1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Recognition of Intracellular Bacteria by Inflammasomes

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Author: Petr Broz1
  • Editors: Pascale Cossart2, Craig R. Roy3, Philippe Sansonetti4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biochemistry, University of Lausanne, Switzerland; 2: Institut Pasteur, Paris, France; 3: Yale University School of Medicine, New Haven, Connecticut; 4: Institut Pasteur, Paris, France
    • Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0003-2019
  • Received 26 March 2018 Accepted 17 May 2018 Published 08 March 2019
  • Petr Broz, [email protected]
image of Recognition of Intracellular Bacteria by Inflammasomes
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Recognition of Intracellular Bacteria by Inflammasomes, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/7/2/BAI-0003-2019-1.gif /docserver/preview/fulltext/microbiolspec/7/2/BAI-0003-2019-2.gif

  • Abstract:

    Inflammasomes are multiprotein signaling complexes that are assembled by cytosolic sensors upon the detection of infectious or noxious stimuli. These complexes activate inflammatory caspases to induce host cell death and cytokine secretion and are an essential part of antimicrobial host defense. In this review, I discuss how intracellular bacteria are detected by inflammasomes, how the specific sensing mechanism of each inflammasome receptor restricts the ability of bacteria to evade immune recognition, and how host cell death is used to control bacterial replication .

  • Citation: Broz P. 2019. Recognition of Intracellular Bacteria by Inflammasomes. Microbiol Spectrum 7(2):BAI-0003-2019. doi:10.1128/microbiolspec.BAI-0003-2019.

References

1. Broz P, Dixit VM. 2016. Inflammasomes: mechanism of assembly, regulation and signalling. Nat Rev Immunol 16:407–420 http://dx.doi.org/10.1038/nri.2016.58. [PubMed]
2. 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 http://dx.doi.org/10.1016/S1097-2765(02)00599-3.
3. Liston A, Masters SL. 2017. Homeostasis-altering molecular processes as mechanisms of inflammasome activation. Nat Rev Immunol 17:208–214 http://dx.doi.org/10.1038/nri.2016.151. [PubMed]
4. Dick MS, Sborgi L, Rühl S, Hiller S, Broz P. 2016. ASC filament formation serves as a signal amplification mechanism for inflammasomes. Nat Commun 7:11929 http://dx.doi.org/10.1038/ncomms11929. [PubMed]
5. Lu A, Magupalli VG, Ruan J, Yin Q, Atianand MK, Vos MR, Schröder GF, Fitzgerald KA, Wu H, Egelman EH. 2014. Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes. Cell 156:1193–1206 http://dx.doi.org/10.1016/j.cell.2014.02.008. [PubMed]
6. 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. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356:768–774 http://dx.doi.org/10.1038/356768a0. [PubMed]
7. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F. 2015. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526:660–665 http://dx.doi.org/10.1038/nature15514. [PubMed]
8. Kayagaki N, Stowe IB, Lee BL, O’Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, Wu J, Kummerfeld S, Zhang J, Lee WP, Snipas SJ, Salvesen GS, Morris LX, Fitzgerald L, Zhang Y, Bertram EM, Goodnow CC, Dixit VM. 2015. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526:666–671 http://dx.doi.org/10.1038/nature15541. [PubMed]
9. Sborgi L, Rühl S, Mulvihill E, Pipercevic J, Heilig R, Stahlberg H, Farady CJ, Müller DJ, Broz P, Hiller S. 2016. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J 35:1766–1778 http://dx.doi.org/10.15252/embj.201694696. [PubMed]
10. Aglietti RA, Estevez A, Gupta A, Ramirez MG, Liu PS, Kayagaki N, Ciferri C, Dixit VM, Dueber EC. 2016. GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc Natl Acad Sci USA 113:7858–7863 http://dx.doi.org/10.1073/pnas.1607769113. [PubMed]
11. Ding J, Wang K, Liu W, She Y, Sun Q, Shi J, Sun H, Wang DC, Shao F. 2016. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535:111–116. ERRATUM Nature 640:150 http://dx.doi.org/10.1038/nature18590. [PubMed]
12. Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG, Wu H, Lieberman J. 2016. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535:153–158 http://dx.doi.org/10.1038/nature18629. [PubMed]
13. Bergsbaken T, Fink SL, Cookson BT. 2009. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7:99–109 http://dx.doi.org/10.1038/nrmicro2070. [PubMed]
14. Evavold CL, Ruan J, Tan Y, Xia S, Wu H, Kagan JC. 2017. The pore-forming protein gasdermin D regulates interleukin-1 secretion from living macrophages. Immunity 48:35–44.e6. [PubMed]
15. Heilig R, Dick MS, Sborgi L, Meunier E, Hiller S, Broz P. 2017. The gasdermin-D pore acts as a conduit for IL-1β secretion in mice. Eur J Immunol 48:584–592. [PubMed]
16. Monteleone M, Stow JL, Schroder K. 2015. Mechanisms of unconventional secretion of IL-1 family cytokines. Cytokine 74:213–218 http://dx.doi.org/10.1016/j.cyto.2015.03.022. [PubMed]
17. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, Lee WP, Roose-Girma M, Erickson S, Dixit VM. 2004. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430:213–218 http://dx.doi.org/10.1038/nature02664. [PubMed]
18. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozören N, Jagirdar R, Inohara N, Vandenabeele P, Bertin J, Coyle A, Grant EP, Núñez G. 2006. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7:576–582 http://dx.doi.org/10.1038/ni1346. [PubMed]
19. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, Aderem A. 2006. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7:569–575 http://dx.doi.org/10.1038/ni1344. [PubMed]
20. Sutterwala FS, Mijares LA, Li L, Ogura Y, Kazmierczak BI, Flavell RA. 2007. Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J Exp Med 204:3235–3245 http://dx.doi.org/10.1084/jem.20071239. [PubMed]
21. Suzuki T, Franchi L, Toma C, Ashida H, Ogawa M, Yoshikawa Y, Mimuro H, Inohara N, Sasakawa C, Nuñez G. 2007. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog 3:e111 http://dx.doi.org/10.1371/journal.ppat.0030111. [PubMed]
22. Zamboni DS, Kobayashi KS, Kohlsdorf T, Ogura Y, Long EM, Vance RE, Kuida K, Mariathasan S, Dixit VM, Flavell RA, Dietrich WF, Roy CR. 2006. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat Immunol 7:318–325 http://dx.doi.org/10.1038/ni1305. [PubMed]
23. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE, Leaf IA, Aderem A. 2010. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 107:3076–3080 http://dx.doi.org/10.1073/pnas.0913087107. [PubMed]
24. Lightfield KL, Persson J, Brubaker SW, Witte CE, von Moltke J, Dunipace EA, Henry T, Sun YH, Cado D, Dietrich WF, Monack DM, Tsolis RM, Vance RE. 2008. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat Immunol 9:1171–1178 http://dx.doi.org/10.1038/ni.1646. [PubMed]
25. 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. [PubMed]
26. 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. [PubMed]
27. Yang J, Zhao Y, Shi J, Shao F. 2013. Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc Natl Acad Sci USA 110:14408–14413 http://dx.doi.org/10.1073/pnas.1306376110. [PubMed]
28. Suzuki S, Franchi L, He Y, Muñoz-Planillo R, Mimuro H, Suzuki T, Sasakawa C, Núñez G. 2014. Shigella type III secretion protein MxiI is recognized by Naip2 to induce Nlrc4 inflammasome activation independently of Pkcδ. PLoS Pathog 10:e1003926 http://dx.doi.org/10.1371/journal.ppat.1003926. [PubMed]
29. Kortmann J, Brubaker SW, Monack DM. 2015. Cutting edge: inflammasome activation in primary human macrophages is dependent on flagellin. J Immunol 195:815–819 http://dx.doi.org/10.4049/jimmunol.1403100. [PubMed]
30. Tenthorey JL, Kofoed EM, Daugherty MD, Malik HS, Vance RE. 2014. Molecular basis for specific recognition of bacterial ligands by NAIP/NLRC4 inflammasomes. Mol Cell 54:17–29 http://dx.doi.org/10.1016/j.molcel.2014.02.018. [PubMed]
31. Tenthorey JL, Haloupek N, López-Blanco JR, Grob P, Adamson E, Hartenian E, Lind NA, Bourgeois NM, Chacón P, Nogales E, Vance RE. 2017. The structural basis of flagellin detection by NAIP5: A strategy to limit pathogen immune evasion. Science 358:888–893 http://dx.doi.org/10.1126/science.aao1140. [PubMed]
32. Bürckstümmer T, Baumann C, Blüml S, Dixit E, Dürnberger G, Jahn H, Planyavsky M, Bilban M, Colinge J, Bennett KL, Superti-Furga G. 2009. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 10:266–272 http://dx.doi.org/10.1038/ni.1702. [PubMed]
33. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES. 2009. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458:509–513 http://dx.doi.org/10.1038/nature07710. [PubMed]
34. Fernandes-Alnemri T, Yu JW, Juliana C, Solorzano L, Kang S, Wu J, Datta P, McCormick M, Huang L, McDermott E, Eisenlohr L, Landel CP, Alnemri ES. 2010. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat Immunol 11:385–393 http://dx.doi.org/10.1038/ni.1859. [PubMed]
35. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, Caffrey DR, Latz E, Fitzgerald KA. 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514–518 http://dx.doi.org/10.1038/nature07725. [PubMed]
36. Rathinam VA, Jiang Z, Waggoner SN, Sharma S, Cole LE, Waggoner L, Vanaja SK, Monks BG, Ganesan S, Latz E, Hornung V, Vogel SN, Szomolanyi-Tsuda E, Fitzgerald KA. 2010. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol 11:395–402 http://dx.doi.org/10.1038/ni.1864. [PubMed]
37. Jones JW, Kayagaki N, Broz P, Henry T, Newton K, O’Rourke K, Chan S, Dong J, Qu Y, Roose-Girma M, Dixit VM, Monack DM. 2010. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc Natl Acad Sci USA 107:9771–9776 http://dx.doi.org/10.1073/pnas.1003738107. [PubMed]
38. Morrone SR, Matyszewski M, Yu X, Delannoy M, Egelman EH, Sohn J. 2015. Assembly-driven activation of the AIM2 foreign-dsDNA sensor provides a polymerization template for downstream ASC. Nat Commun 6:7827 http://dx.doi.org/10.1038/ncomms8827. [PubMed]
39. Sauer JD, Witte CE, Zemansky J, Hanson B, Lauer P, Portnoy DA. 2010. Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 7:412–419 http://dx.doi.org/10.1016/j.chom.2010.04.004. [PubMed]
40. Kim S, Bauernfeind F, Ablasser A, Hartmann G, Fitzgerald KA, Latz E, Hornung V. 2010. Listeria monocytogenes is sensed by the NLRP3 and AIM2 inflammasome. Eur J Immunol 40:1545–1551 http://dx.doi.org/10.1002/eji.201040425. [PubMed]
41. Wassermann R, Gulen MF, Sala C, Perin SG, Lou Y, Rybniker J, Schmid-Burgk JL, Schmidt T, Hornung V, Cole ST, Ablasser A. 2015. Mycobacterium tuberculosis differentially activates cGAS- and inflammasome-dependent intracellular immune responses through ESX-1. Cell Host Microbe 17:799–810 http://dx.doi.org/10.1016/j.chom.2015.05.003. [PubMed]
42. Saiga H, Kitada S, Shimada Y, Kamiyama N, Okuyama M, Makino M, Yamamoto M, Takeda K. 2012. Critical role of AIM2 in Mycobacterium tuberculosis infection. Int Immunol 24:637–644 http://dx.doi.org/10.1093/intimm/dxs062. [PubMed]
43. Marim FM, Franco MMC, Gomes MTR, Miraglia MC, Giambartolomei GH, Oliveira SC. 2017. The role of NLRP3 and AIM2 in inflammasome activation during Brucella abortus infection. Semin Immunopathol 39:215–223 http://dx.doi.org/10.1007/s00281-016-0581-1. [PubMed]
44. Cunha LD, Silva ALN, Ribeiro JM, Mascarenhas DPA, Quirino GFS, Santos LL, Flavell RA, Zamboni DS. 2017. AIM2 engages active but unprocessed caspase-1 to induce noncanonical activation of the NLRP3 inflammasome. Cell Reports 20:794–805 http://dx.doi.org/10.1016/j.celrep.2017.06.086. [PubMed]
45. Henry T, Brotcke A, Weiss DS, Thompson LJ, Monack DM. 2007. Type I interferon signaling is required for activation of the inflammasome during Francisella infection. J Exp Med 204:987–994 http://dx.doi.org/10.1084/jem.20062665. [PubMed]
46. Meunier E, Wallet P, Dreier RF, Costanzo S, Anton L, Rühl S, Dussurgey S, Dick MS, Kistner A, Rigard M, Degrandi D, Pfeffer K, Yamamoto M, Henry T, Broz P. 2015. Guanylate-binding proteins promote activation of the AIM2 inflammasome during infection with Francisella novicida. Nat Immunol 16:476–484 http://dx.doi.org/10.1038/ni.3119. [PubMed]
47. Man SM, Karki R, Malireddi RK, Neale G, Vogel P, Yamamoto M, Lamkanfi M, Kanneganti TD. 2015. The transcription factor IRF1 and guanylate-binding proteins target activation of the AIM2 inflammasome by Francisella infection. Nat Immunol 16:467–475 http://dx.doi.org/10.1038/ni.3118. [PubMed]
48. Meunier E, Broz P. 2016. Interferon-inducible GTPases in cell autonomous and innate immunity. Cell Microbiol 18:168–180 http://dx.doi.org/10.1111/cmi.12546. [PubMed]
49. Man SM, Karki R, Sasai M, Place DE, Kesavardhana S, Temirov J, Frase S, Zhu Q, Malireddi RKS, Kuriakose T, Peters JL, Neale G, Brown SA, Yamamoto M, Kanneganti T-D. 2016. IRGB10 liberates bacterial ligands for sensing by the AIM2 and caspase-11-NLRP3 inflammasomes. Cell 167:382–396.e17 http://dx.doi.org/10.1016/j.cell.2016.09.012. [PubMed]
50. Piro AS, Hernandez D, Luoma S, Feeley EM, Finethy R, Yirga A, Frickel EM, Lesser CF, Coers J. 2017. Detection of cytosolic Shigella flexneri via a C-terminal triple-arginine motif of GBP1 inhibits actin-based motility. mBio 8:e01979-17 http://dx.doi.org/10.1128/mBio.01979-17. [PubMed]
51. Wandel MP, Pathe C, Werner EI, Ellison CJ, Boyle KB, von der Malsburg A, Rohde J, Randow F. 2017. GBPs inhibit motility of Shigella flexneri but are targeted for degradation by the bacterial ubiquitin ligase IpaH9.8. Cell Host Microbe 22:507–518.e5 http://dx.doi.org/10.1016/j.chom.2017.09.007. [PubMed]
52. Li P, Jiang W, Yu Q, Liu W, Zhou P, Li J, Xu J, Xu B, Wang F, Shao F. 2017. Ubiquitination and degradation of GBPs by a Shigella effector to suppress host defence. Nature 551:378–383.
53. 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. [PubMed]
54. Zhong FL, Mamai O, Sborgi L, Boussofara L, Hopkins R, Robinson K, Szeverenyi I, Takeichi T, Balaji R, Lau A, Tye H, Roy K, Bonnard C, Ahl PJ, Jones LA, Baker P, Lacina L, Otsuka A, Fournie PR, Malecaze F, Lane EB, Akiyama M, Kabashima K, Connolly JE, Masters SL, Soler VJ, Omar SS, McGrath JA, Nedelcu R, Gribaa M, Denguezli M, Saad A, Hiller S, Reversade B. 2016. Germline NLRP1 mutations cause skin inflammatory and cancer susceptibility syndromes via inflammasome activation. Cell 167:187–202 e17.
55. 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. [PubMed]
56. Hellmich KA, Levinsohn JL, Fattah R, Newman ZL, Maier N, Sastalla I, Liu S, Leppla SH, Moayeri M. 2012. Anthrax lethal factor cleaves mouse nlrp1b in both toxin-sensitive and toxin-resistant macrophages. PLoS One 7:e49741 http://dx.doi.org/10.1371/journal.pone.0049741. [PubMed]
57. Chavarría-Smith J, Vance RE. 2013. Direct proteolytic cleavage of NLRP1B is necessary and sufficient for inflammasome activation by anthrax lethal factor. PLoS Pathog 9:e1003452 http://dx.doi.org/10.1371/journal.ppat.1003452. [PubMed]
58. Wang G, Roux B, Feng F, Guy E, Li L, Li N, Zhang X, Lautier M, Jardinaud M-F, Chabannes M, Arlat M, Chen S, He C, Noël LD, Zhou J-M. 2015. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18:285–295 http://dx.doi.org/10.1016/j.chom.2015.08.004. [PubMed]
59. van der Hoorn RA, Kamoun S. 2008. From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017 http://dx.doi.org/10.1105/tpc.108.060194. [PubMed]
60. Bernot A, Clepet C, Dasilva C, Devaud C, Petit J-L, Caloustian C, Cruaud C, Samson D, Pulcini F, Weissenbach J, Heilig R, Notanicola C, Domingo C, Rozenbaum M, Benchetrit E, Topaloglu R, Dewalle M, Dross C, Hadjari P, Dupont M, Demaille J, Touitou I, Smaoui N, Nedelec B, Méry J-P, Chaabouni H, Delpech M, Grateau G, French FMF Consortium. 1997. A candidate gene for familial Mediterranean fever. Nat Genet 17:25–31 http://dx.doi.org/10.1038/ng0997-25. [PubMed]
61. Chae JJ, Cho YH, Lee GS, Cheng J, Liu PP, Feigenbaum L, Katz SI, Kastner DL. 2011. Gain-of-function pyrin mutations induce NLRP3 protein-independent interleukin-1β activation and severe autoinflammation in mice. Immunity 34:755–768 http://dx.doi.org/10.1016/j.immuni.2011.02.020. [PubMed]
62. Xu H, Yang J, Gao W, Li L, Li P, Zhang L, Gong YN, Peng X, Xi JJ, Chen S, Wang F, Shao F. 2014. Innate immune sensing of bacterial modifications of Rho GTPases by the pyrin inflammasome. Nature 513:237–241 http://dx.doi.org/10.1038/nature13449. [PubMed]
63. Gao W, Yang J, Liu W, Wang Y, Shao F. 2016. Site-specific phosphorylation and microtubule dynamics control pyrin inflammasome activation. Proc Natl Acad Sci USA 113:E4857–E4866 http://dx.doi.org/10.1073/pnas.1601700113. [PubMed]
64. Park YH, Wood G, Kastner DL, Chae JJ. 2016. Pyrin inflammasome activation and RhoA signaling in the autoinflammatory diseases FMF and HIDS. Nat Immunol 17:914–921 http://dx.doi.org/10.1038/ni.3457. [PubMed]
65. Heilig R, Broz P. 2018. Function and mechanism of the pyrin inflammasome. Eur J Immunol 48:230–238 http://dx.doi.org/10.1002/eji.201746947. [PubMed]
66. 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. [PubMed]
67. Stutz A, Kolbe C-C, Stahl R, Horvath GL, Franklin BS, van Ray O, Brinkschulte R, Geyer M, Meissner F, Latz E. 2017. NLRP3 inflammasome assembly is regulated by phosphorylation of the pyrin domain. J Exp Med 214:1725–1736 http://dx.doi.org/10.1084/jem.20160933. [PubMed]
68. Song N, Liu Z-S, Xue W, Bai Z-F, Wang Q-Y, Dai J, Liu X, Huang Y-J, Cai H, Zhan X-Y, Han Q-Y, Wang H, Chen Y, Li H-Y, Li A-L, Zhang X-M, Zhou T, Li T. 2017. NLRP3 phosphorylation is an essential priming event for inflammasome activation. Mol Cell 68:185–197.e6 http://dx.doi.org/10.1016/j.molcel.2017.08.017. [PubMed]
69. Juliana C, Fernandes-Alnemri T, Kang S, Farias A, Qin F, Alnemri ES. 2012. Non-transcriptional priming and deubiquitination regulate NLRP3 inflammasome activation. J Biol Chem 287:36617–36622 http://dx.doi.org/10.1074/jbc.M112.407130. [PubMed]
70. Py BF, Kim MS, Vakifahmetoglu-Norberg H, Yuan J. 2013. Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity. Mol Cell 49:331–338 http://dx.doi.org/10.1016/j.molcel.2012.11.009. [PubMed]
71. Muñoz-Planillo R, Kuffa P, Martínez-Colón G, Smith BL, Rajendiran TM, Núñez G. 2013. K + efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity 38:1142–1153 http://dx.doi.org/10.1016/j.immuni.2013.05.016. [PubMed]
72. 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. [PubMed]
73. Baker PJ, Boucher D, Bierschenk D, Tebartz C, Whitney PG, D’Silva DB, Tanzer MC, Monteleone M, Robertson AA, Cooper MA, Alvarez-Diaz S, Herold MJ, Bedoui S, Schroder K, Masters SL. 2015. NLRP3 inflammasome activation downstream of cytoplasmic LPS recognition by both caspase-4 and caspase-5. Eur J Immunol 45:2918–2926 http://dx.doi.org/10.1002/eji.201545655. [PubMed]
74. Schmid-Burgk JL, Gaidt MM, Schmidt T, Ebert TS, Bartok E, Hornung V. 2015. Caspase-4 mediates non-canonical activation of the NLRP3 inflammasome in human myeloid cells. Eur J Immunol 45:2911–2917 http://dx.doi.org/10.1002/eji.201545523. [PubMed]
75. Rühl S, Broz P. 2015. Caspase-11 activates a canonical NLRP3 inflammasome by promoting K + efflux. Eur J Immunol 45:2927–2936 http://dx.doi.org/10.1002/eji.201545772. [PubMed]
76. Broz P, Ruby T, Belhocine K, Bouley DM, Kayagaki N, Dixit VM, Monack DM. 2012. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490:288–291 http://dx.doi.org/10.1038/nature11419. [PubMed]
77. Rathinam VA, Vanaja SK, Waggoner L, Sokolovska A, Becker C, Stuart LM, Leong JM, Fitzgerald KA. 2012. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 150:606–619 http://dx.doi.org/10.1016/j.cell.2012.07.007. [PubMed]
78. Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, Miyake K, Zhang J, Lee WP, Muszynski A, Forsberg LS, Carlson RW, Dixit VM. 2013. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341:1246–1249. [PubMed]
79. Hagar JA, Powell DA, Aachoui Y, Ernst RK, Miao EA. 2013. Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341:1250–1253 http://dx.doi.org/10.1126/science.1240988. [PubMed]
80. Shi J, Zhao Y, Wang Y, Gao W, Ding J, Li P, Hu L, Shao F. 2014. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514:187–192 http://dx.doi.org/10.1038/nature13683. [PubMed]
81. Beutler B, Jiang Z, Georgel P, Crozat K, Croker B, Rutschmann S, Du X, Hoebe K. 2006. Genetic analysis of host resistance: toll-like receptor signaling and immunity at large. Annu Rev Immunol 24:353–389 http://dx.doi.org/10.1146/annurev.immunol.24.021605.090552. [PubMed]
82. Meunier E, Dick MS, Dreier RF, Schürmann N, Kenzelmann Broz D, Warming S, Roose-Girma M, Bumann D, Kayagaki N, Takeda K, Yamamoto M, Broz P. 2014. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 509:366–370 http://dx.doi.org/10.1038/nature13157. [PubMed]
83. Pilla DM, Hagar JA, Haldar AK, Mason AK, Degrandi D, Pfeffer K, Ernst RK, Yamamoto M, Miao EA, Coers J. 2014. Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proc Natl Acad Sci USA 111:6046–6051 http://dx.doi.org/10.1073/pnas.1321700111. [PubMed]
84. Santos JC, Dick MS, Lagrange B, Degrandi D, Pfeffer K, Yamamoto M, Meunier E, Pelczar P, Henry T, Broz P. 2018. LPS targets host guanylate-binding proteins to the bacterial outer membrane for non-canonical inflammasome activation. EMBO J 37:e98089 http://dx.doi.org/10.15252/embj.201798089. [PubMed]
85. Finethy R, Luoma S, Orench-Rivera N, Feeley EM, Haldar AK, Yamamoto M, Kanneganti T-D, Kuehn MJ, Coers J. 2017. Inflammasome activation by bacterial outer membrane vesicles requires guanylate binding proteins. mBio 8:e01188-17 http://dx.doi.org/10.1128/mBio.01188-17. [PubMed]
86. Gu L, Meng R, Tang Y, Zhao K, Liang F, Zhang R, Xue Q, Chen F, Xiao X, Wang H, Wang H, Billiar TR, Lu B. 2018. Toll like receptor 4 signaling licenses the cytosolic transport of lipopolysaccharide from bacterial outer membrane vesicles. Shock 51:256–265. [PubMed]
87. Lagrange B, Benaoudia S, Wallet P, Magnotti F, Provost A, Michal F, Martin A, Di Lorenzo F, Py BF, Molinaro A, Henry T. 2018. Human caspase-4 detects tetra-acylated LPS and cytosolic Francisella and functions differently from murine caspase-11. Nat Commun 9:242 http://dx.doi.org/10.1038/s41467-017-02682-y. [PubMed]
88. Vanaja SK, Russo AJ, Behl B, Banerjee I, Yankova M, Deshmukh SD, Rathinam VAK. 2016. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation. Cell 165:1106–1119 http://dx.doi.org/10.1016/j.cell.2016.04.015. [PubMed]
89. Zychlinsky A, Prevost MC, Sansonetti PJ. 1992. Shigella flexneri induces apoptosis in infected macrophages. Nature 358:167–169 http://dx.doi.org/10.1038/358167a0. [PubMed]
90. Fink SL, Bergsbaken T, Cookson BT. 2008. Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci USA 105:4312–4317 http://dx.doi.org/10.1073/pnas.0707370105. [PubMed]
91. 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. [PubMed]
92. Jorgensen I, Zhang Y, Krantz BA, Miao EA. 2016. Pyroptosis triggers pore-induced intracellular traps (PITs) that capture bacteria and lead to their clearance by efferocytosis. J Exp Med 213:2113–2128 http://dx.doi.org/10.1084/jem.20151613. [PubMed]
93. Jorgensen I, Lopez JP, Laufer SA, Miao EA. 2016. IL-1β, IL-18, and eicosanoids promote neutrophil recruitment to pore-induced intracellular traps following pyroptosis. Eur J Immunol 46:2761–2766 http://dx.doi.org/10.1002/eji.201646647. [PubMed]
94. Thurston TL, Matthews SA, Jennings E, Alix E, Shao F, Shenoy AR, Birrell MA, Holden DW. 2016. Growth inhibition of cytosolic Salmonella by caspase-1 and caspase-11 precedes host cell death. Nat Commun 7:13292 http://dx.doi.org/10.1038/ncomms13292. [PubMed]
95. Sellin ME, Müller AA, Felmy B, Dolowschiak T, Diard M, Tardivel A, Maslowski KM, Hardt WD. 2014. Epithelium-intrinsic NAIP/NLRC4 inflammasome drives infected enterocyte expulsion to restrict Salmonella replication in the intestinal mucosa. Cell Host Microbe 16:237–248. http://dx.doi.org/10.1016/j.chom.2014.07.001. [PubMed]
96. Knodler LA, Crowley SM, Sham HP, Yang H, Wrande M, Ma C, Ernst RK, Steele-Mortimer O, Celli J, Vallance BA. 2014. Noncanonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe 16:249–256 http://dx.doi.org/10.1016/j.chom.2014.07.002. [PubMed]
97. Rauch I, Deets KA, Ji DX, von Moltke J, Tenthorey JL, Lee AY, Philip NH, Ayres JS, Brodsky IE, Gronert K, Vance RE. 2017. NAIP-NLRC4 inflammasomes coordinate intestinal epithelial cell expulsion with eicosanoid and IL-18 release via activation of caspase-1 and -8. Immunity 46:649–659 http://dx.doi.org/10.1016/j.immuni.2017.03.016. [PubMed]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.BAI-0003-2019
2019-03-08
2019-10-14

Abstract:

Inflammasomes are multiprotein signaling complexes that are assembled by cytosolic sensors upon the detection of infectious or noxious stimuli. These complexes activate inflammatory caspases to induce host cell death and cytokine secretion and are an essential part of antimicrobial host defense. In this review, I discuss how intracellular bacteria are detected by inflammasomes, how the specific sensing mechanism of each inflammasome receptor restricts the ability of bacteria to evade immune recognition, and how host cell death is used to control bacterial replication .

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Recognition of Intracellular Bacteria by Inflammasomes
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.BAI-0003-2019-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.BAI-0003-2019-1,properties={foaf_givenname=Petr, foaf_name=Petr Broz, foaf_surname=Broz, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.BAI-0003-2019-aff1]]}]]
Citation: Broz P. 2019. Recognition of intracellular bacteria by inflammasomes. microbiolspec 7(2): doi:10.1128/microbiolspec.BAI-0003-2019
/content/microbiolspec/10.1128/microbiolspec.BAI-0003-2019.fig1
FIGURE 1
Activation of canonical and noncanonical inflammasomes by bacteria. () Inflammasome receptors use different recognition mechanisms to sense bacterial infections. The NAIP-NLRC4 and AIM2 pathways involve direct binding of the respective ligands (flagellin, T3SS structural proteins, or DNA). Nlrp1b recognizes the proteolytic activity of the metalloprotease lethal factor from by serving as a decoy substrate. Pyrin uses a guard mechanism to detect the inactivation of RhoA. The kinase activities of RhoA and PNK1/2 are required to keep pyrin in an inactive state, in which it is phosphorylated and bound by 14-3-3 proteins. NLRP3 activation involves priming by signal 1, followed by activation by signal 2. The nature of signal 2 and the mechanism of recognition are yet unknown, but they are linked to membrane permeabilization, K efflux, and mitochondrial dysfunction. The noncanonical pathway involves direct detection of LPS by caspase-11 in mice or caspase-4 (or caspase-5) in humans. () Following activation, inflammasome receptors oligomerize and recruit the bipartite adaptor ASC, which forms long filaments that cluster to form the ASC speck. Pro-caspase-1 is recruited to the filaments by CARD-CARD interaction and activated by dimerization and autoproteolysis. () Active caspase-1 and caspase-11 process GSDMD, removing the regulatory C-terminal domain and unleashing the cytotoxic activity of the N-terminal fragment. The GSDMD N terminus is inserted into the plasma membrane and forms large pores, which disrupt the electrochemical gradient and induce pyroptosis. Caspase-1 also processes IL-1 family cytokines (like IL-1b) and promotes their release from cells in a pathway that is at least partially GSDMD dependent.
microbiolspec/7/2/BAI-0003-2019-fig1_thmb.gif
microbiolspec/7/2/BAI-0003-2019-fig1.gif
Image of FIGURE 1
FIGURE 1

Activation of canonical and noncanonical inflammasomes by bacteria. () Inflammasome receptors use different recognition mechanisms to sense bacterial infections. The NAIP-NLRC4 and AIM2 pathways involve direct binding of the respective ligands (flagellin, T3SS structural proteins, or DNA). Nlrp1b recognizes the proteolytic activity of the metalloprotease lethal factor from by serving as a decoy substrate. Pyrin uses a guard mechanism to detect the inactivation of RhoA. The kinase activities of RhoA and PNK1/2 are required to keep pyrin in an inactive state, in which it is phosphorylated and bound by 14-3-3 proteins. NLRP3 activation involves priming by signal 1, followed by activation by signal 2. The nature of signal 2 and the mechanism of recognition are yet unknown, but they are linked to membrane permeabilization, K efflux, and mitochondrial dysfunction. The noncanonical pathway involves direct detection of LPS by caspase-11 in mice or caspase-4 (or caspase-5) in humans. () Following activation, inflammasome receptors oligomerize and recruit the bipartite adaptor ASC, which forms long filaments that cluster to form the ASC speck. Pro-caspase-1 is recruited to the filaments by CARD-CARD interaction and activated by dimerization and autoproteolysis. () Active caspase-1 and caspase-11 process GSDMD, removing the regulatory C-terminal domain and unleashing the cytotoxic activity of the N-terminal fragment. The GSDMD N terminus is inserted into the plasma membrane and forms large pores, which disrupt the electrochemical gradient and induce pyroptosis. Caspase-1 also processes IL-1 family cytokines (like IL-1b) and promotes their release from cells in a pathway that is at least partially GSDMD dependent.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0003-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.BAI-0003-2019.fig2
FIGURE 2
Antimicrobial effects of pyroptosis. () Activation of canonical or noncanonical inflammasomes in infected phagocytes results in the formation of GSDMD pores and pyroptosis. Intracellular bacteria are trapped within pyroptotic cell bodies, called PITs. GSDMD pores can potentially also damage intracellular bacteria. PITs are recognized and efferocytosed by neutrophils, which efficiently kill PIT-associated bacteria. () Engagement of pyroptosis in IECs promotes the expulsion of pyroptotic cells from the epithelial cell layer into the gut lumen. Any associated bacteria are removed with the dying cells and expelled from the intestines.
microbiolspec/7/2/BAI-0003-2019-fig2_thmb.gif
microbiolspec/7/2/BAI-0003-2019-fig2.gif
Image of FIGURE 2
FIGURE 2

Antimicrobial effects of pyroptosis. () Activation of canonical or noncanonical inflammasomes in infected phagocytes results in the formation of GSDMD pores and pyroptosis. Intracellular bacteria are trapped within pyroptotic cell bodies, called PITs. GSDMD pores can potentially also damage intracellular bacteria. PITs are recognized and efferocytosed by neutrophils, which efficiently kill PIT-associated bacteria. () Engagement of pyroptosis in IECs promotes the expulsion of pyroptotic cells from the epithelial cell layer into the gut lumen. Any associated bacteria are removed with the dying cells and expelled from the intestines.

Source: microbiolspec March 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.BAI-0003-2019
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error