Potentiation of Epithelial Innate Host Responses by Intercellular Communication

English version České info

The epithelium efficiently attracts immune cells upon infection despite the low number of pathogenic microbes and moderate levels of secreted chemokines per cell. Here we examined whether horizontal intercellular communication between cells may contribute to a coordinated response of the epithelium. Listeria monocytogenes infection, transfection, and microinjection of individual cells within a polarized intestinal epithelial cell layer were performed and activation was determined at the single cell level by fluorescence microscopy and flow cytometry. Surprisingly, chemokine production after L. monocytogenes infection was primarily observed in non-infected epithelial cells despite invasion-dependent cell activation. Whereas horizontal communication was independent of gap junction formation, cytokine secretion, ion fluxes, or nitric oxide synthesis, NADPH oxidase (Nox) 4-dependent oxygen radical formation was required and sufficient to induce indirect epithelial cell activation. This is the first report to describe epithelial cell-cell communication in response to innate immune activation. Epithelial communication facilitates a coordinated infectious host defence at the very early stage of microbial infection.

Vyšlo v časopise: Potentiation of Epithelial Innate Host Responses by Intercellular Communication. PLoS Pathog 6(11): e32767. doi:10.1371/journal.ppat.1001194
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001194

Souhrn

Zdroje

1. LotzM

MenardS

HornefM

2007 Innate immune recognition on the intestinal mucosa. Int J Med Microbiol 297 379 392

2. LeeJ

MoJH

ShenC

RuckerAN

RazE

2007 Toll-like receptor signaling in intestinal epithelial cells contributes to colonic homoeostasis. Curr Opin Gastroenterol 23 27 31

3. KobayashiKS

ChamaillardM

OguraY

HenegariuO

InoharaN

2005 Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307 731 734

4. SchillingJD

MartinSM

HungCS

LorenzRG

HultgrenSJ

2003 Toll-like receptor 4 on stromal and hematopoietic cells mediates innate resistance to uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 100 4203 4208

5. AndoneguiG

BonderCS

GreenF

MullalySC

ZbytnuikL

2003 Endothelium-derived Toll-like receptor-4 is the key molecule in LPS-induced neutrophil sequestration into lungs. J Clin Invest 111 1011 1020

6. FreitagNE

PortGC

MinerMD

2009 Listeria monocytogenes - from saprophyte to intracellular pathogen. Nat Rev Microbiol 7 623 628

7. McCaffreyRL

FawcettP

O'RiordanM

LeeKD

HavellEA

2004 A specific gene expression program triggered by Gram-positive bacteria in the cytosol. Proc Natl Acad Sci U S A 101 11386 11391

8. LeberJH

CrimminsGT

RaghavanS

Meyer-MorseNP

CoxJS

2008 Distinct TLR- and NLR-mediated transcriptional responses to an intracellular pathogen. PLoS Pathog 4 e6

9. WarrenSE

MaoDP

RodriguezAE

MiaoEA

AderemA

2008 Multiple Nod-like receptors activate caspase 1 during Listeria monocytogenes infection. J Immunol 180 7558 7564

10. CorrSC

O'NeillLA

2009 Listeria monocytogenes infection in the face of innate immunity. Cell Microbiol

11. DietrichG

BubertA

GentschevI

SokolovicZ

SimmA

1998 Delivery of antigen-encoding plasmid DNA into the cytosol of macrophages by attenuated suicide Listeria monocytogenes. Nat Biotechnol 16 181 185

12. KohlerR

BubertA

GoebelW

SteinertM

HackerJ

2000 Expression and use of the green fluorescent protein as a reporter system in Legionella pneumophila. Mol Gen Genet 262 1060 1069

13. HerskovitsAA

AuerbuchV

PortnoyDA

2007 Bacterial ligands generated in a phagosome are targets of the cytosolic innate immune system. PLoS Pathog 3 e51

14. GekaraNO

WestphalK

MaB

RohdeM

GroebeL

2007 The multiple mechanisms of Ca2+ signalling by listeriolysin O, the cholesterol-dependent cytolysin of Listeria monocytogenes. Cell Microbiol 9 2008 2021

15. TsuchiyaK

KawamuraI

TakahashiA

NomuraT

KohdaC

2005 Listeriolysin O-induced membrane permeation mediates persistent interleukin-6 production in Caco-2 cells during Listeria monocytogenes infection in vitro. Infect Immun 73 3869 3877

16. ChenK

KirberMT

XiaoH

YangY

KeaneyJFJr

2008 Regulation of ROS signal transduction by NADPH oxidase 4 localization. J Cell Biol 181 1129 1139

17. LeaphartCL

QureshiF

CetinS

LiJ

DubowskiT

2007 Interferon-gamma inhibits intestinal restitution by preventing gap junction communication between enterocytes. Gastroenterology 132 2395 2411

18. MartinFJ

PrinceAS

2008 TLR2 regulates gap junction intercellular communication in airway cells. J Immunol 180 4986 4993

19. EyB

EykingA

GerkenG

PodolskyDK

CarioE

2009 TLR2 mediates gap junctional intercellular communication through connexin-43 in intestinal epithelial barrier injury. J Biol Chem 284 22332 22343

20. WuF

TymlK

WilsonJX

2008 iNOS expression requires NADPH oxidase-dependent redox signaling in microvascular endothelial cells. J Cell Physiol 217 207 214

21. PatelSJ

KingKR

CasaliM

YarmushML

2009 DNA-triggered innate immune responses are propagated by gap junction communication. Proc Natl Acad Sci U S A 106 12867 12872

22. Shetron-RamaLM

MarquisH

BouwerHG

FreitagNE

2002 Intracellular induction of Listeria monocytogenes actA expression. Infect Immun 70 1087 1096

23. LecuitM

DramsiS

GottardiC

Fedor-ChaikenM

GumbinerB

1999 A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. Embo J 18 3956 3963

24. Tran Van NhieuG

ClairC

BruzzoneR

MesnilM

SansonettiP

2003 Connexin-dependent inter-cellular communication increases invasion and dissemination of Shigella in epithelial cells. Nat Cell Biol 5 720 726

25. SegalAW

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

26. SundaresanM

YuZX

FerransVJ

IraniK

FinkelT

1995 Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270 296 299

27. ThannickalVJ

FanburgBL

2000 Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279 L1005 1028

28. KimuraH

SawadaT

OshimaS

KozawaK

IshiokaT

2005 Toxicity and roles of reactive oxygen species. Curr Drug Targets Inflamm Allergy 4 489 495

29. AllenRG

TresiniM

2000 Oxidative stress and gene regulation. Free Radic Biol Med 28 463 499

30. ThomasSR

ChenK

KeaneyJFJr

2002 Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J Biol Chem 277 6017 6024

31. El-NajjarN

ChatilaM

MoukademH

VuorelaH

OckerM

2009 Reactive oxygen species mediate thymoquinone-induced apoptosis and activate ERK and JNK signaling. Apoptosis

32. SongHJ

KimJS

LeeMJ

NamYS

SohnUD

2007 Reactive oxygen species mediate ET-1-induced activation of ERK1/2 signaling in cultured feline esophageal smooth muscle cells. Arch Pharm Res 30 1080 1087

33. McCubreyJA

LahairMM

FranklinRA

2006 Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid Redox Signal 8 1775 1789

34. BrarSS

KennedyTP

SturrockAB

HuecksteadtTP

QuinnMT

2002 NADPH oxidase promotes NF-kappaB activation and proliferation in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 282 L782 795

35. JinS

RayRM

JohnsonLR

2008 TNF-alpha/cycloheximide-induced apoptosis in intestinal epithelial cells requires Rac1-regulated reactive oxygen species. Am J Physiol Gastrointest Liver Physiol 294 G928 937

36. AmmendolaR

RuocchioMR

ChiricoG

RussoL

De FeliceC

2002 Inhibition of NADH/NADPH oxidase affects signal transduction by growth factor receptors in normal fibroblasts. Arch Biochem Biophys 397 253 257

37. RichardsSM

ClarkEA

2009 BCR-induced superoxide negatively regulates B-cell proliferation and T-cell-independent type 2 Ab responses. Eur J Immunol 39 3395 3403

38. Mendez-SamperioP

PerezA

TorresL

2009 Role of reactive oxygen species (ROS) in Mycobacterium bovis bacillus Calmette Guerin-mediated up-regulation of the human cathelicidin LL-37 in A549 cells. Microb Pathog 47 252 257

39. YangCS

ShinDM

KimKH

LeeZW

LeeCH

2009 NADPH oxidase 2 interaction with TLR2 is required for efficient innate immune responses to mycobacteria via cathelicidin expression. J Immunol 182 3696 3705

40. Owusu-AnsahE

BanerjeeU

2009 Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461 537 541

41. RyuJH

HaEM

OhCT

SeolJH

BreyPT

2006 An essential complementary role of NF-kappaB pathway to microbicidal oxidants in Drosophila gut immunity. Embo J 25 3693 3701

42. NiethammerP

GrabherC

LookAT

MitchisonTJ

2009 A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459 996 999

43. MillarTM

PhanV

TibblesLA

2007 ROS generation in endothelial hypoxia and reoxygenation stimulates MAP kinase signaling and kinase-dependent neutrophil recruitment. Free Radic Biol Med 42 1165 1177

44. Ogier-DenisE

MkaddemSB

VandewalleA

2008 NOX enzymes and Toll-like receptor signaling. Semin Immunopathol 30 291 300

45. MatsuzawaA

SaegusaK

NoguchiT

SadamitsuC

NishitohH

2005 ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat Immunol 6 587 592

46. LambethJD

2004 NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4 181 189

47. ParkHS

JungHY

ParkEY

KimJ

LeeWJ

2004 Cutting edge: direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-kappa B. J Immunol 173 3589 3593

48. PicardC

PuelA

BonnetM

KuCL

BustamanteJ

2003 Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 299 2076 2079

49. LipinskiS

TillA

SinaC

ArltA

GrasbergerH

2009 DUOX2-derived reactive oxygen species are effectors of NOD2-mediated antibacterial responses. J Cell Sci 122 3522 3530

50. TattoliI

CarneiroLA

JehannoM

MagalhaesJG

ShuY

2008 NLRX1 is a mitochondrial NOD-like receptor that amplifies NF-kappaB and JNK pathways by inducing reactive oxygen species production. EMBO Rep 9 293 300

51. DostertC

PetrilliV

Van BruggenR

SteeleC

MossmanBT

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

52. SerranderL

CartierL

BedardK

BanfiB

LardyB

2007 NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem J 406 105 114

53. ParkHS

ChunJN

JungHY

ChoiC

BaeYS

2006 Role of NADPH oxidase 4 in lipopolysaccharide-induced proinflammatory responses by human aortic endothelial cells. Cardiovasc Res 72 447 455

54. LiJ

StouffsM

SerranderL

BanfiB

BettiolE

2006 The NADPH oxidase NOX4 drives cardiac differentiation: Role in regulating cardiac transcription factors and MAP kinase activation. Mol Biol Cell 17 3978 3988

55. GoettschC

GoettschW

MullerG

SeebachJ

SchnittlerHJ

2009 Nox4 overexpression activates reactive oxygen species and p38 MAPK in human endothelial cells. Biochem Biophys Res Commun

56. KumarA

WuH

Collier-HyamsLS

HansenJM

LiT

2007 Commensal bacteria modulate cullin-dependent signaling via generation of reactive oxygen species. Embo J 26 4457 4466

57. DarjiA

ChakrabortyT

NiebuhrK

TsonisN

WehlandJ

1995 Hyperexpression of listeriolysin in the nonpathogenic species Listeria innocua and high yield purification. J Biotechnol 43 205 212

58. BensM

BogdanovaA

CluzeaudF

MiquerolL

KerneisS

1996 Transimmortalized mouse intestinal cells (m-ICc12) that maintain a crypt phenotype. Am J Physiol 270 C1666 1674

59. ParkSF

StewartGS

1990 High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene 94 129 132

60. HaufN

GoebelW

FiedlerF

SokolovicZ

KuhnM

1997 Listeria monocytogenes infection of P388D1 macrophages results in a biphasic NF-kappaB (RelA/p50) activation induced by lipoteichoic acid and bacterial phospholipases and mediated by IkappaBalpha and IkappaBbeta degradation. Proc Natl Acad Sci U S A 94 9394 9399

61. SlaghuisJ

GoetzM

EngelbrechtF

GoebelW

2004 Inefficient replication of Listeria innocua in the cytosol of mammalian cells. J Infect Dis 189 393 401