Skip to main content
Log in

Inactivation of inflammasomes by pathogens regulates inflammation

Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Inflammatory response is initiated and sustained by the action of quintessential pro-inflammatory cytokines of immune system namely IL-1β and IL-18. The maturation process of those cytokines is ensured by caspase-1 enzymatic activity, that is in turn is tightly controlled by multiprotein complexes called inflammasomes. Inflammasomes are activated in cells of innate immune system in response to recognition of conservative parts of microbes (pathogen-associated molecular patterns) or by sensing molecular signs of tissue damage (damage-associated molecular patterns). Inflammasome activation apart of cytokines secretion leads to pro-inflammatory cell death, so-called pyroptosis. That culminates in release of cytoplasmatic content of cells including cytokines and alarmins that boost immune response against pathogens, as well as pyroptosis destroys replicative niches of intracellular pathogens. During co-evolution with the host, bacterial and viral pathogens developed a range of molecular inhibitors targeting each step of inflammasome activation. In current review, we will discuss the latest knowledge of inflammasomes’ signaling pathways and tricks that pathogens use to avoid immune recognition and clearance. Our better understanding of inflammasome inhibition by pathogens can lead to better therapeutic approaches for the treatment of infectious diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Abbreviations

Alarmins:

(or DAMPs) are endogenous molecules that are released upon tissue damage and activate innate immunity. The best-characterized alarmins are heat shock proteins (HSP), HMGB1, purine metabolites, adenosine diphosphate, uric acid crystals, etc.

Inflammation:

is an immune response towards PAMPs and DAMPs that is mediated by proinflammatory cytokines IL-1β, IL-18, TNF, and IL-8, which is aiming to restrict dissemination and eventually eliminate pathogens

Immune evasion:

is a strategy used by pathogenic organisms to evade a host’s immune response to maximize their probability of being transmitted to a fresh host or to continue growing

Inflammasomes:

are large cytosolic complexes assembled by cytosolic receptors (NLR, AIM, PYRIN) in response to PAMPs and DAMPs that activate caspase-1 and -11 resulting in the production of pro-inflammatory cytokines IL-1β and IL-18 as well as in pyroptotic cell death

Damage-associated molecular patterns:

(DAMPs) are endogenous molecules released by stressed, damaged, or dying cells, which activate PRR and initiate a noninfectious inflammatory response

Pathogen-associated molecular patterns:

(PAMPs) are conservative molecular features of pathogens recognized by the innate immune system

Pattern recognition receptors:

(PRRs) are germ line encoded receptors of the innate immune system, located on the plasma membrane, endosomal membrane, or in cytosol, that detect and respond to exogenous and endogenous stress signals

Pyroptosis:

is a proinflammatory type of cell death characterized by formation of large pores in the cellular membranes and release of cytosolic contents that contains processed IL-1β and IL-18 and other bioactive substances (e.g. alarmins), as well as intracellular pathogens

NOD-like receptors:

(NLRs) represent a large family of intracellular PRRs characterized by the presence of a centrally located nucleotide binding and oligomerization domain (referred to as NBD; NOD or NACHT domain) and carboxy-terminal leucinerich repeats (LRRs). A subset of NLRs can assemble “inflammasomes”

Toll-like receptors:

(TLRs) are membrane-bound PRRs that recognize PAMPs and DAMPs at the cell surface and inside of the endosomes in different cell types; activation of TLR signaling pathways induces expression of inflammatory and antiviral genes

References

  1. Janeway, C. A., (1988) Frontiers of the immune system, Nature, 333, 804–806.

    Article  PubMed  Google Scholar 

  2. Medzhitov, R. (2008) Origin and physiological roles of inflammation, Nature, 454, 428–435.

    Article  CAS  PubMed  Google Scholar 

  3. Kumar, H., Kawai, T., and Akira, S. (2009) Pathogen recognition in the innate immune response, Biochem. J., 420, 1–16.

    Article  CAS  PubMed  Google Scholar 

  4. Murphy, K. W. (2017) Janeway’s immunobiology, in Janeway’s Immunobiology, 9th Edn., Garland Science/Taylor & Francis Group, New York, pp. 35–54.

    Google Scholar 

  5. Medzhitov, R. (2013) Pattern recognition theory and the launch of modern innate immunity, J. Immunol., 191, 4473–4474.

    Article  CAS  PubMed  Google Scholar 

  6. Matzinger, P. (2002) The danger model: a renewed sense of self, Science, 296, 301–305.

    Article  CAS  PubMed  Google Scholar 

  7. Barton, G. M., and Medzhitov, R. (2003) Toll-like receptor signaling pathways, Science, 300, 1524–1525.

    Article  CAS  PubMed  Google Scholar 

  8. Van Gorp, H., Kuchmiy, A., Van Hauwermeiren, F., and Lamkanfi, M. (2014) NOD-like receptors interfacing the immune and reproductive systems, FEBS J., 281, 45684582.

    Google Scholar 

  9. Takeuchi, O., and Akira, S. (2010) Pattern recognition receptors and inflammation, Cell, 140, 805–820.

    Article  CAS  PubMed  Google Scholar 

  10. Drickamer, K., and Taylor, M. E. (2015) Recent insights into structures and functions of C-type lectins in the immune system, Curr. Opin. Struct. Biol., 34, 26–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lamkanfi, M., and Dixit, V. M. (2014) Mechanisms and functions of inflammasomes, Cell, 157, 1013–1022.

    Article  CAS  PubMed  Google Scholar 

  12. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., Taira, K., Akira, S., and Fujita, T. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses, Nat. Immunol., 5, 730–737.

    Article  CAS  PubMed  Google Scholar 

  13. Hornung, V., Ablasser, A., Charrel-Dennis, M., Bauernfeind, F., Horvath, G., Caffrey, D. R., Latz, E., and Fitzgerald, K. A. (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC, Nature, 458, 514–518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hornung, V., Hartmann, R., Ablasser, A., and Hopfner, K. P. (2014) OAS proteins and cGAS: unifying concepts in sensing and responding to cytosolic nucleic acids, Nat. Rev. Immunol., 14, 521–528.

    Article  CAS  PubMed  Google Scholar 

  15. Hornung, V., and Latz, E. (2010) Intracellular DNA recognition, Nat. Rev. Immunol., 10, 123–130.

    Article  CAS  PubMed  Google Scholar 

  16. Schroder, K., and Tschopp, J. (2010) The inflammasomes, Cell, 140, 821–832.

    Article  CAS  PubMed  Google Scholar 

  17. Nedospasov, S. (2012) Innate Immunity and Its Mechanisms [in Russian], Nauchnyi Mir, Moscow, pp. 21–23.

    Google Scholar 

  18. Zhang, P., Dixon, M., Zucchelli, M., Hambiliki, F., Levkov, L., Hovatta, O., and Kere, J. (2008) Expression analysis of the NLRP gene family suggests a role in human preimplantation development, PLoS One, 3, e2755.

    Article  CAS  Google Scholar 

  19. Kufer, T. A., and Sansonetti, P. J. (2011) NLR functions beyond pathogen recognition, Nat. Immunol., 12, 121–128.

    Article  CAS  PubMed  Google Scholar 

  20. Ting, J. P., Lovering, R. C., Alnemri, E. S., Bertin, J., Boss, J. M., Davis, B. K., Flavell, R. A., Girardin, S. E., Godzik, A., Harton, J. A., Hoffman, H. M., Hugot, J. P., Inohara, N., Mackenzie, A., Maltais, L. J., Nunez, G., Ogura, Y., Otten, L. A., Philpott, D., Reed, J. C., Reith, W., Schreiber, S., Steimle, V., and Ward, P. A. (2008) The NLR gene family: a standard nomenclature, Immunity, 28, 285–287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Xu, H., Yang, J., Gao, W., Li, L., Li, P., Zhang, L., Gong, Y. N., Peng, X., Xi, J. J., Chen, S., Wang, F., and Shao, F. (2014) Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome, Nature, 513, 237–241.

    Article  CAS  PubMed  Google Scholar 

  22. Dinarello, C. A. (2009) Immunological and inflammatory functions of the interleukin-1 family, Annu. Rev. Immunol., 27, 519–550.

    Article  CAS  PubMed  Google Scholar 

  23. Liu, T., Yamaguchi, Y., Shirasaki, Y., Shikada, K., Yamagishi, M., Hoshino, K., Kaisho, T., Takemoto, K., Suzuki, T., Kuranaga, E., Ohara, O., and Miura, M. (2014) Single-cell imaging of caspase-1 dynamics reveals an allor-none inflammasome signaling response, Cell Rep., 8, 974–982.

    Article  CAS  PubMed  Google Scholar 

  24. De Vasconcelos, N. M., Van Opdenbosch, N., and Lamkanfi, M. (2016) Inflammasomes as polyvalent cell death platforms, Cell. Mol. Life Sci., 73, 2335–2347.

    Article  PubMed  CAS  Google Scholar 

  25. Aachoui, Y., Leaf, I. A., Hagar, J. A., Fontana, M. F., Campos, C. G., Zak, D. E., Tan, M. H., Cotter, P. A., Vance, R. E., Aderem, A., and Miao, E. A. (2013) Caspase11 protects against bacteria that escape the vacuole, Science, 339, 975–978.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ceballos-Olvera, I., Sahoo, M., Miller, M. A., Barrio, L. D., and Re, F. (2011) Inflammasome-dependent pyroptosis and IL-18 protect against Burkholderia pseudomallei lung infection while IL-1ß is deleterious, PLoS Pathog., 7, e1002452.

    Article  CAS  Google Scholar 

  27. Kayagaki, N., Stowe, I. B., Lee, B. L., O’Rourke, K., Anderson, K., Warming, S., Cuellar, T., Haley, B., Roose-Girma, M., Phung, Q. T., Liu, P. S., Lill, J. R., Li, H., Wu, J., Kummerfeld, S., Zhang, J., Lee, W. P., Snipas, S. J., Salvesen, G. S., Morris, L. X., Fitzgerald, L., Zhang, Y., Bertram, E. M., Goodnow, C. C., and Dixit, V. M. (2015) Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling, Nature, 526, 666–671.

    Article  CAS  PubMed  Google Scholar 

  28. Ding, J., Wang, K., Liu, W., She, Y., Sun, Q., Shi, J., Sun, H., Wang, D. C., and Shao, F. (2016) Pore-forming activity and structural autoinhibition of the gasdermin family, Nature, 535, 111–116.

    Article  CAS  PubMed  Google Scholar 

  29. Gaidt, M. M., Ebert, T. S., Chauhan, D., Schmidt, T., Schmid-Burgk, J. L., Rapino, F., Robertson, A. A., Cooper, M. A., Graf, T., and Hornung, V. (2016) Human monocytes engage an alternative inflammasome pathway, Immunity, 44, 833–846.

    Article  CAS  PubMed  Google Scholar 

  30. Zanoni, I., Tan, Y., Di Gioia, M., Broggi, A., Ruan, J., Shi, J., Donado, C. A., Shao, F., Wu, H., Springstead, J. R., and Kagan, J. C. (2016) An endogenous caspase-11 ligand elicits interleukin-1 release from living dendritic cells, Science, 352, 1232–1236.

    Article  CAS  PubMed  Google Scholar 

  31. Chen, K. W., Gross, C. J., Sotomayor, F. V., Stacey, K. J., Tschopp, J., Sweet, M. J., and Schroder, K. (2014) The neutrophil NLRC4 inflammasome selectively promotes IL1beta maturation without pyroptosis during acute Salmonella challenge, Cell Rep., 8, 570–582.

    Article  CAS  PubMed  Google Scholar 

  32. Sellin, M. E., Muller, A. A., Felmy, B., Dolowschiak, T., Diard, M., Tardivel, A., Maslowski, K. M., and Hardt, W. D. (2014) Epithelium-intrinsic NAIP/NLRC4 inflammasome drives infected enterocyte expulsion to restrict Salmonella replication in the intestinal mucosa, Cell Host Microbe, 16, 237–248.

    Article  CAS  PubMed  Google Scholar 

  33. Saavedra, P. H., Demon, D., Van Gorp, H., and Lamkanfi, M. (2015) Protective and detrimental roles of inflammasomes in disease, Semin. Immunopathol., 37, 313–322.

    Article  CAS  PubMed  Google Scholar 

  34. Lu, A., Magupalli, V. G., Ruan, J., Yin, Q., Atianand, M. K., Vos, M. R., Schroder, G. F., Fitzgerald, K. A., Wu, H., and Egelman, E. H. (2014) Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes, Cell, 156, 1193–1206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Case, C. L., and Roy, C. R. (2011) Asc modulates the function of NLRC4 in response to infection of macrophages by Legionella pneumophila, MBio, 2, pii: e00117-11.

  36. Van Opdenbosch, N., Gurung, P., Van De Walle, L., Fossoul, A., Kanneganti, T. D., and Lamkanfi, M. (2014) Activation of the NLRP1b inflammasome independently of ASC-mediated caspase-1 autoproteolysis and speck formation, Nat. Commun., 5, 3209.

    PubMed  PubMed Central  Google Scholar 

  37. Chavarria-Smith, J., and Vance, R. E. (2015) The NLRP1 inflammasomes, Immunol. Rev., 265, 22–34.

    Article  CAS  PubMed  Google Scholar 

  38. Agostini, L., Martinon, F., Burns, K., McDermott, M. F., Hawkins, P. N., and Tschopp, J. (2004) NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder, Immunity, 20, 319–325.

    Article  CAS  PubMed  Google Scholar 

  39. Kagan, J. C. (2014) Common mechanisms activate plant guard receptors and TLR4, Trends Immunol., 35, 454–456.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Py, B. F., Kim, M. S., Vakifahmetoglu-Norberg, H., and Yuan, J. (2013) Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity, Mol. Cell, 49, 331–338.

    Article  CAS  PubMed  Google Scholar 

  41. Schmid-Burgk, J. L., Chauhan, D., Schmidt, T., Ebert, T. S., Reinhardt, J., Endl, E., and Hornung, V. (2016) A genome-wide CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats) screen identifies NEK7 as an essential component of NLRP3 inflammasome activation, J. Biol. Chem., 291, 103–109.

    Article  CAS  PubMed  Google Scholar 

  42. Shi, H., Wang, Y., Li, X., Zhan, X., Tang, M., Fina, M., Su, L., Pratt, D., Bu, C. H., Hildebrand, S., Lyon, S., Scott, L., Quan, J., Sun, Q., Russell, J., Arnett, S., Jurek, P., Chen, D., Kravchenko, V. V., Mathison, J. C., Moresco, E. M., Monson, N. L., Ulevitch, R. J., and Beutler, B. (2016) NLRP3 activation and mitosis are mutually exclusive events coordinated by NEK7, a new inflammasome component, Nat. Immunol., 17, 250–258.

    Article  CAS  PubMed  Google Scholar 

  43. Fernandes-Alnemri, T., Kang, S., Anderson, C., Sagara, J., Fitzgerald, K. A., and Alnemri, E. S. (2013) Cutting edge: TLR signaling licenses IRAK1 for rapid activation of the NLRP3 inflammasome, J. Immunol., 191, 3995–3999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kayagaki, N., Wong, M. T., Stowe, I. B., Ramani, S. R., Gonzalez, L. C., Akashi-Takamura, S., Miyake, K., Zhang, J., Lee, W. P., Muszynski, A., Forsberg, L. S., Carlson, R. W., and Dixit, V. M. (2013) Noncanonical inflammasome activation by intracellular LPS independent of TLR4, Science, 341, 1246–1249.

    Article  CAS  PubMed  Google Scholar 

  45. Shi, J., Zhao, Y., Wang, Y., Gao, W., Ding, J., Li, P., Hu, L., and Shao, F. (2014) Inflammatory caspases are innate immune receptors for intracellular LPS, Nature, 514, 187192.

    Article  CAS  Google Scholar 

  46. Lamkanfi, M., and Dixit, V. M. (2012) Inflammasomes and their roles in health and disease, Annu. Rev. Cell. Dev. Biol., 28, 137–161.

    Article  CAS  PubMed  Google Scholar 

  47. Miao, E. A., Mao, D. P., Yudkovsky, N., Bonneau, R., Lorang, C. G., Warren, S. E., Leaf, I. A., and Aderem, A. (2010) Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome, Proc. Natl. Acad. Sci. USA, 107, 3076–3080.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Matusiak, M., Van Opdenbosch, N., Van De Walle, L., Sirard, J. C., Kanneganti, T. D., and Lamkanfi, M. (2015) Flagellin-induced NLRC4 phosphorylation primes the inflammasome for activation by NAIP5, Proc. Natl. Acad. Sci. USA, 112, 1541–1546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Zhang, L., Chen, S., Ruan, J., Wu, J., Tong, A. B., Yin, Q., Li, Y., David, L., Lu, A., Wang, W. L., Marks, C., Ouyang, Q., Zhang, X., Mao, Y., and Wu, H. (2015) Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization, Science, 350, 404–409.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Elinav, E., Strowig, T., Kau, A. L., Henao-Mejia, J., Thaiss, C. A., Booth, C. J., Peaper, D. R., Bertin, J., Eisenbarth, S. C., Gordon, J. I., and Flavell, R. A. (2011) NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis, Cell, 145, 745–757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Wang, P., Zhu, S., Yang, L., Cui, S., Pan, W., Jackson, R., Zheng, Y., Rongvaux, A., Sun, Q., Yang, G., Gao, S., Lin, R., You, F., Flavell, R., and Fikrig, E. (2015) Nlrp6 regulates intestinal antiviral innate immunity, Science, 350, 826–830.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Vladimer, G. I., Weng, D., Paquette, S. W., Vanaja, S. K., Rathinam, V. A., Aune, M. H., Conlon, J. E., Burbage, J. J., Proulx, M. K., Liu, Q., Reed, G., Mecsas, J. C., Iwakura, Y., Bertin, J., Goguen, J. D., Fitzgerald, K. A., and Lien, E. (2012) The NLRP12 inflammasome recognizes Yersinia pestis, Immunity, 37, 96–107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Khare, S., Dorfleutner, A., Bryan, N. B., Yun, C., Radian, A. D., De Almeida, L., Rojanasakul, Y., and Stehlik, C. (2012) An NLRP7-containing inflammasome mediates recognition of microbial lipopeptides in human macrophages, Immunity, 36, 464–476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Unterholzner, L., Keating, S. E., Baran, M., Horan, K. A., Jensen, S. B., Sharma, S., Sirois, C. M., Jin, T., Latz, E., Xiao, T. S., Fitzgerald, K. A., Paludan, S. R., and Bowie, A. G. (2010) IFI16 is an innate immune sensor for intracellular DNA, Nat. Immunol., 11, 997–1004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Man, S. M., and Kanneganti, T. D. (2015) Regulation of inflammasome activation, Immunol. Rev., 265, 6–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Strowig, T., Henao-Mejia, J., Elinav, E., and Flavell, R. (2012) Inflammasomes in health and disease, Nature, 481, 278–286.

    Article  CAS  PubMed  Google Scholar 

  57. Finlay, B. B., and McFadden, G. (2006) Anti-immunology: evasion of the host immune system by bacterial and viral pathogens, Cell, 124, 767–782.

    Article  CAS  PubMed  Google Scholar 

  58. Vanden Berghe, T., Linkermann, A., Jouan-Lanhouet, S., Walczak, H., and Vandenabeele, P. (2014) Regulated necrosis: the expanding network of non-apoptotic cell death pathways, Nat. Rev. Mol. Cell Biol., 15, 135–147.

    Article  CAS  PubMed  Google Scholar 

  59. Kaufmann, S. H. E., and Andersen, P. (2011) Immune intervention strategies against tuberculosis, in The Immune Response to Infection (Kaufmann, S. H. E., Rouse, B. T., and Sacks D. L.}, eds.) ASM Press, Washington, D. C., pp. 571-586.

  60. Cunha, L. D., and Zamboni, D. S. (2013) Subversion of inflammasome activation and pyroptosis by pathogenic bacteria, Front. Cell. Infect. Microbiol., 3, 76.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Lamkanfi, M., and Dixit, V. M. (2011) Modulation of inflammasome pathways by bacterial and viral pathogens, J. Immunol., 187, 597–602.

  62. Lupfer, C. R., and Kanneganti, T. D. (2012) The role of inflammasome modulation in virulence, Virulence, 3, 262270.

    Article  Google Scholar 

  63. Schotte, P., Denecker, G., Van Den Broeke, A., Vandenabeele, P., Cornelis, G. R., and Beyaert, R. (2004) Targeting Rac1 by the Yersinia effector protein YopE inhibits caspase-1-mediated maturation and release of interleukin-1beta, J. Biol. Chem., 279, 25134–25142.

    Article  CAS  PubMed  Google Scholar 

  64. Bustelo, X. R., Sauzeau, V., and Berenjeno, I. M. (2007) GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo, BioEssays, 29, 356–370.

    CAS  PubMed  Google Scholar 

  65. Brodsky, I. E., Palm, N. W., Sadanand, S., Ryndak, M. B., Sutterwala, F. S., Flavell, R. A., Bliska, J. B., and Medzhitov, R. (2010) A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system, Cell Host Microbe, 7, 376–387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. LaRock, C. N., and Cookson, B. T. (2012) The Yersinia virulence effector YopM binds caspase-1 to arrest inflammasome assembly and processing, Cell Host Microbe, 12, 799805.

    Article  CAS  Google Scholar 

  67. Hofling, S., Grabowski, B., Norkowski, S., Schmidt, M. A., and Ruter, C. (2015) Current activities of the Yersinia effector protein YopM, Int. J. Med. Microbiol., 305, 424432.

    Article  CAS  Google Scholar 

  68. Zheng, Y., Lilo, S., Mena, P., and Bliska, J. B. (2012) YopJinduced caspase-1 activation in Yersinia-infected macrophages: independent of apoptosis, linked to necrosis, dispensable for innate host defense, PLoS One, 7, e36019.

    Google Scholar 

  69. Tseneva, G. Ya., Solodovnikova, N. Yu., and Voskresenskaya, E. A. (2002) Molecular aspects of Yersinia virulence, Klin. Mikrobiol. Antimikrob. Khimioter., 4, 248–256.

    Google Scholar 

  70. Sutterwala, F. S., Mijares, L. A., Li, L., Ogura, Y., Kazmierczak, B. I., and Flavell, R. A. (2007) Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome, J. Exp. Med., 204, 32353245.

    Article  CAS  Google Scholar 

  71. Galle, M., Schotte, P., Haegman, M., Wullaert, A., Yang, H. J., Jin, S., and Beyaert, R. (2008) The Pseudomonas aeruginosa type III secretion system plays a dual role in the regulation of caspase-1 mediated IL-1beta maturation, J. Cell. Mol. Med., 12, 1767–1776.

    Article  CAS  PubMed  Google Scholar 

  72. Diacovich, L., and Gorvel, J. P. (2010) Bacterial manipulation of innate immunity to promote infection, Nat. Rev. Microbiol., 8, 117–128.

    Article  CAS  PubMed  Google Scholar 

  73. Liu, M., Haenssler, E., Uehara, T., Losick, V. P., Park, J. T., and Isberg, R. R. (2012) The Legionella pneumophila EnhC protein interferes with immunostimulatory muramyl peptide production to evade innate immunity, Cell Host Microbe, 12, 166–176.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Skoble, J., Portnoy, D. A., and Welch, M. D. (2000) Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility, J. Cell Biol., 150, 527–538.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Brodsky, I. E., and Medzhitov, R. (2009) Targeting of immune signalling networks by bacterial pathogens, Nat. Cell Biol., 11, 521–526.

    Article  CAS  PubMed  Google Scholar 

  76. Johannessen, M., Askarian, F., Sangvik, M., and Sollid, J. E. (2013) Bacterial interference with canonical NFkappaB signalling, Microbiology, 159 (Pt. 10), 2001-2013.

  77. Broz, P., and Monack, D. M. (2011) Molecular mechanisms of inflammasome activation during microbial infections, Immunol. Rev., 243, 174–190.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Castro-Eguiluz, D., Pelayo, R., Rosales-Garcia, V., Rosales-Reyes, R., Alpuche-Aranda, C., and OrtizNavarrete, V. (2009) B cell precursors are targets for Salmonella infection, Microb. Pathog., 47, 52–56.

    Article  CAS  PubMed  Google Scholar 

  79. Perez-Lopez, A., Rosales-Reyes, R., Alpuche-Aranda, C. M., and Ortiz-Navarrete, V. (2013) Salmonella downregulates Nod-like receptor family CARD domain containing protein 4 expression to promote its survival in B-cells by preventing inflammasome activation and cell death, J. Immunol., 190, 1201–1209.

    Article  CAS  PubMed  Google Scholar 

  80. Shimada, T., Park, B. G., Wolf, A. J., Brikos, C., Goodridge, H. S., Becker, C. A., Reyes, C. N., Miao, E. A., Aderem, A., Gotz, F., Liu, G. Y., and Underhill, D. M. (2010) Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1beta secretion, Cell Host Microbe, 7, 38–49.

    Article  CAS  Google Scholar 

  81. Abdelaziz, D. H., Gavrilin, M. A., Akhter, A., Caution, K., Kotrange, S., Khweek, A. A., Abdulrahman, B. A., Grandhi, J., Hassan, Z. A., Marsh, C., Wewers, M. D., and Amer, A. O. (2011) Apoptosis-associated speck-like protein (ASC) controls Legionella pneumophila infection in human monocytes, J. Biol. Chem., 286, 3203–3208.

    Article  CAS  PubMed  Google Scholar 

  82. Creasey, E. A., and Isberg, R. R. (2012) The protein SdhA maintains the integrity of the Legionella-containing vacuole, Proc. Natl. Acad. Sci. USA, 109, 3481–3486.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Ulland, T. K., Buchan, B. W., Ketterer, M. R., FernandesAlnemri, T., Meyerholz, D. K., Apicella, M. A., Alnemri, E. S., Jones, B. D., Nauseef, W. M., and Sutterwala, F. S. (2010) Cutting edge: mutation of Francisella tularensis mviN leads to increased macrophage absent in melanoma 2 inflammasome activation and a loss of virulence, J. Immunol., 185, 2670–2674.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Witzenrath, M., Pache, F., Lorenz, D., Koppe, U., Gutbier, B., Tabeling, C., Reppe, K., Meixenberger, K., Dorhoi, A., Ma, J., Holmes, A., Trendelenburg, G., Heimesaat, M. M., Bereswill, S., Van der Linden, M., Tschopp, J., Mitchell, T. J., Suttorp, N., and Opitz, B. (2011) The NLRP3 inflammasome is differentially activated by pneumolysin variants and contributes to host defense in pneumococcal pneumonia, J. Immunol., 187, 434–440.

    Article  CAS  PubMed  Google Scholar 

  85. Master, S. S., Rampini, S. K., Davis, A. S., Keller, C., Ehlers, S., Springer, B., Timmins, G. S., Sander, P., and Deretic, V. (2008) Mycobacterium tuberculosis prevents inflammasome activation, Cell Host Microbe, 3, 224–232.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Jacobs, S. R., and Damania, B. (2012) NLRs, inflammasomes, and viral infection, J. Leukoc. Biol., 92, 469–477.

    Article  CAS  PubMed  Google Scholar 

  87. Best, S. M. (2008) Viral subversion of apoptotic enzymes: escape from death row, Annu. Rev. Microbiol., 62, 171–192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Zhou, Q., Krebs, J. F., Snipas, S. J., Price, A., Alnemri, E. S., Tomaselli, K. J., and Salvesen, G. S. (1998) Interaction of the baculovirus anti-apoptotic protein p35 with caspases. Specificity, kinetics, and characterization of the caspase/p35 complex, Biochemistry, 37, 10757–10765.

    CAS  Google Scholar 

  89. Ray, C. A., Black, R. A., Kronheim, S. R., Greenstreet, T. A., Sleath, P. R., Salvesen, G. S., and Pickup, D. J. (1992) Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme, Cell, 69, 597–604.

    Article  CAS  PubMed  Google Scholar 

  90. Komiyama, T., Ray, C. A., Pickup, D. J., Howard, A. D., Thornberry, N. A., Peterson, E. P., and Salvesen, G. (1994) Inhibition of interleukin-1 beta converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition, J. Biol. Chem., 269, 19331–19337.

    CAS  PubMed  Google Scholar 

  91. MacNeill, A. L., Moldawer, L. L., and Moyer, R. W. (2009) The role of the cowpox virus crmA gene during intratracheal and intradermal infection of C57BL/6 mice, Virology, 384, 151–160.

    Article  CAS  PubMed  Google Scholar 

  92. Turner, S. J., Silke, J., Kenshole, B., and Ruby, J. (2000) Characterization of the ectromelia virus serpin, SPI-2, J. Gen. Virol., 81 (Pt. 10), 2425–2430.

    Article  CAS  PubMed  Google Scholar 

  93. Sawada, M., Kawayama, T., Imaoka, H., Sakazaki, Y., Oda, H., Takenaka, S., Kaku, Y., Azuma, K., Tajiri, M., Edakuni, N., Okamoto, M., Kato, S., and Hoshino, T. (2013) IL-18 induces airway hyperresponsiveness and pulmonary inflammation via CD4+ T-cell and IL-13, PLoS One, 8, e54623.

    Article  CAS  Google Scholar 

  94. Smith, V. P., Bryant, N. A., and Alcami, A. (2000) Ectromelia, vaccinia and cowpox viruses encode secreted interleukin-18-binding proteins, J. Gen. Virol., 81, (Pt. 5), 1223–1230.

    CAS  PubMed  Google Scholar 

  95. Kettle, S., Alcami, A., Khanna, A., Ehret, R., Jassoy, C., and Smith, G. L. (1997) Vaccinia virus serpin B13R (SPI2) inhibits interleukin-1beta-converting enzyme and protects virus-infected cells from TNFand Fas-mediated apoptosis, but does not prevent IL-1beta-induced fever, J. Gen. Virol., 78, 677–685.

    CAS  PubMed  Google Scholar 

  96. Gregory, S. M., Davis, B. K., West, J. A., Taxman, D. J., Matsuzawa, S.-I., Reed, J. C., Ting, J. P. Y., and Damania, B. (2011) Discovery of a viral NLR homolog that inhibits the inflammasome, Science, 331, 330–334.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Komune, N., Ichinohe, T., Ito, M., and Yanagi, Y. (2011) Measles virus V protein inhibits NLRP3 inflammasomemediated interleukin-1beta secretion, J. Virol., 85, 1301913026.

    Article  CAS  Google Scholar 

  98. Moriyama, M., Chen, I. Y., Kawaguchi, A., Koshiba, T., Nagata, K., Takeyama, H., Hasegawa, H., and Ichinohe, T. (2016) The RNAand TRIM25-binding domains of influenza virus NS1 protein are essential for suppression of NLRP3 inflammasome-mediated interleukin-1beta secretion, J. Virol., 90, 4105–4114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Johnston, J. B., Barrett, J. W., Nazarian, S. H., Goodwin, M., Ricciuto, D., Wang, G., and McFadden, G. (2005) A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection, Immunity, 23, 587–598.

    Article  CAS  PubMed  Google Scholar 

  100. Lu, A., Li, Y., Schmidt, F. I., Yin, Q., Chen, S., Fu, T. M., Tong, A. B., Ploegh, H. L., Mao, Y., and Wu, H. (2016) Molecular basis of caspase-1 polymerization and its inhibition by a new capping mechanism, Nat. Struct. Mol. Biol., 23, 416–425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Taylor, A. L., and Llewelyn, M. J. (2010) Superantigeninduced proliferation of human CD4+CD25–T-cells is followed by a switch to a functional regulatory phenotype, J. Immunol., 185, 6591–6598.

    Article  CAS  PubMed  Google Scholar 

  102. Garib, F. Yu., and Rizopulu, A. P. (2015) T-regulatory cells as part of strategy of immune evasion by pathogens, Biochemistry (Moscow), 80, 1141–1159.

    Article  CAS  Google Scholar 

  103. Belkaid, Y., and Tarbell, K. (2009) Regulatory T-cells in the control of host-microorganism interactions, Annu. Rev. Immunol., 27, 551–589.

    Article  CAS  PubMed  Google Scholar 

  104. Dorfleutner, A., Talbott, S. J., Bryan, N. B., Funya, K. N., Rellick, S. L., Reed, J. C., Shi, X., Rojanasakul, Y., Flynn, D. C., and Stehlik, C. (2007) A Shope fibroma virus PYRIN-only protein modulates the host immune response, Virus Genes, 35, 685–694.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Matusiak, M., Van Opdenbosch, N., and Lamkanfi, M. (2015) CARDand pyrin-only proteins regulating inflammasome activation and immunity, Immunol. Rev., 265, 217–230.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Yu. Garib.

Additional information

Original Russian Text © F. Yu. Garib, A. P. Rizopulu, A. A. Kuchmiy, V. F. Garib, 2016, published in Biokhimiya, 2016, Vol. 81, No. 11, pp. 1578–1592.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garib, F.Y., Rizopulu, A.P., Kuchmiy, A.A. et al. Inactivation of inflammasomes by pathogens regulates inflammation. Biochemistry Moscow 81, 1326–1339 (2016). https://doi.org/10.1134/S0006297916110109

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297916110109

Keywords

Navigation