al. NOD proteins: regulators of inflammation in health and disease. Nat Rev Immunol. 2014;14(1):9–23.CrossRefPubMed Philpott DJ, et al. NOD proteins: regulators of inflammation in health and disease. Nat Rev Immunol. 2014;14(1):9–23.CrossRefPubMed
34.
go back to reference Rubino SJ, et al. Nod-like receptors in the control of intestinal inflammation. Curr Opin Immunol. 2012;24(4):398–404.CrossRefPubMed Rubino SJ, et al. Nod-like receptors in the control of intestinal inflammation. Curr Opin Immunol. 2012;24(4):398–404.CrossRefPubMed
36.
go back to reference Silva GK, et al. Cutting edge: nucleotide-binding oligomerization domain 1-dependent responses account for murine resistance against Trypanosoma cruzi infection. J Immunol. 2010;184(3):1148–52.CrossRefPubMed Silva GK, et al. Cutting edge: nucleotide-binding oligomerization domain 1-dependent responses account for murine resistance against Trypanosoma cruzi infection. J Immunol. 2010;184(3):1148–52.CrossRefPubMed
38.
go back to reference Benko S, et al. NLRC5 limits the activation of inflammatory pathways. J Immunol. 2010;185(3):1681–91.CrossRefPubMed Benko S, et al. NLRC5 limits the activation of inflammatory pathways. J Immunol. 2010;185(3):1681–91.CrossRefPubMed
39.
go back to reference Hotez PJ, et al. The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination. PLoS Negl Trop Dis. 2008;2(9):e300.PubMedCentralCrossRefPubMed Hotez PJ, et al. The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination. PLoS Negl Trop Dis. 2008;2(9):e300.PubMedCentralCrossRefPubMed
41.
go back to reference Teixeira MM, Gazzinelli RT, Silva JS. Chemokines, inflammation and Trypanosoma cruzi infection. Trends Parasitol. 2002;18(6):262–5.CrossRefPubMed Teixeira MM, Gazzinelli RT, Silva JS. Chemokines, inflammation and Trypanosoma cruzi infection. Trends Parasitol. 2002;18(6):262–5.CrossRefPubMed
42.
go back to reference Bafica A, et al. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J Immunol. 2006;177(6):3515–9.CrossRefPubMed Bafica A, et al. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J Immunol. 2006;177(6):3515–9.CrossRefPubMed
43.
go back to reference Oliveira AC, et al. Expression of functional TLR4 confers proinflammatory responsiveness to Trypanosoma cruzi glycoinositolphospholipids and higher resistance to infection with T. cruzi. J Immunol. 2004;173(9):5688–96.CrossRefPubMed Oliveira AC, et al. Expression of functional TLR4 confers proinflammatory responsiveness to Trypanosoma cruzi glycoinositolphospholipids and higher resistance to infection with T. cruzi. J Immunol. 2004;173(9):5688–96.CrossRefPubMed
44.
go back to reference Caetano BC, et al. Requirement of UNC93B1 reveals a critical role for TLR7 in host resistance to primary infection with Trypanosoma cruzi. J Immunol. 2011;187(4):1903–11.PubMedCentralCrossRefPubMed Caetano BC, et al. Requirement of UNC93B1 reveals a critical role for TLR7 in host resistance to primary infection with Trypanosoma cruzi. J Immunol. 2011;187(4):1903–11.PubMedCentralCrossRefPubMed
45.
go back to reference Campos MA, et al. Impaired production of proinflammatory cytokines and host resistance to acute infection with Trypanosoma cruzi in mice lacking functional myeloid differentiation factor 88. J Immunol. 2004;172(3):1711–8.CrossRefPubMed Campos MA, et al. Impaired production of proinflammatory cytokines and host resistance to acute infection with Trypanosoma cruzi in mice lacking functional myeloid differentiation factor 88. J Immunol. 2004;172(3):1711–8.CrossRefPubMed
46.
go back to reference Goncalves VM, et al. NLRP3 controls Trypanosoma cruzi infection through a caspase-1-dependent IL-1R-independent NO production. PLoS Negl Trop Dis. 2013;7(10):e2469.PubMedCentralCrossRefPubMed Goncalves VM, et al. NLRP3 controls Trypanosoma cruzi infection through a caspase-1-dependent IL-1R-independent NO production. PLoS Negl Trop Dis. 2013;7(10):e2469.PubMedCentralCrossRefPubMed
47.
go back to reference Silva GK, et al. Apoptosis-associated speck-like protein containing a caspase recruitment domain inflammasomes mediate IL-1β response and host resistance to Trypanosoma cruzi infection. J Immunol. 2013;191(6):3373–83.CrossRefPubMed Silva GK, et al. Apoptosis-associated speck-like protein containing a caspase recruitment domain inflammasomes mediate IL-1β response and host resistance to Trypanosoma cruzi infection. J Immunol. 2013;191(6):3373–83.CrossRefPubMed
48.
go back to reference Julia V, Rassoulzadegan M, Glaichenhaus N. Resistance to Leishmania major induced by tolerance to a single antigen. Science. 1996;274(5286):421–3.CrossRefPubMed Julia V, Rassoulzadegan M, Glaichenhaus N. Resistance to Leishmania major induced by tolerance to a single antigen. Science. 1996;274(5286):421–3.CrossRefPubMed
51.
go back to reference Blackwell JM, et al. Macrophage complement and lectin-like receptors bind Leishmania in the absence of serum. J Exp Med. 1985;162(1):324–31.CrossRefPubMed Blackwell JM, et al. Macrophage complement and lectin-like receptors bind Leishmania in the absence of serum. J Exp Med. 1985;162(1):324–31.CrossRefPubMed
52.
go back to reference Da Silva RP, et al. CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J Immunol. 1989;143(2):617–22.PubMed Da Silva RP, et al. CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J Immunol. 1989;143(2):617–22.PubMed
53.
go back to reference Wilson ME, Pearson RD. Roles of CR3 and mannose receptors in the attachment and ingestion of Leishmania donovani by human mononuclear phagocytes. Infect Immun. 1988;56(2):363–9.PubMedCentralPubMed Wilson ME, Pearson RD. Roles of CR3 and mannose receptors in the attachment and ingestion of Leishmania donovani by human mononuclear phagocytes. Infect Immun. 1988;56(2):363–9.PubMedCentralPubMed
54.
go back to reference Mosser DM, Springer TA, Diamond MS. Leishmania promastigotes require opsonic complement to bind to the human leukocyte integrin Mac-1 (CD11b/CD18). J Cell Biol. 1992;116(2):511–20.CrossRefPubMed Mosser DM, Springer TA, Diamond MS. Leishmania promastigotes require opsonic complement to bind to the human leukocyte integrin Mac-1 (CD11b/CD18). J Cell Biol. 1992;116(2):511–20.CrossRefPubMed
55.
go back to reference Wilson ME, Jeronimo SM, Pearson RD. Immunopathogenesis of infection with the visceralizing Leishmania species. Microb Pathog. 2005;38(4):147–60.CrossRefPubMed Wilson ME, Jeronimo SM, Pearson RD. Immunopathogenesis of infection with the visceralizing Leishmania species. Microb Pathog. 2005;38(4):147–60.CrossRefPubMed
56.
go back to reference Olivier M, Gregory DJ, Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev. 2005;18(2):293–305.PubMedCentralCrossRefPubMed Olivier M, Gregory DJ, Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev. 2005;18(2):293–305.PubMedCentralCrossRefPubMed
57.
go back to reference Kaye P, Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol. 2011;9(8):604–15.CrossRefPubMed Kaye P, Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol. 2011;9(8):604–15.CrossRefPubMed
58.
go back to reference Monteforte GM, et al. Genetically resistant mice lacking IL-18 gene develop Th1 response and control cutaneous Leishmania major infection. J Immunol. 2000;164(11):5890–3.CrossRefPubMed Monteforte GM, et al. Genetically resistant mice lacking IL-18 gene develop Th1 response and control cutaneous Leishmania major infection. J Immunol. 2000;164(11):5890–3.CrossRefPubMed
59.
go back to reference Ohkusu K, et al. Potentiality of interleukin-18 as a useful reagent for treatment and prevention of Leishmania major infection. Infect Immun. 2000;68(5):2449–56.PubMedCentralCrossRefPubMed Ohkusu K, et al. Potentiality of interleukin-18 as a useful reagent for treatment and prevention of Leishmania major infection. Infect Immun. 2000;68(5):2449–56.PubMedCentralCrossRefPubMed
60.
go back to reference Xin L, Li Y, Soong L. Role of interleukin-1β in activating the CD11c(high) CD45RB-dendritic cell subset and priming Leishmania amazonensis-specific CD4+ T cells in vitro and in vivo. Infect Immun. 2007;75(10):5018–26.PubMedCentralCrossRefPubMed Xin L, Li Y, Soong L. Role of interleukin-1β in activating the CD11c(high) CD45RB-dendritic cell subset and priming Leishmania amazonensis-specific CD4+ T cells in vitro and in vivo. Infect Immun. 2007;75(10):5018–26.PubMedCentralCrossRefPubMed
61.
go back to reference Voronov E, et al. IL-1-induced inflammation promotes development of leishmaniasis in susceptible BALB/c mice. Int Immunol. 2010;22(4):245–57.CrossRefPubMed Voronov E, et al. IL-1-induced inflammation promotes development of leishmaniasis in susceptible BALB/c mice. Int Immunol. 2010;22(4):245–57.CrossRefPubMed
62.
go back to reference Kautz-Neu K, et al. IL-1 signalling is dispensable for protective immunity in Leishmania-resistant mice. Exp Dermatol. 2011;20(1):76–8.CrossRefPubMed Kautz-Neu K, et al. IL-1 signalling is dispensable for protective immunity in Leishmania-resistant mice. Exp Dermatol. 2011;20(1):76–8.CrossRefPubMed
63.
go back to reference Fettelschoss A, et al. Inflammasome activation and IL-1β target IL-1α for secretion as opposed to surface expression. Proc Natl Acad Sci USA. 2011;108(44):18055–60.PubMedCentralCrossRefPubMed Fettelschoss A, et al. Inflammasome activation and IL-1β target IL-1α for secretion as opposed to surface expression. Proc Natl Acad Sci USA. 2011;108(44):18055–60.PubMedCentralCrossRefPubMed
64.
go back to reference Von Stebut E, et al. Interleukin 1α promotes Th1 differentiation and inhibits disease progression in Leishmania major-susceptible BALB/c mice. J Exp Med. 2003;198(2):191–9.CrossRef Von Stebut E, et al. Interleukin 1α promotes Th1 differentiation and inhibits disease progression in Leishmania major-susceptible BALB/c mice. J Exp Med. 2003;198(2):191–9.CrossRef
65.
go back to reference Lima-Junior DS, et al. Inflammasome-derived IL-1β production induces nitric oxide-mediated resistance to Leishmania. Nat Med. 2013;19(7):909–15.CrossRefPubMed Lima-Junior DS, et al. Inflammasome-derived IL-1β production induces nitric oxide-mediated resistance to Leishmania. Nat Med. 2013;19(7):909–15.CrossRefPubMed
66.
go back to reference Ji J, Sun J, Soong L. Impaired expression of inflammatory cytokines and chemokines at early stages of infection with Leishmania amazonensis. Infect Immun. 2003;71(8):4278–88.PubMedCentralCrossRefPubMed Ji J, Sun J, Soong L. Impaired expression of inflammatory cytokines and chemokines at early stages of infection with Leishmania amazonensis. Infect Immun. 2003;71(8):4278–88.PubMedCentralCrossRefPubMed
67.
go back to reference Soong L, et al. Role of CD4+ T cells in pathogenesis associated with Leishmania amazonensis infection. J Immunol. 1997;158(11):5374–83.PubMed Soong L, et al. Role of CD4+ T cells in pathogenesis associated with Leishmania amazonensis infection. J Immunol. 1997;158(11):5374–83.PubMed
69.
go back to reference World Health Organization. World malaria report 2012. p. 1–249. World Health Organization. World malaria report 2012. p. 1–249.
70.
go back to reference Moxon CA, Grau GE, Craig AG. Malaria: modification of the red blood cell and consequences in the human host. Br J Haematol. 2011;154(6):670–79. Moxon CA, Grau GE, Craig AG. Malaria: modification of the red blood cell and consequences in the human host. Br J Haematol. 2011;154(6):670–79.
71.
go back to reference Frevert U, Nacer A. Immunobiology of Plasmodium in liver and brain. Parasite Immunol. 2013;35(9–10):267–82.CrossRefPubMed Frevert U, Nacer A. Immunobiology of Plasmodium in liver and brain. Parasite Immunol. 2013;35(9–10):267–82.CrossRefPubMed
73.
go back to reference Krishnegowda G, et al. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem. 2005;280(9):8606–16.CrossRefPubMed Krishnegowda G, et al. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem. 2005;280(9):8606–16.CrossRefPubMed
74.
go back to reference Gowda NM, Wu X, Gowda DC. The nucleosome (histone-DNA complex) is the TLR9-specific immunostimulatory component of Plasmodium falciparum that activates DCs. PLoS ONE. 2011;6(6):e20398.PubMedCentralCrossRefPubMed Gowda NM, Wu X, Gowda DC. The nucleosome (histone-DNA complex) is the TLR9-specific immunostimulatory component of Plasmodium falciparum that activates DCs. PLoS ONE. 2011;6(6):e20398.PubMedCentralCrossRefPubMed
75.
go back to reference Parroche P, et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci USA. 2007;104(6):1919–24.PubMedCentralCrossRefPubMed Parroche P, et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci USA. 2007;104(6):1919–24.PubMedCentralCrossRefPubMed
76.
go back to reference Ockenhouse CF, et al. Common and divergent immune response signaling pathways discovered in peripheral blood mononuclear cell gene expression patterns in presymptomatic and clinically apparent malaria. Infect Immun. 2006;74(10):5561–73.PubMedCentralCrossRefPubMed Ockenhouse CF, et al. Common and divergent immune response signaling pathways discovered in peripheral blood mononuclear cell gene expression patterns in presymptomatic and clinically apparent malaria. Infect Immun. 2006;74(10):5561–73.PubMedCentralCrossRefPubMed
77.
go back to reference Finney CA, et al. Disruption of Nod-like receptors alters inflammatory response to infection but does not confer protection in experimental cerebral malaria. Am J Trop Med Hyg. 2009;80(5):718–22.PubMed Finney CA, et al. Disruption of Nod-like receptors alters inflammatory response to infection but does not confer protection in experimental cerebral malaria. Am J Trop Med Hyg. 2009;80(5):718–22.PubMed
78.
go back to reference Griffith JW, et al. Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol. 2009;183(8):5208–20.PubMedCentralCrossRefPubMed Griffith JW, et al. Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol. 2009;183(8):5208–20.PubMedCentralCrossRefPubMed
80.
go back to reference Shio MT, et al. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog. 2009;5(8):e1000559.CrossRefPubMed Shio MT, et al. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog. 2009;5(8):e1000559.CrossRefPubMed
82.
go back to reference Kordes M, Matuschewski K, Hafalla JC. Caspase-1 activation of interleukin-1β (IL-1β) and IL-18 is dispensable for induction of experimental cerebral malaria. Infect Immun. 2011;79(9):3633–41.PubMedCentralCrossRefPubMed Kordes M, Matuschewski K, Hafalla JC. Caspase-1 activation of interleukin-1β (IL-1β) and IL-18 is dispensable for induction of experimental cerebral malaria. Infect Immun. 2011;79(9):3633–41.PubMedCentralCrossRefPubMed
83.
go back to reference Coban C, et al. Immunogenicity of whole-parasite vaccines against Plasmodium falciparum involves malarial hemozoin and host TLR9. Cell Host Microbe. 2010;7(1):50–61.CrossRefPubMed Coban C, et al. Immunogenicity of whole-parasite vaccines against Plasmodium falciparum involves malarial hemozoin and host TLR9. Cell Host Microbe. 2010;7(1):50–61.CrossRefPubMed
84.
go back to reference Zhou J, et al. Opsonization of malaria-infected erythrocytes activates the inflammasome and enhances inflammatory cytokine secretion by human macrophages. Malar J. 2012;11:343.PubMedCentralCrossRefPubMed Zhou J, et al. Opsonization of malaria-infected erythrocytes activates the inflammasome and enhances inflammatory cytokine secretion by human macrophages. Malar J. 2012;11:343.PubMedCentralCrossRefPubMed
85.
go back to reference Ataide MA, et al. Malaria-induced NLRP12/NLRP3-dependent caspase-1 activation mediates inflammation and hypersensitivity to bacterial superinfection. PLoS Pathog. 2014;10(1):e1003885.PubMedCentralCrossRefPubMed Ataide MA, et al. Malaria-induced NLRP12/NLRP3-dependent caspase-1 activation mediates inflammation and hypersensitivity to bacterial superinfection. PLoS Pathog. 2014;10(1):e1003885.PubMedCentralCrossRefPubMed
86.
go back to reference Flegr J, et al. Toxoplasmosis—a global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS ONE. 2014;9(3):e90203.PubMedCentralCrossRefPubMed Flegr J, et al. Toxoplasmosis—a global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS ONE. 2014;9(3):e90203.PubMedCentralCrossRefPubMed
88.
go back to reference Michailowsky V, et al. Pivotal role of interleukin-12 and interferon-γ axis in controlling tissue parasitism and inflammation in the heart and central nervous system during Trypanosoma cruzi infection. Am J Pathol. 2001;159(5):1723–33.PubMedCentralCrossRefPubMed Michailowsky V, et al. Pivotal role of interleukin-12 and interferon-γ axis in controlling tissue parasitism and inflammation in the heart and central nervous system during Trypanosoma cruzi infection. Am J Pathol. 2001;159(5):1723–33.PubMedCentralCrossRefPubMed
89.
go back to reference Cardillo F, et al. Regulation of Trypanosoma cruzi infection in mice by γ interferon and interleukin 10: role of NK cells. Infect Immun. 1996;64(1):128–34.PubMedCentralPubMed Cardillo F, et al. Regulation of Trypanosoma cruzi infection in mice by γ interferon and interleukin 10: role of NK cells. Infect Immun. 1996;64(1):128–34.PubMedCentralPubMed
91.
go back to reference Witola WH, et al. NALP1 influences susceptibility to human congenital toxoplasmosis, proinflammatory cytokine response, and fate of Toxoplasma gondii-infected monocytic cells. Infect Immun. 2011;79(2):756–66.PubMedCentralCrossRefPubMed Witola WH, et al. NALP1 influences susceptibility to human congenital toxoplasmosis, proinflammatory cytokine response, and fate of Toxoplasma gondii-infected monocytic cells. Infect Immun. 2011;79(2):756–66.PubMedCentralCrossRefPubMed
93.
go back to reference Gov L, et al. Human innate immunity to Toxoplasma gondii is mediated by host caspase-1 and ASC and parasite GRA15. MBio. 2013;4(4):e0255-13. Gov L, et al. Human innate immunity to Toxoplasma gondii is mediated by host caspase-1 and ASC and parasite GRA15. MBio. 2013;4(4):e0255-13.
94.
go back to reference Gorfu G, et al. Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii. MBio 2014;5(1):e01117-13. Gorfu G, et al. Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii. MBio 2014;5(1):e01117-13.
96.
98.
go back to reference Jenkins SJ, et al. Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways. Int Immunol. 2005;17(11):1409–18.PubMedCentralCrossRefPubMed Jenkins SJ, et al. Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways. Int Immunol. 2005;17(11):1409–18.PubMedCentralCrossRefPubMed
99.
go back to reference Ritter M, et al. Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc Natl Acad Sci USA. 2010;107(47):20459–64.PubMedCentralCrossRefPubMed Ritter M, et al. Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc Natl Acad Sci USA. 2010;107(47):20459–64.PubMedCentralCrossRefPubMed
Metadata
Title
NLR proteins and parasitic disease
Authors
Gwendolyn M. Clay
Fayyaz S. Sutterwala
Mary E. Wilson
Publication date
01-08-2014
Publisher
Springer US
Published in
Immunologic Research / Issue 1-3/2014
Print ISSN: 0257-277X
Electronic ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-014-8544-x

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