Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii

mBio

Volumn 5, Issue 1, 2014, Pages

  Gorfu, Gezahegn ^a,e   Cirelli, Kimberly M ^b   Melo, Mariane B ^b   Mayer Barber, Katrin ^a   Crown, Devorah ^a   Koller, Beverly H ^c   Masters, Seth ^d   Sher, Alan ^a   Leppla, Stephen H ^a   Moayeri, Mahtab ^a   Saeij, Jeroen P J ^b   Grigg, Michael E ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e HOWARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; CASPASE 11; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 18; INTERLEUKIN 18 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 8; PROTEIN NLRP1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEATH; FEMALE; HOST RESISTANCE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFECTION RESISTANCE; MACROPHAGE; MALE; MOUSE; NONHUMAN; PARASITE LOAD; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS REGULATORY PROTEINS; CARRIER PROTEINS; DISEASE RESISTANCE; FEMALE; INFLAMMASOMES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PARASITE LOAD; SURVIVAL ANALYSIS; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL;

EID: 84903369192     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01117-13     Document Type: Article

References (66)

1. Lamkanfi M, Dixit VM. 2012. Inflammasomes and their roles in health and disease. Annu. Rev. Cell Dev. Biol. 28:137-161. http://dx.doi.org/ 10.1146/annurev-cellbio-101011-155745.
2. Song DH, Lee JO. 2012. Sensing of microbial molecular patterns by Toll-like receptors. Immunol. Rev. 250:216-229. http://dx.doi.org/ 10.1111/j.1600-065X.2012.01167.x.
3. Hunter CA, Sibley LD. 2012. Modulation of innate immunity by Toxoplasma gondii virulence effectors. Nat. Rev. Microbiol. 10:766-778. http:// dx.doi.org/10.1038/nrmicro2858.
4. Melo MB, Jensen KD, Saeij JP. 2011. Toxoplasma gondii effectors are master regulators of the inflammatory response. Trends Parasitol. 27: 487-495. http://dx.doi.org/10.1016/j.pt.2011.08.001.
5. Khan IA, Schwartzman JD, Matsuura T, Kasper LH. 1997. A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc. Natl. Acad. Sci. U. S. A. 94:13955-13960. http://dx.doi.org/ 10.1073/pnas.94.25.13955.
6. LaRosa DF, Stumhofer JS, Gelman AE, Rahman AH, Taylor DK, Hunter CA, Turka LA. 2008. T cell expression of MyD88 is required for resistance to Toxoplasma gondii. Proc. Natl. Acad. Sci. U. S. A. 105: 3855-3860. http://dx.doi.org/10.1073/pnas.0706663105.
7. Scanga CA, Aliberti J, Jankovic D, Tilloy F, Bennouna S, Denkers EY, Medzhitov R, Sher A. 2002. Cutting edge: MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. J. Immunol. 168:5997-6001.
8. Scharton-Kersten TM, Wynn TA, Denkers EY, Bala S, Grunvald E, Hieny S, Gazzinelli RT, Sher A. 1996. In the absence of endogenous IFN-gamma, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J. Immunol. 157: 4045-4054.
9. Scharton-Kersten TM, Yap G, Magram J, Sher A. 1997. Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J. Exp. Med. 185: 1261-1273. http://dx.doi.org/10.1084/jem.185.7.1261.
10. Sher A, Collazzo C, Scanga C, Jankovic D, Yap G, Aliberti J. 2003. Induction and regulation of IL-12-dependent host resistance to Toxoplasma gondii. Immunol. Res. 27:521-528. http://dx.doi.org/10.1385/IR: 27:2-3:521.
11. Suzuki Y, Orellana MA, Schreiber RD, Remington JS. 1988. Interferongamma: the major mediator of resistance against Toxoplasma gondii. Science 240:516-518. http://dx.doi.org/10.1126/science.3128869.
12. 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. http://dx.doi.org/10.1016/j.immuni.2008.05.019.
13. 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. http://dx.doi.org/10.1084/jem.20050054.
14. Martinon F, Mayor A, Tschopp J. 2009. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27:229-265. http://dx.doi.org/ 10.1146/annurev.immunol.021908.132715.
15. Boyden ED, Dietrich WF. 2006. Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 38:240-244. http:// dx.doi.org/10.1038/ng1724.
16. 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, Elias LS, 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. http://dx.doi.org/10.1038/gene.2010.31.
17. 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. http://dx.doi.org/ 10.1128/IAI.00898-10.
18. Gov L, Karimzadeh A, Ueno N, Lodoen MB. 2013. Human innate immunity to Toxoplasma gondii is mediated by host caspase-1 and ASC and parasite GRA15. mBio 4(4):e00255-13. http://dx.doi.org/10.1128/ mBio.00255-13.
19. 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. http://dx.doi.org/10.4049/ jimmunol.1000012.
20. Dinarello CA, Novick D, Puren AJ, Fantuzzi G, Shapiro L, Mühl H, Yoon DY, Reznikov LL, Kim SH, Rubinstein M. 1998. Overview of interleukin-18: more than an interferon-gamma inducing factor. J. Leukoc. Biol. 63:658-664.
21. Chang HR, Grau GE, Pechère JC. 1990. Role of TNF and IL-1 in infections with Toxoplasma gondii. Immunology 69:33-37.
22. 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.
23. Broz P, von Moltek J, Jones JW, Vance RE, Monack DM. 2010. Differential requirement for caspase-1 autoproteolysis in pathogeninduced cell death and cytokine processing. Cell Host Microbe 8:471-483. http://dx.doi.org/10.1016/j.chom.2010.11.007.
24. 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. http://dx.doi.org/10.1084/jem.20100717.
25. Sastalla I, Crown D, Masters SL, McKenzie A, Leppla SH, Moayeri M. 2013. Transcriptional analysis of the three Nlrp1 paralogs in mice. BMC Genomics 14:188. http://dx.doi.org/10.1186/1471-2164-14-188.
26. 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. http://dx.doi.org/10.1038/nature10558.
27. Latz E, Xiao TS, Stutz A. 2013. Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13:397-411. http://dx.doi.org/10.1038/ nri3452.
28. Cai G, Kastelein R, Hunter CA. 2000. Interleukin-18 (IL-18) enhances innate IL-12-mediated resistance to Toxoplasma gondii. Infect. Immun. 68:6932-6938. http://dx.doi.org/10.1128/IAI.68.12.6932-6938.2000.
29. Yap GS, Ortmann R, Shevach E, Sher A. 2001. A heritable defect in IL-12 signaling in B10. Q/J mice. II. Effect on acute resistance to Toxoplasma gondii and rescue by IL-18 treatment. J. Immunol. 166:5720-5725.
30. Mordue DG, Monroy F, La Regina M, Dinarello CA, Sibley LD. 2001. Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. J. Immunol. 167:4574-4584.
31. Okamura H, Tsutsi H, Komatsu T, Yutsudo M, Hakura A, Tanimoto T, Torigoe K, Okura T, Nukada Y, Hattori K. 1995. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 378: 88-91. http://dx.doi.org/10.1038/378088a0.
32. 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. USA 96:2256-2261. http://dx.doi.org/10.1073/ pnas.96.5.2256.
33. 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. http://dx.doi.org/10.1038/386619a0.
34. 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. http://dx.doi.org/10.1126/ science.275.5297.206.
35. Bossaller L, Chiang PI, Schmidt-Lauber C, Ganesan S, Kaiser WJ, Rathinam VA, Mocarski ES, Subramanian D, Green DR, Silverman N, Fitzgerald KA, Marshak-Rothstein A, Latz E. 2012. Cutting edge: FAS (CD95) mediates noncanonical IL-1beta and IL-18 maturation via caspase-8 in an RIP3-independent manner. J. Immunol. 189:5508-5512. http://dx.doi.org/10.4049/jimmunol.1202121.
36. Howard JC, Hunn JP, Steinfeldt T. 2011. The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii. Curr. Opin. Microbiol. 14:414-421. http://dx.doi.org/10.1016/ j.mib.2011.07.002.
37. Hunn JP, Feng CG, Sher A, Howard JC. 2011. The immunity-related GTPases in mammals: a fast-evolving cell-autonomous resistance system against intracellular pathogens. Mamm. Genome 22:43-54. http:// dx.doi.org/10.1007/s00335-010-9293-3.
38. Gavrilescu LC, Denkers EY. 2001. IFN-gamma overproduction and high level apoptosis are associated with high but not low virulence Toxoplasma gondii infection. J. Immunol. 167:902-909.
39. 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. http://dx.doi.org/ 10.1111/j.1462-5822.2005.00517.x.
40. Cavaillès P, Sergent V, Bisanz C, Papapietro O, Colacios C, Mas M, Subra JF, Lagrange D, Calise M, Appolinaire S, Faraut T, Druet P, Saoudi A, Bessieres MH, Pipy B, Cesbron-Delauw MF, Fournié GJ. 2006. The rat Toxo1 locus directs toxoplasmosis outcome and controls parasite proliferation and spreading by macrophage-dependent mechanisms. Proc. Natl. Acad. Sci. U. S. A. 103:744-749. http://dx.doi.org/ 10.1073/pnas.0506643103.
41. Miao EA, Leaf IA, Treuting PM, Mao DP, Dors M, Sarkar A, Warren SE, Wewers MD, Aderem A. 2010. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11:1136-1142. http://dx.doi.org/10.1038/ni.1960.
42. Chou DB, Sworder B, Bouladoux N, Roy CN, Uchida AM, Grigg M, Robey PG, Belkaid Y. 2012. Stromal-derived IL-6 alters the balance of myeloerythroid progenitors during Toxoplasma gondii infection. J. Leukoc. Biol. 92:123-131. http://dx.doi.org/10.1189/jlb.1011527.
43. Corrêa G, Marques da SC, 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. http://dx.doi.org/10.1016/ j.micinf.2010.03.004.
44. Miller CM, Zakrzewski AM, Ikin RJ, Boulter NR, Katrib M, Lees MP, Fuller SJ, Wiley JS, Smith NC. 2011. Dysregulation of the inflammatory response to the parasite, Toxoplasma gondii, in P2X7 receptor-deficient mice. Int. J. Parasitol. 41:301-308. http://dx.doi.org/10.1016/ j.ijpara.2010.10.001.
45. Wen H, Miao EA, Ting JP. 2013. Mechanisms of NOD-like receptorassociated inflammasome activation. Immunity 39:432-441. http:// dx.doi.org/10.1016/j.immuni.2013.08.037.
46. Yamamoto M, Ma JS, Mueller C, Kamiyama N, Saiga H, Kubo E, Kimura T, Okamoto T, Okuyama M, Kayama H, Nagamune K, Takashima S, Matsuura Y, Soldati-Favre D, Takeda K. 2011. ATF6beta is a host cellular target of the Toxoplasma gondii virulence factor ROP18. J. Exp. Med. 208:1533-1546. http://dx.doi.org/10.1084/jem.20101660.
47. Niedelman W, Sprokholt JK, Clough B, Frickel EM, Saeij JP. 2013. Cell death of interferon-gamma stimulated human fibroblasts upon Toxoplasma gondii infection induces early parasite egress and limits parasite replication. Infect. Immun. 81:4341-4349.
48. Selleck EM, Fentress SJ, Beatty WL, Degrandi D, Pfeffer K, Virgin HW, Macmicking JD, Sibley LD. 2013. Guanylate-binding protein 1 (Gbp1) contributes to cell-autonomous immunity against Toxoplasma gondii. PLoS Pathog. 9:e1003320. http://dx.doi.org/10.1371/ journal.ppat.1003320.
49. Fruth IA, Arrizabalaga G. 2007. Toxoplasma gondii: induction of egress by the potassium ionophore nigericin. Int. J. Parasitol. 37:1559-1567. http://dx.doi.org/10.1016/j.ijpara.2007.05.010.
50. Levinsohn JL, Newman ZL, Hellmich KA, Fattah R, Getz MA, Liu S, Sastalla I, Leppla SH, Moayeri M. 2012. Anthrax lethal factor cleavage of Nlrp1 is required for activation of the inflammasome. PLoS Pathog. 8:e1002638. http://dx.doi.org/10.1371/journal.ppat.1002638.
51. Newman ZL, Printz MP, Liu S, Crown D, Breen L, Miller-Randolph S, Flodman P, Leppla SH, Moayeri M. 2010. Susceptibility to anthrax lethal toxin-induced rat death is controlled by a single chromosome 10 locus that includes rNlrp1. PLoS Pathog. 6:e1000906. http://dx.doi.org/ 10.1371/journal.ppat.1000906.
52. Binder EM, Kim K. 2004. Location, location, location: trafficking and function of secreted proteases of Toxoplasma and Plasmodium. Traffic 5:914-924. http://dx.doi.org/10.1111/j.1600-0854.2004.00244.x.
53. Choi WY, Nam HW, Youn JH. 1989. Characterization of proteases of Toxoplasma gondii. Kisaengchunghak Chapchi 27:161-170.
54. Dou Z, Carruthers VB. 2011. Cathepsin proteases in Toxoplasma gondii. Adv. Exp. Med. Biol. 712:49-61. http://dx.doi.org/10.1007/978-1-4419-8414-2_4.
55. Dou Z, Coppens I, Carruthers VB. 2013. Non-canonical maturation of two papain-family proteases in Toxoplasma gondii. J. Biol. Chem. 288: 3523-3534. http://dx.doi.org/10.1074/jbc.M112.443697.
56. Kim K. 2004. Role of proteases in host cell invasion by Toxoplasma gondii and other Apicomplexa. Acta Trop. 91:69-81. http://dx.doi.org/10.1016/ j.actatropica.2003.11.016.
57. Shea M, Jäkle U, Liu Q, Berry C, Joiner KA, Soldati-Favre D. 2007. A family of aspartic proteases and a novel, dynamic and cell-cycledependent protease localization in the secretory pathway of Toxoplasma gondii. Traffic 8:1018-1034. http://dx.doi.org/10.1111/j.1600-0854.2007.00589.x.
58. Kofoed EM, Vance RE. 2011. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477: 592-595. http://dx.doi.org/10.1038/nature10394.
59. Zhao Y, Yang J, Shi J, Gong YN, Lu Q, Xu H, Liu L, Shao F. 2011. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477:596-600. http://dx.doi.org/10.1038/ nature10510.
60. Sutterwala FS, Ogura Y, Szczepanik M, Lara-Tejero M, Lichtenberger GS, Grant EP, Bertin J, Coyle AJ, Galán JE, Askenase PW, Flavell RA. 2006. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24:317-327. http://dx.doi.org/10.1016/j.immuni.2006.02.004.
61. Kovarova M, Hesker PR, Jania L, Nguyen M, Snouwaert JN, Xiang Z, Lommatzsch SE, Huang MT, Ting JP, Koller BH. 2012. NLRP1-dependent pyroptosis leads to acute lung injury and morbidity in mice. J. Immunol. 189:2006-2016. http://dx.doi.org/10.4049/ jimmunol.1201065.
62. Masters SL, Gerlic M, Metcalf D, Preston S, Pellegrini M, O'Donnell JA, McArthur K, Baldwin TM, Chevrier S, Nowell CJ, Cengia LH, Henley KJ, Collinge JE, Kastner DL, Feigenbaum L, Hilton DJ, Alexander WS, Kile BT, Croker BA. 2012. NLRP1 inflammasome activation induces pyroptosis of hematopoietic progenitor cells. Immunity 37:1009-1023. http://dx.doi.org/10.1016/j.immuni.2012.08.027.
63. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM. 2006. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440:228-232. http://dx.doi.org/10.1038/nature04515.
64. Saeij JP, Boyle JP, Grigg ME, Arrizabalaga G, Boothroyd JC. 2005. Bioluminescence imaging of Toxoplasma gondii infection in living mice reveals dramatic differences between strains. Infect. Immun. 73:695-702. http://dx.doi.org/10.1128/IAI.73.2.695-702.2005.
65. Jensen KD, Wang Y, Wojno ED, Shastri AJ, Hu K, Cornel L, Boedec E, Ong YC, Chien YH, Hunter CA, Boothroyd JC, Saeij JP. 2011. Toxoplasma polymorphic effectors determine macrophage polarization and intestinal inflammation. Cell Host Microbe 9:472-483. http://dx.doi.org/ 10.1016/j.chom.2011.04.015.
66. Cirelli KM, Gorfu G, Hassan MA, Printz M, Crown D, Leppla SH, Grigg ME, Saeij JPJ, Moayeri M. Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii. PLoS Pathog., in press.