Low CCR7-Mediated Migration of Human Monocyte Derived Dendritic Cells in Response to Human Respiratory Syncytial Virus and Human Metapneumovirus

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Human respiratory syncytial virus (HRSV) and, to a lesser extent, human metapneumovirus (HMPV) and human parainfluenza virus type 3 (HPIV3), can re-infect symptomatically throughout life without significant antigenic change, suggestive of incomplete or short-lived immunity. In contrast, re-infection by influenza A virus (IAV) largely depends on antigenic change, suggestive of more complete immunity. Antigen presentation by dendritic cells (DC) is critical in initiating the adaptive immune response. Antigen uptake by DC induces maturational changes that include decreased expression of the chemokine receptors CCR1, CCR2, and CCR5 that maintain DC residence in peripheral tissues, and increased expression of CCR7 that mediates the migration of antigen-bearing DC to lymphatic tissue. We stimulated human monocyte-derived DC (MDDC) with virus and found that, in contrast to HPIV3 and IAV, HMPV and HRSV did not efficiently decrease CCR1, 2, and 5 expression, and did not efficiently increase CCR7 expression. Consistent with the differences in CCR7 mRNA and protein expression, MDDC stimulated with HRSV or HMPV migrated less efficiently to the CCR7 ligand CCL19 than did IAV-stimulated MDDC. Using GFP-expressing recombinant virus, we showed that the subpopulation of MDDC that was robustly infected with HRSV was particularly inefficient in chemokine receptor modulation. HMPV- or HRSV-stimulated MDDC responded to secondary stimulation with bacterial lipopolysaccharide or with a cocktail of proinflammatory cytokines by increasing CCR7 and decreasing CCR1, 2 and 5 expression, and by more efficient migration to CCL19, suggesting that HMPV and HRSV suboptimally stimulate rather than irreversibly inhibit MDDC migration. This also suggests that the low concentration of proinflammatory cytokines released from HRSV- and HMPV-stimulated MDDC is partly responsible for the low CCR7-mediated migration. We propose that inefficient migration of HRSV- and HMPV-stimulated DC to lymphatic tissue contributes to reduced adaptive responses to these viruses.

Vyšlo v časopise: Low CCR7-Mediated Migration of Human Monocyte Derived Dendritic Cells in Response to Human Respiratory Syncytial Virus and Human Metapneumovirus. PLoS Pathog 7(6): e32767. doi:10.1371/journal.ppat.1002105
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002105

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1. CanqueBRosenzwajgMGluckmanJC 2003 In vitro generation of dendritic cells from cord blood CD34+ hematopoietic progenitors cells. Methods Mol Biol 215 311 325

2. NairHNokesDJGessnerBDDheraniMMadhiSA 2010 Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375 1545 1555

3. HallCB 2001 Respiratory syncytial virus and parainfluenza virus. N Engl J Med 344 1917 1928

4. WelliverRCWongDTSunMMcCarthyN 1986 Parainfluenza virus bronchiolitis. Epidemiology and pathogenesis. Am J Dis Child 140 34 40

5. FalseyAR 2008 Human metapneumovirus infection in adults. Pediatr Infect Dis J 27 S80 83

6. HamelinMEAbedYBoivinG 2004 Human metapneumovirus: a new player among respiratory viruses. Clin Infect Dis 38 983 990

7. WilliamsJVHarrisPATollefsonSJHalburnt-RushLLPingsterhausJM 2004 Human metapneumovirus and lower respiratory tract disease in otherwise healthy infants and children. N Engl J Med 350 443 450

8. FalseyARHennesseyPAFormicaMACoxCWalshEE 2005 Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352 1749 1759

9. ThompsonWWShayDKWeintraubEBrammerLBridgesCB 2004 Influenza-associated hospitalizations in the United States. JAMA 292 1333 1340

10. ThompsonWWShayDKWeintraubEBrammerLCoxN 2003 Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289 179 186

11. 2009 Update: influenza activity–United States, September 28, 2008-April 4, 2009, and composition of the 2009-10 influenza vaccine. MMWR Morb Mortal Wkly Rep 58 369 374

12. ZhangLBukreyevAThompsonCIWatsonBPeeplesME 2005 Infection of ciliated cells by human parainfluenza virus type 3 in an in vitro model of human airway epithelium. J Virol 79 1113 1124

13. ZhangLPeeplesMEBoucherRCCollinsPLPicklesRJ 2002 Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. J Virol 76 5654 5666

14. AhmedROldstoneMBPaleseP 2007 Protective immunity and susceptibility to infectious diseases: lessons from the 1918 influenza pandemic. Nat Immunol 8 1188 1193

15. CouchRBKaselJA 1983 Immunity to influenza in man. Annu Rev Microbiol 37 529 549

16. GlezenWPTaberLHFrankALKaselJA 1986 Risk of primary infection and reinfection with respiratory syncytial virus. Am J Dis Child 140 543 546

17. JohnsonKMChanockRMRifkindDKravetzHMKnightV 1961 Respiratory syncytial virus. IV. Correlation of virus shedding, serologic response, and illness in adult volunteers. JAMA 176 663 667

18. HallCBWalshEELongCESchnabelKC 1991 Immunity to and frequency of reinfection with respiratory syncytial virus. J Infect Dis 163 693 698

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

20. GeissmannF 2007 The origin of dendritic cells. Nat Immunol 8 558 560

21. 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

22. Cheong C, Matos I, Choi JH, Dandamudi DB, Shrestha E, et al. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell 143 416 429

23. FrascaLFedeleGDeaglioSCapuanoCPalazzoR 2006 CD38 orchestrates migration, survival, and Th1 immune response of human mature dendritic cells. Blood 107 2392 2399

24. Reis e SousaC 2006 Dendritic cells in a mature age. Nat Rev Immunol 6 476 483

25. AlvarezDVollmannEHvon AndrianUH 2008 Mechanisms and consequences of dendritic cell migration. Immunity 29 325 342

26. ForsterRDavalos-MisslitzACRotA 2008 CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 8 362 371

27. GunnMDTangemannKTamCCysterJGRosenSD 1998 A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc Natl Acad Sci U S A 95 258 263

28. LutherSATangHLHymanPLFarrAGCysterJG 2000 Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse. Proc Natl Acad Sci U S A 97 12694 12699

29. WillimannKLeglerDFLoetscherMRoosRSDelgadoMB 1998 The chemokine SLC is expressed in T cell areas of lymph nodes and mucosal lymphoid tissues and attracts activated T cells via CCR7. Eur J Immunol 28 2025 2034

30. SozzaniS 2005 Dendritic cell trafficking: more than just chemokines. Cytokine Growth Factor Rev 16 581 592

31. Lukacs-KornekVEngelDTackeFKurtsC 2008 The role of chemokines and their receptors in dendritic cell biology. Front Biosci 13 2238 2252

32. Le NouenCMunirSLosqSWinterCCMcCartyT 2009 Infection and maturation of monocyte-derived human dendritic cells by human respiratory syncytial virus, human metapneumovirus, and human parainfluenza virus type 3. Virology

33. Le NouenCHillyerPMunirSWinterCCMcCartyT 2010 Effects of Human Respiratory Syncytial Virus, Metapneumovirus, Parainfluenza Virus 3 and Influenza Virus on CD4+ T Cell Activation by Dendritic Cells. PLoS One 5 e15017

34. JakubzickCTackeFGinhouxFWagersAJvan RooijenN 2008 Blood monocyte subsets differentially give rise to CD103+ and CD103- pulmonary dendritic cell populations. J Immunol 180 3019 3027

35. VarolCLandsmanLFoggDKGreenshteinLGildorB 2007 Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med 204 171 180

36. XuYZhanYLewAMNaikSHKershawMH 2007 Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J Immunol 179 7577 7584

37. BiacchesiSSkiadopoulosMHTranKCMurphyBRCollinsPL 2004 Recovery of human metapneumovirus from cDNA: optimization of growth in vitro and expression of additional genes. Virology 321 247 259

38. HallakLKSpillmannDCollinsPLPeeplesME 2000 Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J Virol 74 10508 10513

39. BiacchesiSMurphyBRCollinsPLBuchholzUJ 2007 Frequent frameshift and point mutations in the SH gene of human metapneumovirus passaged in vitro. J Virol 81 6057 6067

40. De SmedtTPajakBMurailleELespagnardLHeinenE 1996 Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J Exp Med 184 1413 1424

41. VerhasseltVBuelensCWillemsFDe GrooteDHaeffner-CavaillonN 1997 Bacterial lipopolysaccharide stimulates the production of cytokines and the expression of costimulatory molecules by human peripheral blood dendritic cells: evidence for a soluble CD14-dependent pathway. J Immunol 158 2919 2925

42. DieuMCVanbervlietBVicariABridonJMOldhamE 1998 Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 188 373 386

43. VecchiAMassimilianoLRamponiSLuiniWBernasconiS 1999 Differential responsiveness to constitutive vs. inducible chemokines of immature and mature mouse dendritic cells. J Leukoc Biol 66 489 494

44. ZhangWChenZLiFKamencicHJuurlinkB 2003 Tumour necrosis factor-alpha (TNF-alpha) transgene-expressing dendritic cells (DCs) undergo augmented cellular maturation and induce more robust T-cell activation and anti-tumour immunity than DCs generated in recombinant TNF-alpha. Immunology 108 177 188

45. MoutaftsiMBrennanPSpectorSATabiZ 2004 Impaired lymphoid chemokine-mediated migration due to a block on the chemokine receptor switch in human cytomegalovirus-infected dendritic cells. J Virol 78 3046 3054

46. ScandellaEMenYLeglerDFGillessenSPriklerL 2004 CCL19/CCL21-triggered signal transduction and migration of dendritic cells requires prostaglandin E2. Blood 103 1595 1601

47. RemoliMEGafaVGiacominiESeveraMLandeR 2007 IFN-beta modulates the response to TLR stimulation in human DC: involvement of IFN regulatory factor-1 (IRF-1) in IL-27 gene expression. Eur J Immunol 37 3499 3508

48. LehnerMStilperAMorhartPHolterW 2008 Plasticity of dendritic cell function in response to prostaglandin E2 (PGE2) and interferon-gamma (IFN-gamma). J Leukoc Biol 83 883 893

49. YenJHKongWGaneaD 2010 IFN-beta inhibits dendritic cell migration through STAT-1-mediated transcriptional suppression of CCR7 and matrix metalloproteinase 9. J Immunol 184 3478 3486

50. BanchereauJBriereFCauxCDavoustJLebecqueS 2000 Immunobiology of dendritic cells. Annu Rev Immunol 18 767 811

51. RandolphGJSanchez-SchmitzGAngeliV 2005 Factors and signals that govern the migration of dendritic cells via lymphatics: recent advances. Springer Semin Immunopathol 26 273 287

52. Sanchez-SanchezNRiol-BlancoLRodriguez-FernandezJL 2006 The multiple personalities of the chemokine receptor CCR7 in dendritic cells. J Immunol 176 5153 5159

53. YoshidaRImaiTHieshimaKKusudaJBabaM 1997 Molecular cloning of a novel human CC chemokine EBI1-ligand chemokine that is a specific functional ligand for EBI1, CCR7. J Biol Chem 272 13803 13809

54. GillMAPaluckaAKBartonTGhaffarFJafriH 2005 Mobilization of plasmacytoid and myeloid dendritic cells to mucosal sites in children with respiratory syncytial virus and other viral respiratory infections. J Infect Dis 191 1105 1115

55. GillMALongKKwonTMunizLMejiasA 2008 Differential recruitment of dendritic cells and monocytes to respiratory mucosal sites in children with influenza virus or respiratory syncytial virus infection. J Infect Dis 198 1667 1676

56. BeyerMBartzHHornerKDothsSKoerner-RettbergC 2004 Sustained increases in numbers of pulmonary dendritic cells after respiratory syncytial virus infection. J Allergy Clin Immunol 113 127 133

57. LukensMVKruijsenDCoenjaertsFEKimpenJLvan BleekGM 2009 Respiratory syncytial virus-induced activation and migration of respiratory dendritic cells and subsequent antigen presentation in the lung-draining lymph node. J Virol 83 7235 7243

58. McGillJVan RooijenNLeggeKL 2008 Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J Exp Med 205 1635 1646

59. GraysonMHRamosMSRohlfingMMKitchensRWangHD 2007 Controls for lung dendritic cell maturation and migration during respiratory viral infection. J Immunol 179 1438 1448

60. LeggeKLBracialeTJ 2003 Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18 265 277

61. AbtMGassertESchneider-SchauliesS 2009 Measles virus modulates chemokine release and chemotactic responses of dendritic cells. J Gen Virol 90 909 914

62. HumrichJYThumannPGreinerSHumrichJHAverbeckM 2007 Vaccinia virus impairs directional migration and chemokine receptor switch of human dendritic cells. Eur J Immunol 37 954 965

63. PrechtelATTurzaNMKobeltDJEisemannJICoffinRS 2005 Infection of mature dendritic cells with herpes simplex virus type 1 dramatically reduces lymphoid chemokine-mediated migration. J Gen Virol 86 1645 1657

64. CollinsPLGrahamBS 2008 Viral and host factors in human respiratory syncytial virus pathogenesis. J Virol 82 2040 2055

65. OlsonMRHartwigSMVargaSM 2008 The number of respiratory syncytial virus (RSV)-specific memory CD8 T cells in the lung is critical for their ability to inhibit RSV vaccine-enhanced pulmonary eosinophilia. J Immunol 181 7958 7968

66. KrappmannDWegenerESunamiYEsenMThielA 2004 The IkappaB kinase complex and NF-kappaB act as master regulators of lipopolysaccharide-induced gene expression and control subordinate activation of AP-1. Mol Cell Biol 24 6488 6500

67. ShaWCLiouHCTuomanenEIBaltimoreD 1995 Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell 80 321 330