NLR proteins and parasitic disease

Immunologic Research

Volumn 59, Issue 1-3, 2014, Pages 142-152

  Clay, Gwendolyn M ^a   Sutterwala, Fayyaz S ^b,c   Wilson, Mary E ^b,c  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Inflammasomes; Innate immune defense; NLR proteins; Parasitology

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CRYOPYRIN; INFLAMMASOME; APOPTOSIS REGULATORY PROTEIN; CARRIER PROTEIN; NLRP1 PROTEIN, HUMAN; NLRP3 PROTEIN, HUMAN; NOD1 PROTEIN, HUMAN; NOD2 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

BRAIN MALARIA; CHAGAS DISEASE; HUMAN; IMMUNE RESPONSE; IMMUNITY; LEISHMANIA; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW; SCHISTOSOMA; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRYPANOSOMA CRUZI; ANIMAL; ART; IMMUNOLOGY; PATHOLOGY; PROTOZOAL INFECTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS REGULATORY PROTEINS; CARRIER PROTEINS; HUMANS; INFLAMMASOMES; NOD1 SIGNALING ADAPTOR PROTEIN; NOD2 SIGNALING ADAPTOR PROTEIN; PORTRAITS AS TOPIC; PROTOZOAN INFECTIONS;

EID: 84905718120     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-014-8544-x     Document Type: Review

References (99)

1. Schroder K, Tschopp J. The inflammasomes. Cell. 2010;140(6):821-32.
2. Davis BK, Wen H, Ting JP. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol. 2011;29:707-35.
3. Franchi L, Munoz-Planillo R, Nunez G. Sensing and reacting to microbes through the inflammasomes. Nat Immunol. 2012;13(4):325-32.
4. Elinav E, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell. 2011;145(5):745-57.
5. Wlodarska M, et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell. 2014;156(5):1045-59.
6. Eisenbarth SC, et al. NLRP10 is a NOD-like receptor essential to initiate adaptive immunity by dendritic cells. Nature. 2012;484(7395):510-3.
7. Joly S, et al. Cutting edge: Nlrp10 is essential for protective antifungal adaptive immunity against Candida albicans. J Immunol. 2012;189(10):4713-7.
8. 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.
9. Arthur JC, et al. Cutting edge: NLRP12 controls dendritic and myeloid cell migration to affect contact hypersensitivity. J Immunol. 2010;185(8):4515-9.
10. Zaki MH, et al. The NOD-like receptor NLRP12 attenuates colon inflammation and tumorigenesis. Cancer Cell. 2011;20(5):649-60.
11. 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.
12. Vladimer GI, et al. The NLRP12 inflammasome recognizes Yersinia pestis. Immunity. 2012;37(1):96-107.
13. Faustin B, et al. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell. 2007;25(5):713-24. (Pubitemid 46341921)
14. 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.
15. 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.
16. 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.
17. Zhao Y, et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature. 2011;477(7366):596-600.
18. Kofoed EM, Vance RE. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature. 2011;477(7366):592-5.
19. 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.
20. Tenthorey JL, et al. Molecular basis for specific recognition of bacterial ligands by NAIP/NLRC4 inflammasomes. Mol Cell. 2014;54(1):17-29.
21. Rayamajhi M, et al. Cutting edge: mouse NAIP1 detects the type III secretion system needle protein. J Immunol. 2013;191(8):3986-9.
22. Qu Y, et al. Phosphorylation of NLRC4 is critical for inflammasome activation. Nature. 2012;490(7421):539-42.
23. Hornung V, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature. 2009;458(7237):514-8.
24. Fernandes-Alnemri T, et al. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature. 2009;458(7237):509-13.
25. Roberts TL, et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science. 2009;323(5917):1057-60.
26. 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.
27. 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.
28. Adamczak SE, et al. Pyroptotic neuronal cell death mediated by the AIM2 inflammasome. J Cereb Blood Flow Metab. 2014;34(4):621-9.
29. Cassel SL, Sutterwala FS. Sterile inflammatory responses mediated by the NLRP3 inflammasome. Eur J Immunol. 2010;40(3):607-11.
30. Wen H, Miao EA, Ting JP. Mechanisms of NOD-like receptor-associated inflammasome activation. Immunity. 2013;39(3):432-41.
31. Horng T. Calcium signaling and mitochondrial destabilization in the triggering of the NLRP3 inflammasome. Trends Immunol. 2014;35(6):253-61.
32. Fitzgerald KA. NLR-containing inflammasomes: central mediators of host defense and inflammation. Eur J Immunol. 2010;40(3):595-8.
33. Philpott DJ, et al. NOD proteins: regulators of inflammation in health and disease. Nat Rev Immunol. 2014;14(1):9-23.
34. Rubino SJ, et al. Nod-like receptors in the control of intestinal inflammation. Curr Opin Immunol. 2012;24(4):398-404.
35. Moreira LO, Zamboni DS. NOD1 and NOD2 Signaling in Infection and Inflammation. Front Immunol. 2012;3:328.
36. 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.
37. Cui J, et al. NLRC5 negatively regulates the NF-κB and type I interferon signaling pathways. Cell. 2010;141(3):483-96.
38. Benko S, et al. NLRC5 limits the activation of inflammatory pathways. J Immunol. 2010;185(3):1681-91.
39. 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.
40. Tanowitz HB, et al. Perspectives on Trypanosoma cruzi-induced heart disease (Chagas disease). Prog Cardiovasc Dis. 2009;51(6):524-39.
41. Teixeira MM, Gazzinelli RT, Silva JS. Chemokines, inflammation and Trypanosoma cruzi infection. Trends Parasitol. 2002;18(6):262-5. (Pubitemid 34569236)
42. 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. (Pubitemid 44359881)
43. 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.
44. 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.
45. 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. (Pubitemid 38116819)
46. 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.
47. 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.
48. Julia V, Rassoulzadegan M, Glaichenhaus N. Resistance to Leishmania major induced by tolerance to a single antigen. Science. 1996;274(5286):421-3. (Pubitemid 26353355)
49. World Health Organization. Leishmaniasis; 2014. www.who.int/topics/ leishmaniasis/en/ and www.who.int/mediacentre/factsheets/fs375/en/.
50. Alvar J, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE. 2012;7(5):e35671.
51. 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. (Pubitemid 15028911)
52. 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. (Pubitemid 19191560)
53. 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. (Pubitemid 18040498)
54. 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.
55. Wilson ME, Jeronimo SM, Pearson RD. Immunopathogenesis of infection with the visceralizing Leishmania species. Microb Pathog. 2005;38(4):147-60. (Pubitemid 40417730)
56. 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. (Pubitemid 40548295)
57. Kaye P, Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol. 2011;9(8):604-15.
58. 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. (Pubitemid 30389835)
59. 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. (Pubitemid 30253812)
60. 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. (Pubitemid 47502175)
61. Voronov E, et al. IL-1-induced inflammation promotes development of leishmaniasis in susceptible BALB/c mice. Int Immunol. 2010;22(4):245-57.
62. Kautz-Neu K, et al. IL-1 signalling is dispensable for protective immunity in Leishmania-resistant mice. Exp Dermatol. 2011;20(1):76-8.
63. 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.
64. 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. (Pubitemid 36992177)
65. Lima-Junior DS, et al. Inflammasome-derived IL-1β production induces nitric oxide-mediated resistance to Leishmania. Nat Med. 2013;19(7):909-15.
66. 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. (Pubitemid 36919890)
67. Soong L, et al. Role of CD4+ T cells in pathogenesis associated with Leishmania amazonensis infection. J Immunol. 1997;158(11):5374-83. (Pubitemid 127681244)
68. Moyes CL, et al. Defining the geographical range of the Plasmodium knowlesi reservoir. PLoS Negl Trop Dis. 2014;8(3):e2780.
69. World Health Organization. World malaria report 2012. p. 1-249.
70. 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. Frevert U, Nacer A. Immunobiology of Plasmodium in liver and brain. Parasite Immunol. 2013;35(9-10):267-82.
72. Coban C, et al. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med. 2005;201(1):19-25. (Pubitemid 40130079)
73. 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. (Pubitemid 40349765)
74. 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.
75. 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. (Pubitemid 46239879)
76. 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. (Pubitemid 44484539)
77. 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.
78. 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.
79. Dostert C, et al. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS ONE. 2009;4(8):e6510.
80. Shio MT, et al. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog. 2009;5(8):e1000559.
81. Reimer T, et al. Experimental cerebral malaria progresses independently of the Nlrp3 inflammasome. Eur J Immunol. 2010;40(3):764-9.
82. 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.
83. 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.
84. 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.
85. 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.
86. 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.
87. Robert-Gangneux F, Darde ML. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 2012;25(2):264-96.
88. 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. (Pubitemid 33062515)
89. 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. (Pubitemid 26009351)
90. Shaw MH, et al. T cell-intrinsic role of Nod2 in promoting type 1 immunity to Toxoplasma gondii. Nat Immunol. 2009;10(12):1267-74.
91. 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.
92. Ewald SE, Chavarria-Smith J, Boothroyd JC. NLRP1 is an inflammasome sensor for Toxoplasma gondii. Infect Immun. 2014;82(1):460-8.
93. 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. Gorfu G, et al. Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii. MBio 2014;5(1):e01117-13.
95. World Health Organization. Schistosomiasis: progress report 2001-2011, strategic plan 2012-2020. Geneva: World Health Organization; 2013. http://apps.who.int/iris/handle/10665/78074#sthash.H3fFKrLo.dpuf.
96. Fairfax K, et al. Th2 responses in schistosomiasis. Semin Immunopathol. 2012;34(6):863-71.
97. Maizels RM, et al. Regulation of pathogenesis and immunity in helminth infections. J Exp Med. 2009;206(10):2059-66.
98. Jenkins SJ, et al. Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways. Int Immunol. 2005;17(11):1409-18. (Pubitemid 41631317)
99. 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.