Human innate immunity to Toxoplasma gondii is mediated by host caspase-1 and ASC and parasite GRA15

mBio

Volumn 4, Issue 4, 2013, Pages

  Gov, Lanny ^a   Karimzadeh, Alborz ^a   Ueno, Norikiyo ^a   Lodoen, Melissa B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS REPRESSOR WITH CASPASE RECRUITMENT DOMAIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MESSENGER RNA; PARASITE ANTIGEN; PROTEIN GRA15; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANTIPROTOZOAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GENE SILENCING; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOSTIMULATION; INFLAMMATION; INNATE IMMUNITY; LYMPH VESSEL METASTASIS; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRAIN DIFFERENCE; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRANSCRIPTION REGULATION;

PROTOZOA; TOXOPLASMA GONDII;

EID: 84883444752     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00255-13     Document Type: Article

References (57)

1. Dubey JP. 2008. The history of Toxoplasma gondii-the first 100 years. J. Eukaryot. Microbiol. 55:467-475.
2. Montoya JG, Liesenfeld O. 2004. Toxoplasmosis. Lancet 363:1965-1976.
3. Tenter AM, Heckeroth AR, Weiss LM. 2000. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30:1217-1258.
4. Luft BJ, Remington JS. 1992. Toxoplasmic encephalitis in AIDS. Clin. Infect. Dis. 15:211-222.
5. Jones JL, Lopez A, Wilson M, Schulkin J, Gibbs R. 2001. Congenital toxoplasmosis: a review. Obstet. Gynecol. Surv. 56:296-305.
6. Suzuki Y, Orellana MA, Schreiber RD, Remington JS. 1988. Interferongamma: the major mediator of resistance against Toxoplasma gondii. Science 240:516-518.
7. Gazzinelli RT, Hakim FT, Hieny S, Shearer GM, Sher A. 1991. Synergistic role of CD4+and CD8+T lymphocytes in IFN-gamma production and protective immunity induced by an attenuated Toxoplasma gondii vaccine. J. Immunol. 146:286-292.
8. Goldszmid RS, Caspar P, Rivollier A, White S, Dzutsev A, Hieny S, Kelsall B, Trinchieri G, Sher A. 2012. NK cell-derived interferon-gamma orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity 36:1047-1059.
9. Mordue DG, Sibley LD. 2003. A novel population of Gr-1+-activated macrophages induced during acute toxoplasmosis. J. Leukoc. Biol. 74: 1015-1025.
10. Robben PM, LaRegina M, Kuziel WA, Sibley LD. 2005. Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis. J. Exp. Med. 201:1761-1769.
11. Dunay IR, Damatta RA, Fux B, Presti R, Greco S, Colonna M, Sibley LD. 2008. Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29:306-317.
12. Channon JY, Seguin RM, Kasper LH. 2000. Differential infectivity and division of Toxoplasma gondii in human peripheral blood leukocytes. Infect. Immun. 68:4822-4826.
13. Dinarello CA. 2011. A clinical perspective of IL-1beta as the gatekeeper of inflammation. Eur. J. Immunol. 41:1203-1217.
14. Witola WH, Mui E, Hargrave A, Liu S, Hypolite M, Montpetit A, Cavailles P, Bisanz C, Cesbron-Delauw MF, Fournié GJ, McLeod R. 2011. NALP1 influences susceptibility to human congenital toxoplasmosis, proinflammatory cytokine response, and fate of Toxoplasma gondiiinfected monocytic cells. Infect. Immun. 79:756-766.
15. Kim SK, Fouts AE, Boothroyd JC. 2007. Toxoplasma gondii dysregulates IFN-gamma-inducible gene expression in human fibroblasts: insights from a genome-wide transcriptional profiling. J. Immunol. 178: 5154-5165.
16. Blader IJ, Manger ID, Boothroyd JC. 2001. Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. J. Biol. Chem. 276:24223-24231.
17. Nagineni CN, Detrick B, Hooks JJ. 2000. Toxoplasma gondii infection induces gene expression and secretion of interleukin 1 (IL-1), IL-6, granulocyte-macrophage colony-stimulating factor, and intercellular adhesion molecule 1 by human retinal pigment epithelial cells. Infect. Immun. 68:407-410.
18. Chang HR, Grau GE, Pechère JC. 1990. Role of TNF and IL-1 in infections with Toxoplasma gondii. Immunology 69:33-37.
19. Hunter CA, Chizzonite R, Remington JS. 1995. IL-1 beta is required for IL-12 to induce production of IFN-gamma byNKcells. Arole for IL-1 beta in the T cell-independent mechanism of resistance against intracellular pathogens. J. Immunol. 155:4347-4354.
20. van de Veerdonk FL, Netea MG, Dinarello CA, Joosten LA. 2011. Inflammasome activation and IL-1beta and IL-18 processing during infection. Trends Immunol. 32:110-116.
21. Martinon F, Burns K, Tschopp J. 2002. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell 10:417-426.
22. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J, Elliston KO, Ayala JM, Casano FJ, Chin J, Ding GJ-F, Egger LA, Gaffney EP, Limjuco G, Palyha OC, Raju SM, Rolando AM, Salley JP, Yamin T-T, Lee TD, Shively JE, Maccross M, Mumford RA, Schmidt JA, Tocci MJ. 1992. Anovel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356:768-774.
23. Martinon F, Pétrilli V, Mayor A, Tardivel A, Tschopp J. 2006. Goutassociated uric acid crystals activate the NALP3 inflammasome. Nature 440:237-241.
24. Masumoto J, Taniguchi S, Ayukawa K, Sarvotham H, Kishino T, Niikawa N, Hidaka E, Katsuyama T, Higuchi T, Sagara J. 1999. ASC, a novel 22-kDa protein, aggregates during apoptosis of human promyelocytic leukemia HL-60 cells. J. Biol. Chem. 274:33835-33838.
25. Martinon F, Hofmann K, Tschopp J. 2001. The pyrin domain: a possible member of the death domain-fold family implicated in apoptosis and inflammation. Curr. Biol. 11:R118-R120. doi: 10.1016/S0960-9822(01)00056-2.
26. Taxman DJ, Zhang J, Champagne C, Bergstralh DT, Iocca HA, Lich JD, Ting JP. 2006. Cutting edge: ASC mediates the induction of multiple cytokines by Porphyromonas gingivalis via caspase-1-dependent and-independent pathways. J. Immunol. 177:4252-4256.
27. Dobrowolski JM, Sibley LD. 1996. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84:933-939.
28. Howe DK, Sibley LD. 1995. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J. Infect. Dis. 172:1561-1566.
29. Sibley LD, Boothroyd JC. 1992. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature 359:82-85.
30. Rosowski EE, Lu D, Julien L, Rodda L, Gaiser RA, Jensen KD, Saeij JP. 2011. Strain-specific activation of the NF-kappaB pathway by GRA15, a novel Toxoplasma gondii dense granule protein. J. Exp. Med. 208: 195-212.
31. Atianand MK, Duffy EB, Shah A, Kar S, Malik M, Harton JA. 2011. Francisella tularensis reveals a disparity between human and mouse NLRP3 inflammasome activation. J. Biol. Chem. 286:39033-39042.
32. Netea MG, Nold-Petry CA, Nold MF, Joosten LA, Opitz B, van der Meer JH, van de Veerdonk FL, Ferwerda G, Heinhuis B, Devesa I, Funk CJ, Mason RJ, Kullberg BJ, Rubartelli A, van der Meer JW, Dinarello CA. 2009. Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 113:2324-2335.
33. Gu Y, Kuida K, Tsutsui H, Ku G, Hsiao K, Fleming MA, Hayashi N, Higashino K, Okamura H, Nakanishi K, Kurimoto M, Tanimoto T, Flavell RA, Sato V, Harding MW, Livingston DJ, Su MS. 1997. Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science 275:206-209.
34. Ghayur T, Banerjee S, Hugunin M, Butler D, Herzog L, Carter A, Quintal L, Sekut L, Talanian R, Paskind M, Wong W, Kamen R, Tracey D, Allen H. 1997. Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature 386:619-623.
35. Puren AJ, Fantuzzi G, Dinarello CA. 1999. Gene expression, synthesis, and secretion of interleukin 18 and interleukin 1beta are differentially regulated in human blood mononuclear cells and mouse spleen cells. Proc. Natl. Acad. Sci. U. S. A. 96:2256-2261.
36. Rathinam VA, Vanaja SK, Fitzgerald KA. 2012. Regulation of inflammasome signaling. Nat. Immunol. 13:333. doi: 10.1038/ni.2237.
37. Martinon F, Tschopp J. 2007. Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ. 14:10-22.
38. Hitziger N, Dellacasa I, Albiger B, Barragan A. 2005. Dissemination of Toxoplasma gondii to immunoprivileged organs and role of toll/ interleukin-1 receptor signalling for host resistance assessed by in vivo bioluminescence imaging. Cell. Microbiol. 7:837-848.
39. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, Su MS, Flavell RA. 1995. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267:2000-2003.
40. Kayagaki N, Warming S, Lamkanfi M, Vande Walle L, Louie S, Dong J, Newton K, Qu Y, Liu J, Heldens S, Zhang J, Lee WP, Roose-Girma M, Dixit VM. 2011. Non-canonical inflammasome activation targets caspase-11. Nature 479:117-121.
41. Hunter CA, Sibley LD. 2012. Modulation of innate immunity by Toxoplasma gondii virulence effectors. Nat. Rev. Microbiol. 10:766-778.
42. Ferrari D, Chiozzi P, Falzoni S, Dal Susino M, Melchiorri L, Baricordi OR, Di Virgilio F. 1997. Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J. Immunol. 159:1451-1458.
43. Corrêa G, Marques da Silva C, de Abreu Moreira-Souza AC, Vommaro RC, Coutinho-Silva R. 2010. Activation of the P2X(7) receptor triggers the elimination of Toxoplasma gondii tachyzoites from infected macrophages. Microbes Infect. 12:497-504.
44. Jamieson SE, Peixoto-Rangel AL, Hargrave AC, Roubaix LA, Mui EJ, Boulter NR, Miller EN, Fuller SJ, Wiley JS, Castellucci L, Boyer K, Peixe RG, Kirisits MJ, de Souza Elias L, Coyne JJ, Correa-Oliveira R, Sautter M, Smith NC, Lees MP, Swisher CN, Heydemann P, Noble AG, Patel D, Bardo D, Burrowes D, McLone D, Roizen N, Withers S, Bahia-Oliveira LM, McLeod R, Blackwell JM. 2010. Evidence for associations between the purinergic receptor P2X(7) (P2RX7) and toxoplasmosis. Genes Immun. 11:374-383.
45. Lees MP, Fuller SJ, McLeod R, Boulter NR, Miller CM, Zakrzewski AM, Mui EJ, Witola WH, Coyne JJ, Hargrave AC, Jamieson SE, Blackwell JM, Wiley JS, Smith NC. 2010. P2X7 receptor-mediated killing of an intracellular parasite, Toxoplasma gondii, by human and murine macrophages. J. Immunol. 184:7040-7046.
46. Bobak DA, Frank MM, Tenner AJ. 1986. Characterization of C1q receptor expression on human phagocytic cells: effects of PDBu and fMLP. J. Immunol. 136:4604-4610.
47. Pernas L, Boothroyd JC. 2010. Association of host mitochondria with the parasitophorous vacuole during Toxoplasma infection is not dependent on rhoptry proteins ROP2/8. Int. J. Parasitol. 40:1367-1371.
48. Kim SK, Karasov A, Boothroyd JC. 2007. Bradyzoite-specific surface antigen SRS9 plays a role in maintaining Toxoplasma gondii persistence in the brain and in host control of parasite replication in the intestine. Infect. Immun. 75:1626-1634.
49. Morgado P, Ong YC, Boothroyd JC, Lodoen MB. 2011. Toxoplasma gondii induces B7-2 expression through activation of JNK signal transduction. Infect. Immun. 79:4401-4412.
50. Lavine MD, Arrizabalaga G. 2008. Exit from host cells by the pathogenic parasite Toxoplasma gondii does not require motility. Eukaryot. Cell 7:131-140.
51. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta delta C(T) method. Methods 25:402-408.
52. Jasper MJ, Tremellen KP, Robertson SA. 2007. Reduced expression of IL-6 and IL-1alpha mRNAs in secretory phase endometrium of women with recurrent miscarriage. J. Reprod. Immunol. 73:74-84.
53. Wong BC, Chan KC, Chan AT, Leung SF, Chan LY, Chow KC, Lo YM. 2006. Reduced plasma RNA integrity in nasopharyngeal carcinoma patients. Clin. Cancer Res. 12:2512-2516.
54. Khoury MK, Parker I, Aswad DW. 2010. Acquisition of chemiluminescent signals from immunoblots with a digital single-lens reflex camera. Anal. Biochem. 397:129-131.
55. Lodoen MB, Gerke C, Boothroyd JC. 2010. A highly sensitive FRETbased approach reveals secretion of the actin-binding protein toxofilin during Toxoplasma gondii infection. Cell. Microbiol. 12:55-66.
56. Saharia A, Guittat L, Crocker S, Lim A, Steffen M, Kulkarni S, Stewart SA. 2008. Flap endonuclease 1 contributes to telomere stability. Curr. Biol. 18:496-500.
57. Papin S, Cuenin S, Agostini L, Martinon F, Werner S, Beer HD, Grütter C, Grütter M, Tschopp J. 2007. The SPRY domain of pyrin, mutated in familial Mediterranean fever patients, interacts with inflammasome components and inhibits proIL-1beta processing. Cell Death Differ. 14: 1457-1466.