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Type I Interferon Signaling Regulates Ly6C Monocytes and Neutrophils during Acute Viral Pneumonia in Mice


Type I interferon (IFN-I) plays a critical role in the homeostasis of hematopoietic stem cells and influences neutrophil influx to the site of inflammation. IFN-I receptor knockout (Ifnar1−/−) mice develop significant defects in the infiltration of Ly6Chi monocytes in the lung after influenza infection (A/PR/8/34, H1N1). Ly6Chi monocytes of wild-type (WT) mice are the main producers of MCP-1 while the alternatively generated Ly6Cint monocytes of Ifnar1−/− mice mainly produce KC for neutrophil influx. As a consequence, Ifnar1−/− mice recruit more neutrophils after influenza infection than do WT mice. Treatment of IFNAR1 blocking antibody on the WT bone marrow (BM) cells in vitro failed to differentiate into Ly6Chi monocytes. By using BM chimeric mice (WT BM into Ifnar1−/− and vice versa), we confirmed that IFN-I signaling in hematopoietic cells is required for the generation of Ly6Chi monocytes. Of note, WT BM reconstituted Ifnar1−/− chimeric mice with increased numbers of Ly6Chi monocytes survived longer than influenza-infected Ifnar1−/− mice. In contrast, WT mice that received Ifnar1−/− BM cells with alternative Ly6Cint monocytes and increased numbers of neutrophils exhibited higher mortality rates than WT mice given WT BM cells. Collectively, these data suggest that IFN-I contributes to resistance of influenza infection by control of monocytes and neutrophils in the lung.


Vyšlo v časopise: Type I Interferon Signaling Regulates Ly6C Monocytes and Neutrophils during Acute Viral Pneumonia in Mice. PLoS Pathog 7(2): e32767. doi:10.1371/journal.ppat.1001304
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001304

Souhrn

Type I interferon (IFN-I) plays a critical role in the homeostasis of hematopoietic stem cells and influences neutrophil influx to the site of inflammation. IFN-I receptor knockout (Ifnar1−/−) mice develop significant defects in the infiltration of Ly6Chi monocytes in the lung after influenza infection (A/PR/8/34, H1N1). Ly6Chi monocytes of wild-type (WT) mice are the main producers of MCP-1 while the alternatively generated Ly6Cint monocytes of Ifnar1−/− mice mainly produce KC for neutrophil influx. As a consequence, Ifnar1−/− mice recruit more neutrophils after influenza infection than do WT mice. Treatment of IFNAR1 blocking antibody on the WT bone marrow (BM) cells in vitro failed to differentiate into Ly6Chi monocytes. By using BM chimeric mice (WT BM into Ifnar1−/− and vice versa), we confirmed that IFN-I signaling in hematopoietic cells is required for the generation of Ly6Chi monocytes. Of note, WT BM reconstituted Ifnar1−/− chimeric mice with increased numbers of Ly6Chi monocytes survived longer than influenza-infected Ifnar1−/− mice. In contrast, WT mice that received Ifnar1−/− BM cells with alternative Ly6Cint monocytes and increased numbers of neutrophils exhibited higher mortality rates than WT mice given WT BM cells. Collectively, these data suggest that IFN-I contributes to resistance of influenza infection by control of monocytes and neutrophils in the lung.


Zdroje

1. JewellNA

VaghefiN

MertzSE

AkterP

PeeblesRSJr

2007 Differential type I interferon induction by respiratory syncytial virus and influenza a virus in vivo. J Virol 81 9790 9800

2. KumagaiY

TakeuchiO

KatoH

KumarH

MatsuiK

2007 Alveolar macrophages are the primary interferon-alpha producer in pulmonary infection with RNA viruses. Immunity 27 240 252

3. SadlerAJ

WilliamsBR

2008 Interferon-inducible antiviral effectors. Nat Rev Immunol 8 559 568

4. DerSD

LauAS

1995 Involvement of the double-stranded-RNA-dependent kinase PKR in interferon expression and interferon-mediated antiviral activity. Proc Natl Acad Sci U S A 92 8841 8845

5. MinJY

KrugRM

2006 The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: Inhibiting the 2′-5′ oligo (A) synthetase/RNase L pathway. Proc Natl Acad Sci U S A 103 7100 7105

6. DittmannJ

StertzS

GrimmD

SteelJ

Garcia-SastreA

2008 Influenza A virus strains differ in sensitivity to the antiviral action of Mx-GTPase. J Virol 82 3624 3631

7. Garcia-SastreA

2004 Identification and characterization of viral antagonists of type I interferon in negative-strand RNA viruses. Curr Top Microbiol Immunol 283 249 280

8. StetsonDB

MedzhitovR

2006 Type I interferons in host defense. Immunity 25 373 381

9. Garcia-SastreA

2006 Antiviral response in pandemic influenza viruses. Emerg Infect Dis 12 44 47

10. KoernerI

KochsG

KalinkeU

WeissS

StaeheliP

2007 Protective role of beta interferon in host defense against influenza A virus. J Virol 81 2025 2030

11. SzretterKJ

GangappaS

BelserJA

ZengH

ChenH

2009 Early control of H5N1 influenza virus replication by the type I interferon response in mice. J Virol 83 5825 5834

12. LinKL

SuzukiY

NakanoH

RamsburgE

GunnMD

2008 CCR2+ monocyte-derived dendritic cells and exudate macrophages produce influenza-induced pulmonary immune pathology and mortality. J Immunol 180 2562 2572

13. SerbinaNV

PamerEG

2006 Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7 311 317

14. EssersMA

OffnerS

Blanco-BoseWE

WaiblerZ

KalinkeU

2009 IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458 904 908

15. SatoT

OnaiN

YoshiharaH

AraiF

SudaT

2009 Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat Med 15 696 700

16. MumyKL

McCormickBA

2009 The role of neutrophils in the event of intestinal inflammation. Curr Opin Pharmacol 9 697 701

17. TateMD

BrooksAG

ReadingPC

2008 The role of neutrophils in the upper and lower respiratory tract during influenza virus infection of mice. Respir Res 9 57

18. TateMD

DengYM

JonesJE

AndersonGP

BrooksAG

2009 Neutrophils ameliorate lung injury and the development of severe disease during influenza infection. J Immunol 183 7441 7450

19. TumpeyTM

Garcia-SastreA

TaubenbergerJK

PaleseP

SwayneDE

2005 Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J Virol 79 14933 14944

20. PerroneLA

PlowdenJK

Garcia-SastreA

KatzJM

TumpeyTM

2008 H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 4 e1000115

21. TumpeyTM

BaslerCF

AguilarPV

ZengH

SolorzanoA

2005 Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310 77 80

22. Garcia-SastreA

DurbinRK

ZhengH

PaleseP

GertnerR

1998 The role of interferon in influenza virus tissue tropism. J Virol 72 8550 8558

23. PriceGE

Gaszewska-MastarlarzA

MoskophidisD

2000 The role of alpha/beta and gamma interferons in development of immunity to influenza A virus in mice. J Virol 74 3996 4003

24. GabrilovichDI

NagarajS

2009 Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9 162 174

25. SwirskiFK

NahrendorfM

EtzrodtM

WildgruberM

Cortez-RetamozoV

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

26. JiaT

LeinerI

DorotheeG

BrandlK

PamerEG

2009 MyD88 and Type I interferon receptor-mediated chemokine induction and monocyte recruitment during Listeria monocytogenes infection. J Immunol 183 1271 1278

27. KoyamaS

IshiiKJ

KumarH

TanimotoT

CobanC

2007 Differential role of TLR- and RLR-signaling in the immune responses to influenza A virus infection and vaccination. J Immunol 179 4711 4720

28. D'AvilaH

MeloRC

ParreiraGG

Werneck-BarrosoE

Castro-Faria-NetoHC

2006 Mycobacterium bovis bacillus Calmette-Guerin induces TLR2-mediated formation of lipid bodies: intracellular domains for eicosanoid synthesis in vivo. J Immunol 176 3087 3097

29. BelperioJA

KeaneMP

BurdickMD

LondheV

XueYY

2002 Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilator-induced lung injury. J Clin Invest 110 1703 1716

30. DawsonTC

BeckMA

KuzielWA

HendersonF

MaedaN

2000 Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am J Pathol 156 1951 1959

31. SakaiS

KawamataH

MantaniN

KogureT

ShimadaY

2000 Therapeutic effect of anti-macrophage inflammatory protein 2 antibody on influenza virus-induced pneumonia in mice. J Virol 74 2472 2476

32. BouchonA

FacchettiF

WeigandMA

ColonnaM

2001 TREM-1 amplifies inflammation and is a crucial mediator of septic shock. Nature 410 1103 1107

33. FoellD

WittkowskiH

VoglT

RothJ

2007 S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol 81 28 37

34. EspinosaA

DardalhonV

BraunerS

AmbrosiA

HiggsR

2009 Loss of the lupus autoantigen Ro52/Trim21 induces tissue inflammation and systemic autoimmunity by disregulating the IL-23-Th17 pathway. J Exp Med 206 1661 1671

35. ShiM

DengW

BiE

MaoK

JiY

2008 TRIM30 alpha negatively regulates TLR-mediated NF-kappa B activation by targeting TAB2 and TAB3 for degradation. Nat Immunol 9 369 377

36. BillharzR

ZengH

ProllSC

KorthMJ

LedererS

2009 The NS1 protein of the 1918 pandemic influenza virus blocks host interferon and lipid metabolism pathways. J Virol 83 10557 10570

37. NaghaviM

WydeP

LitovskyS

MadjidM

AkhtarA

2003 Influenza infection exerts prominent inflammatory and thrombotic effects on the atherosclerotic plaques of apolipoprotein E-deficient mice. Circulation 107 762 768

38. AldridgeJRJr

MoseleyCE

BoltzDA

NegovetichNJ

ReynoldsC

2009 TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci U S A 106 5306 5311

39. HohlTM

RiveraA

LipumaL

GallegosA

ShiC

2009 Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe 6 470 481

40. CraneMJ

Hokeness-AntonelliKL

Salazar-MatherTP

2009 Regulation of inflammatory monocyte/macrophage recruitment from the bone marrow during murine cytomegalovirus infection: role for type I interferons in localized induction of CCR2 ligands. J Immunol 183 2810 2817

41. LeePY

LiY

KumagaiY

XuY

WeinsteinJS

2009 Type I interferon modulates monocyte recruitment and maturation in chronic inflammation. Am J Pathol 175 2023 2033

42. RoseCEJr

SungSS

FuSM

2003 Significant involvement of CCL2 (MCP-1) in inflammatory disorders of the lung. Microcirculation 10 273 288

43. DessingMC

van der SluijsKF

FlorquinS

van der PollT

2007 Monocyte chemoattractant protein 1 contributes to an adequate immune response in influenza pneumonia. Clin Immunol 125 328 336

44. KannanS

HuangH

SeegerD

AudetA

ChenY

2009 Alveolar epithelial type II cells activate alveolar macrophages and mitigate P. Aeruginosa infection. PLoS One 4 e4891

45. NarasarajuT

NgHH

PhoonMC

ChowVT

2009 MCP-1 Antibody Treatment Enhances Damage and Impedes Repair of the Alveolar Epithelium in Influenza Pneumonitis. Am J Respir Cell Mol Biol 42 732 743

46. RaoustE

BalloyV

Garcia-VerdugoI

TouquiL

RamphalR

2009 Pseudomonas aeruginosa LPS or flagellin are sufficient to activate TLR-dependent signaling in murine alveolar macrophages and airway epithelial cells. PLoS One 4 e7259

47. GeissmannF

JungS

LittmanDR

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

48. HeroldS

SteinmuellerM

von WulffenW

CakarovaL

PintoR

2008 Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J Exp Med 205 3065 3077

49. WareLB

MatthayMA

2000 The acute respiratory distress syndrome. N Engl J Med 342 1334 1349

50. WareingMD

SheaAL

InglisCA

DiasPB

SarawarSR

2007 CXCR2 is required for neutrophil recruitment to the lung during influenza virus infection, but is not essential for viral clearance. Viral Immunol 20 369 378

51. MillerAL

StrieterRM

GruberAD

HoSB

LukacsNW

2003 CXCR2 regulates respiratory syncytial virus-induced airway hyperreactivity and mucus overproduction. J Immunol 170 3348 3356

52. NagarkarDR

WangQ

ShimJ

ZhaoY

TsaiWC

2009 CXCR2 is required for neutrophilic airway inflammation and hyperresponsiveness in a mouse model of human rhinovirus infection. J Immunol 183 6698 6707

53. BentoAF

LeiteDF

ClaudinoRF

HaraDB

LealPC

2008 The selective nonpeptide CXCR2 antagonist SB225002 ameliorates acute experimental colitis in mice. J Leukoc Biol 84 1213 1221

54. CraxiA

Di BonaD

CammaC

2003 Interferon-alpha for HBeAg-positive chronic hepatitis B. J Hepatol 39 Suppl 1 S99 105

55. HoofnagleJH

SeeffLB

2006 Peginterferon and ribavirin for chronic hepatitis C. N Engl J Med 355 2444 2451

56. KapposL

FreedmanMS

PolmanCH

EdanG

HartungHP

2007 Effect of early versus delayed interferon beta-1b treatment on disability after a first clinical event suggestive of multiple sclerosis: a 3-year follow-up analysis of the BENEFIT study. Lancet 370 389 397

57. HermeshT

MoltedoB

MoranTM

LopezCB

2010 Antiviral instruction of bone marrow leukocytes during respiratory viral infections. Cell Host Microbe 7 343 353

58. Garcia-SastreA

EgorovA

MatassovD

BrandtS

LevyDE

1998 Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252 324 330

59. GeissGK

SalvatoreM

TumpeyTM

CarterVS

WangX

2002 Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc Natl Acad Sci U S A 99 10736 10741

60. SeoSH

HoffmannE

WebsterRG

2002 Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8 950 954

61. CillonizC

ShinyaK

PengX

KorthMJ

ProllSC

2009 Lethal influenza virus infection in macaques is associated with early dysregulation of inflammatory related genes. PLoS Pathog 5 e1000604

62. KobasaD

JonesSM

ShinyaK

KashJC

CoppsJ

2007 Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445 319 323

63. ShimDH

ChangSY

ParkSM

JangH

CarbisR

2007 Immunogenicity and protective efficacy offered by a ribosomal-based vaccine from Shigella flexneri 2a. Vaccine 25 4828 4836

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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