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Induction and Consequences of the Type I IFN Response to Listeria monocytogenes

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Bacterial Activation of Type I Interferons
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Summary

Listeria monocytogenes is a Gram-positive intracellular bacterial pathogen. During infection of host cells, L. monocytogenes introduces microbial components into both vacuolar compartments and the cytoplasm. Innate receptors in these compartments recognize the pathogen and induce pro-inflammatory cytokines, including type I interferons (IFNs). Strikingly, production of type I IFNs and responsiveness to these cytokines is deleterious to the host during infections by L. monocytogenes and several other bacteria. Hence, a better understanding of their regulation has potential importance for antimicrobial therapy. Recent studies have revealed involvement of cytosolic immune sensors and pathways in host detection of L. monocytogenes components and stimulation of type I IFN production. This chapter will examine these receptors and their downstream adaptor and effector molecules that have proven to be vital for signal transduction and subsequent type I IFN secretion.

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References

  1. McCollum JT, Cronquist AB, Silk BJ et al (2013) Multistate outbreak of listeriosis associated with cantaloupe. N Engl J Med 369:944–953

    Article  PubMed  CAS  Google Scholar 

  2. Mostowy S, Cossart P (2009) Cytoskeleton rearrangements during Listeria infection: clathrin and septins as new players in the game. Cell Motil Cytoskeleton 66:816–823

    Article  PubMed  CAS  Google Scholar 

  3. Hamon M, Bierne H, Cossart P (2006) Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4:423–434

    Article  PubMed  CAS  Google Scholar 

  4. Ireton K (2007) Entry of the bacterial pathogen Listeria monocytogenes into mammalian cells. Cell Microbiol 9:1365–1375

    Article  PubMed  CAS  Google Scholar 

  5. Schnupf P, Portnoy DA (2007) Listeriolysin O: a phagosome-specific lysin. Microbes Infect 9:1176–1187

    Article  PubMed  CAS  Google Scholar 

  6. Portnoy D, Jacks P, Hinrichs D (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167:1459–1471

    Article  PubMed  CAS  Google Scholar 

  7. Berche P, Gaillard JL, Sansonetti PJ (1987) Intracellular growth of Listeria monocytogenes as a prerequisite for in vivo induction of T cell-mediated immunity. J Immunol 138:2266–2271

    PubMed  CAS  Google Scholar 

  8. Taniguchi T, Ogasawara K, Takaoka A, Tanaka N (2001) IRF family of transcription factors as regulators of host defense. Annu Rev Immunol 19:623–655

    Article  PubMed  CAS  Google Scholar 

  9. O’Connell RM, Saha SK, Vaidya SA et al (2004) Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J Exp Med 200:437–445

    Article  PubMed  PubMed Central  Google Scholar 

  10. Garifulin O, Qi Z, Shen H et al (2007) Irf3 polymorphism alters induction of interferon beta in response to Listeria monocytogenes infection. PLoS Genet 3:1587–1597

    Article  PubMed  CAS  Google Scholar 

  11. O’Connell R, Vaidya S, Perry AK et al (2005) Immune activation of type I IFNs by Listeria monocytogenes occurs independently of TLR4, TLR2, and receptor interacting protein 2 but involves TANK-binding kinase. J Immunol 174:1602–1607

    Article  PubMed  Google Scholar 

  12. Stockinger S, Reutterer B, Schaljo B et al (2004) IFN regulatory factor 3-dependent induction of type I IFNs by intracellular bacteria is mediated by a TLR- and Nod2-independent mechanism. J Immunol 173:7416–7425

    Article  PubMed  CAS  Google Scholar 

  13. Aubry C, Corr SC, Wienerroither S et al (2012) Both TLR2 and TRIF contribute to interferon-β production during Listeria infection. PLoS One 7:e33299

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  14. Leber JH, Crimmins GT, Raghavan S et al (2008) Distinct TLR- and NLR-mediated transcriptional responses to an intracellular pathogen. PLoS Pathog 4:e6

    Article  PubMed  PubMed Central  Google Scholar 

  15. Pomerantz JL, Baltimore D (1999) NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. EMBO J 18:6694–6704

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  16. Fitzgerald KA, McWhirter SM, Faia KL et al (2003) IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4:491–496

    Article  PubMed  CAS  Google Scholar 

  17. Sharma S, tenOever BR, Grandvaux N et al (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300:1148–1151

    Article  PubMed  CAS  Google Scholar 

  18. Perry AK, Chow EK, Goodnough JB et al (2004) Differential requirement for TANK-binding kinase-1 in type I interferon responses to Toll-like receptor activation and viral infection. J Exp Med 199:1651–1658

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  19. Yu T, Yi Y-S, Yang Y et al (2012) The pivotal role of TBK1 in inflammatory responses mediated by macrophages. Mediators Inflamm 2012:979105

    Article  PubMed  PubMed Central  Google Scholar 

  20. Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17:1–14

    Article  PubMed  CAS  Google Scholar 

  21. Doyle S, Vaidya S, O’Connell R et al (2002) IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17:251–263

    Article  PubMed  CAS  Google Scholar 

  22. Takeuchi O, Hoshino K, Kawai T et al (1999) Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11:443–451

    Article  PubMed  CAS  Google Scholar 

  23. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732–738

    Article  PubMed  CAS  Google Scholar 

  24. Seki E, Tsutsui H, Tsuji NM et al (2002) Critical roles of myeloid differentiation factor 88-dependent proinflammatory cytokine release in early phase clearance of Listeria monocytogenes in mice. J Immunol 169:3863–3868

    Article  PubMed  CAS  Google Scholar 

  25. Janot L, Secher T, Torres D et al (2008) CD14 works with toll-like receptor 2 to contribute to recognition and control of Listeria monocytogenes infection. J Infect Dis 198:115–124

    Article  PubMed  CAS  Google Scholar 

  26. Torres D, Barrier M, Bihl F et al (2004) Toll-like receptor 2 is required for optimal control of Listeria monocytogenes infection. Infect Immun 72:2131–2139

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  27. Edelson BT, Unanue ER (2002) MyD88-dependent but Toll-like receptor 2-independent innate immunity to Listeria: no role for either in macrophage listericidal activity. J Immunol 169:3869–3875

    Article  PubMed  CAS  Google Scholar 

  28. Barbalat R, Lau L, Locksley RM, Barton GM (2009) Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat Immunol 10:1200–1207

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  29. Dietrich N, Lienenklaus S, Weiss S, Gekara NO (2010) Murine toll-like receptor 2 activation induces type I interferon responses from endolysosomal compartments. PLoS One 5:e10250

    Article  PubMed  PubMed Central  Google Scholar 

  30. McCaffrey RL, Fawcett P, O’Riordan M et al (2004) A specific gene expression program triggered by Gram-positive bacteria in the cytosol. Proc Natl Acad Sci U S A 101:11386–11391

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. Creagh EM, O’Neill LAJ (2006) TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol 27:352–357

    Article  PubMed  CAS  Google Scholar 

  32. Kufer TA, Banks DJ, Philpott DJ (2006) Innate immune sensing of microbes by Nod proteins. Ann N Y Acad Sci 1072:19–27

    Article  PubMed  CAS  Google Scholar 

  33. Park J-H, Kim Y-G, McDonald C et al (2007) RICK/RIP2 mediates innate immune responses induced through Nod1 and Nod2 but not TLRs. J Immunol 178:2380–2386

    Article  PubMed  CAS  Google Scholar 

  34. Kobayashi K, Inohara N, Hernandez LD et al (2002) RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 416:194–199

    Article  PubMed  CAS  Google Scholar 

  35. Chin AI, Dempsey PW, Bruhn K et al (2002) Involvement of receptor-interacting protein 2 in innate and adaptive immune responses. Nature 416:190–194

    Article  PubMed  CAS  Google Scholar 

  36. Rehwinkel J, Reis e Sousa C (2010) RIGorous detection: exposing virus through RNA sensing. Science 327:284–286

    Article  PubMed  CAS  Google Scholar 

  37. Hiscott J, Lin R, Nakhaei P, Paz S (2006) MasterCARD: a priceless link to innate immunity. Trends Mol Med 12:53–56

    Article  PubMed  CAS  Google Scholar 

  38. Sun Q, Sun L, Liu H-H et al (2006) The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24:633–642

    Article  PubMed  CAS  Google Scholar 

  39. Chiu Y-H, Macmillan JB, Chen ZJ (2009) RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138:576–591

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  40. Soulat D, Bauch A, Stockinger S et al (2006) Cytoplasmic Listeria monocytogenes stimulates IFN-beta synthesis without requiring the adapter protein MAVS. FEBS Lett 580:2341–2346

    Article  PubMed  CAS  Google Scholar 

  41. Abdullah Z, Schlee M, Roth S et al (2012) RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J 31:4153–4164

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  42. Lenz LL, Mohammadi S, Geissler A, Portnoy DA (2003) SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc Natl Acad Sci U S A 100:12432–12437

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  43. Hagmann CA, Herzner AM, Abdullah Z et al (2013) RIG-I detects triphosphorylated RNA of Listeria monocytogenes during infection in non-immune cells. PLoS One 8:e62872

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  44. Stetson DB, Medzhitov R (2006) Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24:93–103

    Article  PubMed  CAS  Google Scholar 

  45. Takaoka A, Wang Z, Choi MK et al (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448:501–505

    Article  PubMed  CAS  Google Scholar 

  46. Yanai H, Savitsky D, Tamura T, Taniguchi T (2009) Regulation of the cytosolic DNA-sensing system in innate immunity: a current view. Curr Opin Immunol 21:17–22

    Article  PubMed  CAS  Google Scholar 

  47. Lippmann J, Rothenburg S, Deigendesch N et al (2008) IFNbeta responses induced by intracellular bacteria or cytosolic DNA in different human cells do not require ZBP1 (DLM-1/DAI). Cell Microbiol 10:2579–2588

    Article  PubMed  CAS  Google Scholar 

  48. Wilson SA, Brown EC, Kingsman AJ, Kingsman SM (1998) TRIP: a novel double stranded RNA binding protein which interacts with the leucine rich repeat of flightless I. Nucleic Acids Res 26:3460–3467

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  49. Yang P, An H, Liu X et al (2010) The cytosolic nucleic acid sensor LRRFIP1 mediates the production of type I interferon via a beta-catenin-dependent pathway. Nat Immunol 11:487–494

    Article  PubMed  CAS  Google Scholar 

  50. Suriano A, Sanford A, Kim N (2005) GCF2/LRRFIP1 represses tumor necrosis factor alpha expression. Mol Cell Biol 25:9073–9081

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  51. Hornung V, Ablasser A, Charrel-Dennis M et al (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514–518

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  52. Hornung V, Latz E (2010) Critical functions of priming and lysosomal damage for NLRP3 activation. Eur J Immunol 40:620–623

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  53. Tsuchiya K, Hara H, Kawamura I et al (2010) Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes. J Immunol 185:1186–1195

    Article  PubMed  CAS  Google Scholar 

  54. Unterholzner L, Keating SE, Baran M et al (2010) IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11:997–1004

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  55. Schattgen SA, Fitzgerald KA (2011) The PYHIN protein family as mediators of host defenses. Immunol Rev 243:109–118

    Article  PubMed  CAS  Google Scholar 

  56. Ishikawa H, Barber GN (2008) STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455:674–678

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  57. Zhong B, Yang Y, Li S et al (2008) The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29:538–550

    Article  PubMed  CAS  Google Scholar 

  58. Jin L, Waterman PM, Jonscher KR et al (2008) MPYS, a novel membrane tetraspanner, is associated with major histocompatibility complex class II and mediates transduction of apoptotic signals. Mol Cell Biol 28:5014–5026

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  59. Sun W, Li Y, Chen L et al (2009) ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc Natl Acad Sci U S A 106:8653–8658

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  60. Ishikawa H, Ma Z, Barber GN (2009) STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461:788–792

    Article  PubMed  CAS  Google Scholar 

  61. Jin L, Hill KK, Filak H et al (2011) MPYS is required for IFN response factor 3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. J Immunol 187:2595–2601

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  62. Sauer J-D, Sotelo-Troha K, von Moltke J et al (2011) The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect Immun 79:688–694

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  63. Burdette DL, Monroe KM, Sotelo-Troha K et al (2011) STING is a direct innate immune sensor of cyclic di-GMP. Nature 478:515–518

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  64. Parvatiyar K, Zhang Z, Teles RM et al (2012) The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat Immunol 13:1155–1161

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  65. Zhang Z, Yuan B, Bao M et al (2011) The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12:959–965

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  66. Woodward JJ, Iavarone AT, Portnoy DA (2010) c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328:1703–1705

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  67. Witte CE, Whiteley AT, Burke TP et al (2013) Cyclic di-AMP is critical for Listeria monocytogenes growth, cell wall homeostasis, and establishment of infection. MBio 4:e00282-13

    Google Scholar 

  68. Wu J, Sun L, Chen X et al (2013) Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339:826–830

    Article  PubMed  CAS  Google Scholar 

  69. Sun L, Wu J, Du F et al (2013) Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339:786–791

    Article  PubMed  CAS  Google Scholar 

  70. Auerbuch V, Brockstedt DG, Meyer-Morse N et al (2004) Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J Exp Med 200:527–533

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  71. Rayamajhi M, Humann J, Penheiter K et al (2010) Induction of IFN-alpha/beta enables Listeria monocytogenes to suppress macrophage activation by IFN-gamma. J Exp Med 207:327–337

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  72. Rayamajhi M, Humann J, Kearney S et al (2010) Antagonistic crosstalk between type I and II interferons and increased host susceptibility to bacterial infections. Virulence 1:418–422

    Article  PubMed  PubMed Central  Google Scholar 

  73. Carrero JA, Calderon B, Unanue ER (2004) Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J Exp Med 200:535–540

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  74. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958–969

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  75. Kearney SJ, Delgado C, Eshleman EM et al (2013) Type I IFNs downregulate myeloid cell IFN-γ receptor by inducing recruitment of an early growth response 3/NGFI-A binding protein 1 complex that silences ifngr1 transcription. J Immunol 191:3384–3392

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  76. Swirnoff A, Milbrandt J (1995) DNA-binding specificity of NGFI-A and related zinc finger transcription factors. Mol Cell Biol 15:2275–2287

    PubMed  CAS  PubMed Central  Google Scholar 

  77. O’Donovan KJ, Tourtellotte WG, Millbrandt J, Baraban JM (1999) The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci 22:167–173

    Article  PubMed  Google Scholar 

  78. Yu J, de Belle I, Liang H, Adamson ED (2004) Coactivating factors p300 and CBP are transcriptionally crossregulated by Egr1 in prostate cells, leading to divergent responses. Mol Cell 15:83–94

    Article  PubMed  CAS  Google Scholar 

  79. Huang RP, Fan Y, deBelle I et al (1998) Egr-1 inhibits apoptosis during the UV response: correlation of cell survival with Egr-1 phosphorylation. Cell Death Differ 5:96–106

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Laurel L. Lenz .

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Eshleman, E.M., Lenz, L.L. (2014). Induction and Consequences of the Type I IFN Response to Listeria monocytogenes . In: Parker, D. (eds) Bacterial Activation of Type I Interferons. Springer, Cham. https://doi.org/10.1007/978-3-319-09498-4_2

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