Quantitative Subcellular Proteome and Secretome Profiling of Influenza A Virus-Infected Human Primary Macrophages

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Influenza A viruses are important pathogens that cause acute respiratory diseases and annual epidemics in humans. Macrophages recognize influenza A virus infection with their pattern recognition receptors, and are involved in the activation of proper innate immune response. Here, we have used high-throughput subcellular proteomics combined with bioinformatics to provide a global view of host cellular events that are activated in response to influenza A virus infection in human primary macrophages. We show that viral infection regulates the expression and/or subcellular localization of more than one thousand host proteins at early phases of infection. Our data reveals that there are dramatic changes in mitochondrial and nuclear proteomes in response to infection. We show that a rapid cytoplasmic leakage of lysosomal proteins, including cathepsins, followed by their secretion, contributes to inflammasome activation and apoptosis seen in the infected macrophages. Also, our results demonstrate that P2X₇ receptor and src tyrosine kinase activity are essential for inflammasome activation during influenza A virus infection. Finally, we show that influenza A virus infection is associated with robust secretion of different danger-associated molecular patterns (DAMPs) suggesting an important role for DAMPs in host response to influenza A virus infection. In conclusion, our high-throughput quantitative proteomics study provides important new insight into host-response against influenza A virus infection in human primary macrophages.

Vyšlo v časopise: Quantitative Subcellular Proteome and Secretome Profiling of Influenza A Virus-Infected Human Primary Macrophages. PLoS Pathog 7(5): e32767. doi:10.1371/journal.ppat.1001340
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001340

Souhrn

Zdroje

1. AkiraS

UematsuS

TakeuchiO

2006 Pathogen recognition and innate immunity. Cell 124 783 801

2. KawaiT

AkiraS

2006 Innate immune recognition of viral infection. Nat Immunol 7 131 137

3. 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

4. PirhonenJ

SarenevaT

KurimotoM

JulkunenI

MatikainenS

1999 Virus infection activates IL-1β and IL-18 production in human macrophages by a caspase-1-dependent pathway. J Immunol 162 7322 7329

5. PirhonenJ

SarenevaT

JulkunenI

MatikainenS

2001 Virus infection induces proteolytic processing of IL-18 in human macrophages via caspase-1 and caspase-3 activation. Eur J Immunol 31 726 733

6. DinarelloCA

2009 Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 27 519 550

7. MartinonF

BurnsK

TschoppJ

2002 The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol Cell 10 417 426

8. MartinonF

MayorA

TschoppJ

2009 The inflammasomes: guardians of the body. Annu Rev Immunol 27 229 265

9. HornungV

LatzE

2010 Intracellular DNA recognition. Nat Rev Immunol 10 123 130

10. AllenIC

ScullMA

MooreCB

HollEK

McElvania-TeKippeE

2009 The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30 556 565

11. IchinoheT

LeeHK

OguraY

FlavellR

IwasakiA

2009 Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 206 79 87

12. ThomasPG

DashP

AldridgeJRJr

EllebedyAH

ReynoldsC

2009 The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30 566 575

13. ChoudharyC

MannM

2010 Decoding signalling networks by mass spectrometry-based proteomics. Nat Rev Mol Cell Biol 11 427 439

14. LuberCA

CoxJ

LauterbachH

FanckeB

SelbachM

2010 Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 32 279 289

15. TrostM

EnglishL

LemieuxS

CourcellesM

DesjardinsM

2009 The phagosomal proteome in interferon-γ-activated macrophages. Immunity 30 143 154

16. EmmottE

WiseH

LoucaidesEM

MatthewsDA

DigardP

2010 Quantitative proteomics using SILAC coupled to LC-MS/MS reveals changes in the nucleolar proteome in influenza A virus infected cells. J Proteome Res 9 5335 5345

17. QattanAT

MulveyC

CrawfordM

NataleDA

Godovac-ZimmermannJ

2010 Quantitative organelle proteomics of MCF-7 breast cancer cells reveals multiple subcellular locations for proteins in cellular functional processes. J Proteome Res 9 495 508

18. WatanabeT

WatanabeS

KawaokaY

2010 Cellular networks involved in the influenza virus life cycle. Cell Host Microbe 7 427 439

19. KellerM

RüeggA

WernerS

BeerH-D

2008 Active caspase-1 is a regulator of unconventional protein secretion. Cell 132 818 831

20. HornungV

BauernfeindF

HalleA

SamstadEO

KonoH

2008 Silica crystals and aluminium salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9 847 856

21. SolleM

LabasiJ

PerregauxDG

StamE

PetrushovaN

2001 Altered cytokine production in mice lacking P2X7 receptors. J Biol Chem 276 125 132

22. MariathasanS

WeissDS

NewtonK

McBrideJ

O'RourkeK

2006 Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440 228 232

23. RintahakaJ

WiikD

KovanenPE

AleniusH

MatikainenS

2008 Cytosolic antiviral RNA recognition pathway activates caspases 1 and 3. J Immunol 180 1749 1757

24. CruzCM

RinnaA

FormanHJ

VenturaALM

PersechiniPM

2007 ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J Biol Chem 282 2871 2879

25. DostertC

PétrilliV

Van BruggenR

SteeleC

MossmanBT

2008 Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320 674 677

26. GrossO

PoeckH

BscheiderM

DostertC

HannesschlägerN

2009 Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 459 433 436

27. GiannoniE

TaddeiML

ChiarugiP

2010 Src redox regulation: again in the front line. Free Radic Biol Med 49 516 527

28. HaoL

SakuraiA

WatanabeT

SorensenE

NidomCA

2008 Drosofila RNAi screen identifies host genes important for influenza virus replication. Nature 454 890 893

29. BrassAL

HuangI-C

BenitaY

JohnSP

KrishnanMN

2009 The IFITM proteins mediate cellular resistance to Influenza A H1N1 virus, West Nile Virus, and Dengue Virus. Cell 139 1243 1254

30. ShapiraSD

Gat-ViksI

ShumBOV

DricotA

de GraceMM

2009 A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 139 1255 1267

31. SuiHY

ZhaoGY

HuangJD

JinDY

YuenKY

2009 Small interfering RNA targeting m2 gene induces effective and long term inhibition of influenza A virus replication. PLoS One 4 e5671

32. KönigR

StertzS

ZhouY

InoueA

HoffmanH-H

2010 Human host factors required for influenza virus replication. Nature 463 813 817

33. KarlasA

MachuyN

ShinY

PleissnerK-P

ArtariniA

2010 Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 463 818 822

34. LiuN

SongW

WangP

LeeK

ChanW

2008 Proteomics analysis of differential expression of cellular proteins in response to avian H9N2 virus infection in human cells. Proteomics 8 1851 1858

35. VesterD

RappE

GadeD

GenzelY

ReichlU

2009 Quantitative analysis of cellular proteome alterations in human influenza A virus-infected mammalian cell lines. Proteomics 9 3316 3327

36. van DiepenA

BrandHK

SamaI

LambooyLHJ

van den HeuvelLP

2010 Quantitative proteome profiling of respiratory virus-infected lung epithelial cells. J Proteomics 73 1680 1693

37. CoombsKM

BerardA

XuW

KrokhinO

MengX

2010 Quantitative proteomic analyses of influenza virus-infected cultured human lung cells. J Virol 84 10888 10906

38. EmmottE

RodgersMA

MacdonaldA

McCroryS

AjuhP

2010 Quantitative proteomics using stable isotope labeling with amino acids in cell culture reveals changes in the cytoplasmic, nuclear, and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus. Mol Cell Proteomics 9 1920 1936

39. MundayDC

EmmottE

SurteesR

LardeauC-H

WuW

2010 Quantitative proteomic analysis of A549 cells infected with human respiratory syncytial virus. Mol Cell Proteomics 9 2438 2459

40. ÖhmanT

RintahakaJ

KalkkinenN

MatikainenS

NymanTA

2009 Actin and RIG-I/MAVS signaling components translocate to mitochondria upon influenza A virus infection of human primary macrophages. J Immunol 182 5682 5692

41. KannegantiT-D

Body-MalapelM

AmerA

ParkJ-H

WhitfieldJ

2006 Critical role for cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J Biol Chem 281 36560 36568

42. IchinoheT

PangIK

IwasakiA

2010 Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat Immunol 11 404 410

43. ZhouR

TardivelA

ThorensB

ChoiI

TschoppJ

2010 Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 11 136 140

44. ShioMT

EisenbarthSC

SavariaM

VinetAF

BellemareMJ

2009 Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog 5 e1000559

45. DiazB

ShaniG

PassI

AndersonD

QuintavalleM

2009 Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci Signal 2 ra53

46. JohanssonA-C

AppelqvistH

NilssonC

KågedalK

RobergK

2010 Regulation of apoptosis-associated lysosomal membrane permeabilization. Apoptosis 15 527 540

47. NickelW

RabouilleC

2009 Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 10 148 155

48. BianchiME

2007 DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81 1 5

49. ChowVW

MattsonMP

WongPC

GleichmannM

2010 An overview of APP processing enzymes and products. Neuromolecular Med 12 1 12

50. HalleA

HornungV

PetzoldGC

StewartCR

MonksBG

2008 The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nature Immunol 9 857 865

51. Meyer-LuehmannM

Spires-JonesTL

PradaC

Garcia-AllozaM

de CalignonA

2008 Rapid appearance and local toxicity of amyloid-β plaques in a mouse model of Alzheimer's disease. Nature 451 720 724

52. YanaiH

BanT

WangZ

ChoiMK

KawamuraT

2009 HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 462 99 103

53. SatoS

St-PierreC

BhaumikP

NieminenJ

2009 Galectins in innate immunity: dual functions of hos soluble β-galactoside-binding lectins as damage-associated molecular patterns (DAMPs) and as receptors for pathogen-associated molecular patterns (PAMPs). Immunol Rev 230 172 187

54. EliasJE

GygiSP

2007 Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4 207 214

55. BackesC

KellerA

KuentzerJ

KneisslB

ComtesseN

2007 GeneTrail—advanced gene set enrichment analysis. Nucleic Acids Res 35 W186 W192

56. JensenLJ

KuhnM

StarkM