Neutrophil-Derived CCL3 Is Essential for the Rapid Recruitment of Dendritic Cells to the Site of Inoculation in Resistant Mice
Neutrophils are rapidly and massively recruited to sites of microbial infection, where they can influence the recruitment of dendritic cells. Here, we have analyzed the role of neutrophil released chemokines in the early recruitment of dendritic cells (DCs) in an experimental model of Leishmania major infection. We show in vitro, as well as during infection, that the parasite induced the expression of CCL3 selectively in neutrophils from L. major resistant mice. Neutrophil-secreted CCL3 was critical in chemotaxis of immature DCs, an effect lost upon CCL3 neutralisation. Depletion of neutrophils prior to infection, as well as pharmacological or genetic inhibition of CCL3, resulted in a significant decrease in DC recruitment at the site of parasite inoculation. Decreased DC recruitment in CCL3−/− mice was corrected by the transfer of wild type neutrophils at the time of infection. The early release of CCL3 by neutrophils was further shown to have a transient impact on the development of a protective immune response. Altogether, we identified a novel role for neutrophil-secreted CCL3 in the first wave of DC recruitment to the site of infection with L. major, suggesting that the selective release of neutrophil-secreted chemokines may regulate the development of immune response to pathogens.
Vyšlo v časopise:
Neutrophil-Derived CCL3 Is Essential for the Rapid Recruitment of Dendritic Cells to the Site of Inoculation in Resistant Mice. PLoS Pathog 6(2): e32767. doi:10.1371/journal.ppat.1000755
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000755
Souhrn
Neutrophils are rapidly and massively recruited to sites of microbial infection, where they can influence the recruitment of dendritic cells. Here, we have analyzed the role of neutrophil released chemokines in the early recruitment of dendritic cells (DCs) in an experimental model of Leishmania major infection. We show in vitro, as well as during infection, that the parasite induced the expression of CCL3 selectively in neutrophils from L. major resistant mice. Neutrophil-secreted CCL3 was critical in chemotaxis of immature DCs, an effect lost upon CCL3 neutralisation. Depletion of neutrophils prior to infection, as well as pharmacological or genetic inhibition of CCL3, resulted in a significant decrease in DC recruitment at the site of parasite inoculation. Decreased DC recruitment in CCL3−/− mice was corrected by the transfer of wild type neutrophils at the time of infection. The early release of CCL3 by neutrophils was further shown to have a transient impact on the development of a protective immune response. Altogether, we identified a novel role for neutrophil-secreted CCL3 in the first wave of DC recruitment to the site of infection with L. major, suggesting that the selective release of neutrophil-secreted chemokines may regulate the development of immune response to pathogens.
Zdroje
1. NathanC
2006 Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6 173 182
2. AppelbergR
2007 Neutrophils and intracellular pathogens: beyond phagocytosis and killing. Trends Microbiol 15 87 92
3. SacksD
Noben-TrauthN
2002 The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol 2 845 858
4. BeilWJ
Meinardus-HagerG
NeugebauerDC
SorgC
1992 Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice. J Leukoc Biol 52 135 142
5. Tacchini-CottierF
ZweifelC
BelkaidY
MukankundiyeC
VaseiM
2000 An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. J Immunol 165 2628 2636
6. PetersNC
EgenJG
SecundinoN
DebrabantA
KimblinN
2008 In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321 970 974
7. Ribeiro-GomesFL
OteroAC
GomesNA
Moniz-De-SouzaMC
Cysne-FinkelsteinL
2004 Macrophage interactions with neutrophils regulate Leishmania major infection. J Immunol 172 4454 4462
8. McFarlaneE
PerezC
CharmoyM
AllenbachC
CarterKC
2008 Neutrophils contribute to development of a protective immune response during onset of infection with Leishmania donovani. Infect Immun 76 532 541
9. CharmoyM
MegnekouR
AllenbachC
ZweifelC
PerezC
2007 Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol 82 288 299
10. BaldwinT
HenriS
CurtisJ
O'KeeffeM
VremecD
2004 Dendritic cell populations in Leishmania major-infected skin and draining lymph nodes. Infect Immun 72 1991 2001
11. BrewigN
KissenpfennigA
MalissenB
VeitA
BickertT
2009 Priming of CD8+ and CD4+ T cells in experimental leishmaniasis is initiated by different dendritic cell subtypes. J Immunol 182 774 783
12. SoongL
2008 Modulation of dendritic cell function by Leishmania parasites. J Immunol 180 4355 4360
13. StoitznerP
PfallerK
StosselH
RomaniN
2002 A close-up view of migrating Langerhans cells in the skin. J Invest Dermatol 118 117 125
14. ShklovskayaE
RoedigerB
Fazekas de St GrothB
2008 Epidermal and dermal dendritic cells display differential activation and migratory behavior while sharing the ability to stimulate CD4+ T cell proliferation in vivo. J Immunol 181 418 430
15. RandolphGJ
OchandoJ
Partida-SanchezS
2008 Migration of dendritic cell subsets and their precursors. Annu Rev Immunol 26 293 316
16. LeonB
Lopez-BravoM
ArdavinC
2005 Monocyte-derived dendritic cells. Semin Immunol 17 313 318
17. DieuMC
VanbervlietB
VicariA
BridonJM
OldhamE
1998 Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 188 373 386
18. PowerCA
ChurchDJ
MeyerA
AlouaniS
ProudfootAE
1997 Cloning and characterization of a specific receptor for the novel CC chemokine MIP-3alpha from lung dendritic cells. J Exp Med 186 825 835
19. SozzaniS
SallustoF
LuiniW
ZhouD
PiemontiL
1995 Migration of dendritic cells in response to formyl peptides, C5a, and a distinct set of chemokines. J Immunol 155 3292 3295
20. CassatellaMA
1999 Neutrophil-derived proteins: selling cytokines by the pound. Adv Immunol 73 369 509
21. LarsenCP
SteinmanRM
Witmer-PackM
HankinsDF
MorrisPJ
1990 Migration and maturation of Langerhans cells in skin transplants and explants. J Exp Med 172 1483 1493
22. BelkaidY
JouinH
MilonG
1996 A method to recover, enumerate and identify lymphomyeloid cells present in an inflammatory dermal site: a study in laboratory mice. J Immunol Methods 199 5 25
23. LeonB
Lopez-BravoM
ArdavinC
2007 Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26 519 531
24. FrauenschuhA
PowerCA
DeruazM
FerreiraBR
SilvaJS
2007 Molecular cloning and characterization of a highly selective chemokine-binding protein from the tick Rhipicephalus sanguineus. J Biol Chem 282 27250 27258
25. DeruazM
FrauenschuhA
AlessandriAL
DiasJM
CoelhoFM
2008 Ticks produce highly selective chemokine binding proteins with antiinflammatory activity. J Exp Med
26. SatoN
AhujaSK
QuinonesM
KosteckiV
ReddickRL
2000 CC chemokine receptor (CCR)2 is required for langerhans cell migration and localization of T helper cell type 1 (Th1)-inducing dendritic cells. Absence of CCR2 shifts the Leishmania major-resistant phenotype to a susceptible state dominated by Th2 cytokines, b cell outgrowth, and sustained neutrophilic inflammation. J Exp Med 192 205 218
27. YangD
ChenQ
ChertovO
OppenheimJJ
2000 Human neutrophil defensins selectively chemoattract naive T and immature dendritic cells. J Leukoc Biol 68 9 14
28. KasamaT
StrieterRM
StandifordTJ
BurdickMD
KunkelSL
1993 Expression and regulation of human neutrophil-derived macrophage inflammatory protein 1 alpha. J Exp Med 178 63 72
29. BennounaS
BlissSK
CurielTJ
DenkersEY
2003 Cross-talk in the innate immune system: neutrophils instruct recruitment and activation of dendritic cells during microbial infection. J Immunol 171 6052 6058
30. AntoniaziS
PriceHP
KropfP
FreudenbergMA
GalanosC
2004 Chemokine gene expression in toll-like receptor-competent and -deficient mice infected with Leishmania major. Infect Immun 72 5168 5174
31. QuinonesMP
EstradaCA
JimenezF
MartinezH
WillmonO
2007 CCL2-independent role of CCR2 in immune responses against Leishmania major. Parasite Immunol 29 211 217
32. SantiagoHC
OliveiraCF
SantiagoL
FerrazFO
de SouzaDG
2004 Involvement of the chemokine RANTES (CCL5) in resistance to experimental infection with Leishmania major. Infect Immun 72 4918 4923
33. MorelC
BadellE
AbadieV
RobledoM
SetterbladN
2008 Mycobacterium bovis BCG-infected neutrophils and dendritic cells cooperate to induce specific T cell responses in humans and mice. Eur J Immunol 38 437 447
34. van GisbergenKP
Sanchez-HernandezM
GeijtenbeekTB
van KooykY
2005 Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J Exp Med 201 1281 1292
35. EkenC
GasserO
ZenhaeusernG
OehriI
HessC
2008 Polymorphonuclear neutrophil-derived ectosomes interfere with the maturation of monocyte-derived dendritic cells. J Immunol 180 817 824
36. NgLG
HsuA
MandellMA
RoedigerB
HoellerC
2008 Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLoS Pathog 4 e1000222 doi:10.1371/journal.ppat.1000222
37. RitterU
MeissnerA
ScheidigC
KornerH
2004 CD8 alpha- and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. Eur J Immunol 34 1542 1550
38. IezziG
FrohlichA
ErnstB
AmpenbergerF
SaelandS
2006 Lymph node resident rather than skin-derived dendritic cells initiate specific T cell responses after Leishmania major infection. J Immunol 177 1250 1256
39. ZhangN
SchroppelB
ChenD
FuS
HudkinsKL
2003 Adenovirus transduction induces expression of multiple chemokines and chemokine receptors in murine beta cells and pancreatic islets. Am J Transplant 3 1230 1241
40. InabaK
SteinmanRM
PackMW
AyaH
InabaM
1992 Identification of proliferating dendritic cell precursors in mouse blood. J Exp Med 175 1157 1167
41. LopezAF
StrathM
SandersonCJ
1984 Differentiation antigens on mouse eosinophils and neutrophils identified by monoclonal antibodies. Br J Haematol 57 489 494
42. Tacchini-CottierF
AllenbachC
OttenLA
RadtkeF
2004 Notch1 expression on T cells is not required for CD4+ T helper differentiation. Eur J Immunol 34 1588 1596
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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