Inflammatory Monocytes and Neutrophils Are Licensed to Kill during Memory Responses

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Immunological memory is a hallmark of B and T lymphocytes that have undergone a previous encounter with a given antigen. It is assumed that memory cells mediate better protection of the host upon re-infection because of improved effector functions such as antibody production, cytotoxic activity and cytokine secretion. In contrast to cells of the adaptive immune system, innate immune cells are believed to exhibit a comparable functional effector response each time the same pathogen is encountered. Here, using mice infected by the intracellular bacterium Listeria monocytogenes, we show that during a recall bacterial infection, the chemokine CCL3 secreted by memory CD8⁺ T cells drives drastic modifications of the functional properties of several populations of phagocytes. We found that inflammatory ly6C⁺ monocytes and neutrophils largely mediated memory CD8⁺ T cell bacteriocidal activity by producing increased levels of reactive oxygen species (ROS), augmenting the pH of their phagosomes and inducing antimicrobial autophagy. These events allowed an extremely rapid control of bacterial growth in vivo and accounted for protective immunity. Therefore, our results provide evidence that cytotoxic memory CD8⁺ T cells can license distinct antimicrobial effector mechanisms of innate cells to efficiently clear pathogens.

Vyšlo v časopise: Inflammatory Monocytes and Neutrophils Are Licensed to Kill during Memory Responses. PLoS Pathog 7(12): e32767. doi:10.1371/journal.ppat.1002457
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002457

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Zdroje

1. HartyJTTvinnereimARWhiteDW 2000 CD8+ T cell effector mechanisms in resistance to infection. Annu Rev Immunol 18 275 308

2. MasopustDVezysVMarzoALLefrancoisL 2001 Preferential localization of effector memory cells in nonlymphoid tissue. Science 291 2413 2417

3. GuidottiLGChisariFV 2001 Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 19 65 91

4. CowleySCSedgwickJDElkinsKL 2007 Differential requirements by CD4+ and CD8+ T cells for soluble and membrane TNF in control of Francisella tularensis live vaccine strain intramacrophage growth. J Immunol 179 7709 7719

5. MullerIKropfPEtgesRJLouisJA 1993 Gamma interferon response in secondary Leishmania major infection: role of CD8+ T cells. Infect Immun 61 3730 3738

6. Narni-MancinelliECampisiLBassandDCazarethJGounonP 2007 Memory CD8+ T cells mediate antibacterial immunity via CCL3 activation of TNF/ROI+ phagocytes. J Exp Med 204 2075 2087

7. BartonESWhiteDWCathelynJSBrett-McClellanKAEngleM 2007 Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447 326 329

8. StruttTMMcKinstryKKDibbleJPWinchellCKuangY 2010 Memory CD4+ T cells induce innate responses independently of pathogen. Nat Med 16 558 564 551p following 564

9. ZhangZClarkeTBWeiserJN 2009 Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest 119 1899 1909

10. GeissmannFAuffrayCPalframanRWirrigCCioccaA 2008 Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol Cell Biol 86 398 408

11. SerbinaNVJiaTHohlTMPamerEG 2008 Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 26 421 452

12. IshiiKJKoyamaSNakagawaACobanCAkiraS 2008 Host innate immune receptors and beyond: making sense of microbial infections. Cell Host Microbe 3 352 363

13. HenryRMHoppeADJoshiNSwansonJA 2004 The uniformity of phagosome maturation in macrophages. J Cell Biol 164 185 194

14. SegalAW 2005 How neutrophils kill microbes. Annu Rev Immunol 23 197 223

15. BabiorBM 2000 Phagocytes and oxidative stress. Am J Med 109 33 44

16. NathanCDingA 2010 SnapShot: Reactive Oxygen Intermediates (ROI). Cell 140 951 951 e952

17. MacMickingJXieQWNathanC 1997 Nitric oxide and macrophage function. Annu Rev Immunol 15 323 350

18. IsmailNOlanoJPFengHMWalkerDH 2002 Current status of immune mechanisms of killing of intracellular microorganisms. FEMS Microbiol Lett 207 111 120

19. KirkegaardKTaylorMPJacksonWT 2004 Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat Rev Microbiol 2 301 314

20. PyBFLipinskiMMYuanJ 2007 Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection. Autophagy 3 117 125

21. WalkerDHPopovVLCrocquet-ValdesPAWelshCJFengHM 1997 Cytokine-induced, nitric oxide-dependent, intracellular antirickettsial activity of mouse endothelial cells. Lab Invest 76 129 138

22. MurailleENarni-MancinelliEGounonPBassandDGlaichenhausN 2007 Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity. Cell Microbiol 9 1445 1454

23. IdoyagaJSudaNSudaKParkCGSteinmanRM 2009 Antibody to Langerin/CD207 localizes large numbers of CD8alpha+ dendritic cells to the marginal zone of mouse spleen. Proc Natl Acad Sci U S A 106 1524 1529

24. CookDNSmithiesOStrieterRMFrelingerJASerodyJS 1999 CD8+ T cells are a biologically relevant source of macrophage inflammatory protein-1 alpha in vivo. J Immunol 162 5423 5428

25. KaoCOestreichKJPaleyMACrawfordAAngelosantoJM 2011 Transcription factor T-bet represses expression of the inhibitory receptor PD-1 and sustains virus-specific CD8+ T cell responses during chronic infection. Nat Immunol 12 663 671

26. WirthTCXueHHRaiDSabelJTBairT 2010 Repetitive antigen stimulation induces stepwise transcriptome diversification but preserves a core signature of memory CD8(+) T cell differentiation. Immunity 33 128 140

27. WhiteDWMacNeilABuschDHPilipIMPamerEG 1999 Perforin-deficient CD8+ T cells: in vivo priming and antigen-specific immunity against Listeria monocytogenes. J Immunol 162 980 988

28. MessinghamKABadovinacVPJabbariAHartyJT 2007 A role for IFN-gamma from antigen-specific CD8+ T cells in protective immunity to Listeria monocytogenes. J Immunol 179 2457 2466

29. GeissmannFJungSLittmanDR 2003 Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19 71 82

30. SerbinaNVSalazar-MatherTPBironCAKuzielWAPamerEG 2003 TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19 59 70

31. FlannaganRSCosioGGrinsteinS 2009 Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7 355 366

32. ReevesEPLuHJacobsHLMessinaCGBolsoverS 2002 Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416 291 297

33. SegalAWGeisowMGarciaRHarperAMillerR 1981 The respiratory burst of phagocytic cells is associated with a rise in vacuolar pH. Nature 290 406 409

34. SavinaAVargasPGuermonprezPLennonAMAmigorenaS 2010 Measuring pH, ROS production, maturation, and degradation in dendritic cell phagosomes using cytofluorometry-based assays. Methods Mol Biol 595 383 402

35. SavinaAJancicCHuguesSGuermonprezPVargasP 2006 NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126 205 218

36. DramsiSCossartP 2002 Listeriolysin O: a genuine cytolysin optimized for an intracellular parasite. J Cell Biol 156 943 946

37. PortnoyDAAuerbuchVGlomskiIJ 2002 The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cell-mediated immunity. J Cell Biol 158 409 414

38. Vazquez-BolandJAKuhnMBerchePChakrabortyTDominguez-BernalG 2001 Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14 584 640

39. MoorsMALevittBYoungmanPPortnoyDA 1999 Expression of listeriolysin O and ActA by intracellular and extracellular Listeria monocytogenes. Infect Immun 67 131 139

40. Scherz-ShouvalRShvetsEFassEShorerHGilL 2007 Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. Embo J 26 1749 1760

41. KimJVKangSSDustinMLMcGavernDB 2009 Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis. Nature 457 191 195

42. FosterSLHargreavesDCMedzhitovR 2007 Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447 972 978

43. AuffrayCFoggDGarfaMElainGJoin-LambertO 2007 Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317 666 670

44. SwirskiFKNahrendorfMEtzrodtMWildgruberMCortez-RetamozoV 2009 Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325 612 616

45. GeissmannFManzMGJungSSiewekeMHMeradM 2010 Development of monocytes, macrophages, and dendritic cells. Science 327 656 661

46. BajenoffMNarni-MancinelliEBrauFLauvauG 2010 Visualizing early splenic memory CD8+ T cells reactivation against intracellular bacteria. PLoS One 5 e11524

47. DangPMStensballeABoussettaTRaadHDewasC 2006 A specific p47phox -serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites. J Clin Invest 116 2033 2043

48. JungSAlibertiJGraemmelPSunshineMJKreutzbergGW 2000 Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20 4106 4114

49. LauvauGVijhSKongPHorngTKerksiekK 2001 Priming of memory but not effector CD8 T cells by a killed bacterial vaccine. Science 294 1735 1739