Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response

PLoS Pathogens

Volumn 8, Issue 2, 2012, Pages

  Ribeiro Gomes, Flavia L ^a   Peters, Nathan C ^a   Debrabant, Alain ^b   Sacks, David L ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CD45 ANTIGEN; ELASTASE; LANGERIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELOPEROXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; DERMIS; FEMALE; INFLAMMATORY CELL; LANGERHANS CELL; LEISHMANIASIS; MACROPHAGE; MONOCYTE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROMASTIGOTE; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; CELL SEPARATION; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LEISHMANIA; PARASITOLOGY; SKIN LEISHMANIASIS;

ARTHROPODA; LEISHMANIA MAJOR; MUS; PHLEBOTOMINAE;

ADOPTIVE TRANSFER; ANIMALS; APOPTOSIS; CELL SEPARATION; DENDRITIC CELLS; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; LEISHMANIA; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED C57BL; NEUTROPHILS;

EID: 84860895881     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002536     Document Type: Article

References (55)

1. Sacks D, Anderson C, (2004) Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Immunol Rev 201: 225-238.
2. Belkaid Y, Mendez S, Lira R, Kadambi N, Milon G, et al. (2000) A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J Immunol 165: 969-977.
3. Laskay T, van Zandbergen G, Solbach W, (2008) Neutrophil granulocytes as host cells and transport vehicles for intracellular pathogens: apoptosis as infection-promoting factor. Immunobiology 213: 183-191.
4. Peters NC, Sacks DL, (2009) The impact of vector-mediated neutrophil recruitment on cutaneous leishmaniasis. Cell Microbiol 11: 1290-1296.
5. Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N, et al. (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321: 970-974.
6. Kennedy AD, DeLeo FR, (2009) Neutrophil apoptosis and the resolution of infection. Immunol Res 43: 25-61.
7. Nauseef WM, (2007) How human neutrophils kill and degrade microbes: an integrated view. Immunol Rev 219: 88-102.
8. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, et al. (2000) The neutrophil as a cellular source of chemokines. Immunol Rev 177: 195-203.
9. Yang D, Chen Q, Chertov O, Oppenheim JJ, (2000) Human neutrophil defensins selectively chemoattract naive T and immature dendritic cells. J Leukoc Biol 68: 9-14.
10. Megiovanni AM, Sanchez F, Robledo-Sarmiento M, Morel C, Gluckman JC, et al. (2006) Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J Leukoc Biol 79: 977-988.
11. Blomgran R, Ernst JD, (2011) Lung Neutrophils Facilitate Activation of Naive Antigen-Specific CD4+ T Cells during Mycobacterium tuberculosis Infection. J Immunol 186: 7110-7119.
12. Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, et al. (2000) Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med 191: 423-434.
13. Steinman RM, Turley S, Mellman I, Inaba K, (2000) The induction of tolerance by dendritic cells that have captured apoptotic cells. J Exp Med 191: 411-416.
14. Stuart LM, Lucas M, Simpson C, Lamb J, Savill J, et al. (2002) Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J Immunol 168: 1627-1635.
15. Leon B, Lopez-Bravo M, Ardavin C, (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.
16. Laskay T, van Zandbergen G, Solbach W, (2003) Neutrophil granulocytes-Trojan horses for Leishmania major and other intracellular microbes? Trends Microbiol 11: 210-214.
17. van Zandbergen G, Klinger M, Mueller A, Dannenberg S, Gebert A, et al. (2004) Cutting Edge: Neutrophil Granulocyte Serves as a Vector for Leishmania Entry into Macrophages. J Immunol 173: 6521-6525.
18. Faust N, Varas F, Kelly LM, Heck S, Graf T, (2000) Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 96: 719-726.
19. Egan CE, Sukhumavasi W, Bierly AL, Denkers EY, (2008) Understanding the multiple functions of Gr-1(+) cell subpopulations during microbial infection. Immunol Res 40: 35-48.
20. Wojtasiak M, Pickett DL, Tate MD, Londrigan SL, Bedoui S, et al. (2010) Depletion of Gr-1+, but not Ly6G+, immune cells exacerbates virus replication and disease in an intranasal model of herpes simplex virus type 1 infection. J Gen Virol 91: 2158-2166.
21. Merad M, Ginhoux F, Collin M, (2008) Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 8: 935-947.
22. Peters NC, Kimblin N, Secundino N, Kamhawi S, Lawyer P, et al. (2009) Vector transmission of leishmania abrogates vaccine-induced protective immunity. PLoS Pathog 5: e1000484.
23. Beil WJ, Meinardus-Hager G, Neugebauer DC, Sorg C, (1992) Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice. J Leukoc Biol 52: 135-142.
24. Thalhofer CJ, Chen Y, Sudan B, Love-Homan L, Wilson ME, (2011) Leukocytes infiltrate the skin and draining lymph nodes in response to the protozoan Leishmania infantum chagasi. Infect Immun 79: 108-117.
25. Goncalves R, Zhang X, Cohen H, Debrabant A, Mosser DM, (2011) Platelet activation attracts a subpopulation of effector monocytes to sites of Leishmania major infection. J Exp Med 208: 1253-1265.
26. van Zandbergen G, Hermann N, Laufs H, Solbach W, Laskay T, (2002) Leishmania promastigotes release a granulocyte chemotactic factor and induce interleukin-8 release but inhibit gamma interferon-inducible protein 10 production by neutrophil granulocytes. Infect Immun 70: 4177-4184.
27. Ng LG, Hsu A, Mandell MA, Roediger B, Hoeller C, et al. (2008) Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLoS Pathog 4: e1000222.
28. Watson RW, Redmond HP, Wang JH, Condron C, Bouchier-Hayes D, (1996) Neutrophils undergo apoptosis following ingestion of Escherichia coli. J Immunol 156: 3986-3992.
29. Zysk G, Bejo L, Schneider-Wald BK, Nau R, Heinz H, (2000) Induction of necrosis and apoptosis of neutrophil granulocytes by Streptococcus pneumoniae. Clin Exp Immunol 122: 61-66.
30. Engelich G, White M, Hartshorn KL, (2001) Neutrophil survival is markedly reduced by incubation with influenza virus and Streptococcus pneumoniae: role of respiratory burst. J Leukoc Biol 69: 50-56.
31. Rotstein D, Parodo J, Taneja R, Marshall JC, (2000) Phagocytosis of Candida albicans induces apoptosis of human neutrophils. Shock 14: 278-283.
32. Yamamoto A, Taniuchi S, Tsuji S, Hasui M, Kobayashi Y, (2002) Role of reactive oxygen species in neutrophil apoptosis following ingestion of heat-killed Staphylococcus aureus. Clin Exp Immunol 129: 479-484.
33. Perskvist N, Long M, Stendahl O, Zheng L, (2002) Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol 168: 6358-6365.
34. Aga E, Katschinski DM, van Zandbergen G, Laufs H, Hansen B, et al. (2002) Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J Immunol 169: 898-905.
35. Charmoy M, Auderset F, Allenbach C, Tacchini-Cottier F, (2010) The prominent role of neutrophils during the initial phase of infection by Leishmania parasites. J Biomed Biotechnol 2010: 719361.
36. Xin L, Vargas-Inchaustegui DA, Raimer SS, Kelly BC, Hu J, et al. (2010) Type I IFN receptor regulates neutrophil functions and innate immunity to Leishmania parasites. J Immunol 184: 7047-7056.
37. Gueirard P, Laplante A, Rondeau C, Milon G, Desjardins M, (2008) Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macrophages. Cell Microbiol 10: 100-111.
38. Savill J, Dransfield I, Gregory C, Haslett C, (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2: 965-975.
39. Clayton AR, Prue RL, Harper L, Drayson MT, Savage CO, (2003) Dendritic cell uptake of human apoptotic and necrotic neutrophils inhibits CD40, CD80, and CD86 expression and reduces allogeneic T cell responses: relevance to systemic vasculitis. Arthritis Rheum 48: 2362-2374.
40. Aleman M, de la Barrera S, Schierloh P, Yokobori N, Baldini M, et al. (2007) Spontaneous or Mycobacterium tuberculosis-induced apoptotic neutrophils exert opposite effects on the dendritic cell-mediated immune response. Eur J Immunol 37: 1524-1537.
41. Urban BC, Willcox N, Roberts DJ, (2001) A role for CD36 in the regulation of dendritic cell function. Proc Natl Acad Sci U S A 98: 8750-8755.
42. Charmoy M, Brunner-Agten S, Aebischer D, Auderset F, Launois P, et al. (2010) Neutrophil-derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of Leishmania major inoculation in resistant mice. PLoS Pathog 6: e1000755.
43. Yang CW, Strong BS, Miller MJ, Unanue ER, (2010) Neutrophils influence the level of antigen presentation during the immune response to protein antigens in adjuvants. J Immunol 185: 2927-2934.
44. Xiaoxiao W, Sibiao Y, Xiaopeng X, Ping Z, Gang C, (2007) Neutrophils induce the maturation of immature dendritic cells: a regulatory role of neutrophils in adaptive immune responses. Immunol Invest 36: 337-350.
45. Bennouna S, Bliss SK, Curiel TJ, Denkers EY, (2003) Cross-talk in the innate immune system: neutrophils instruct recruitment and activation of dendritic cells during microbial infection. J Immunol 171: 6052-6058.
46. Wanderley JLM, Moreira MEC, Benjamin A, Bonomo AC, Barcinski MA, (2006) Mimicry of Apoptotic Cells by Exposing Phosphatidylserine Participates in the Establishment of Amastigotes of Leishmania (L) amazonensis in Mammalian Hosts. J Immunol 176: 1834-1839.
47. van Zandbergen G, Bollinger A, Wenzel A, Kamhawi S, Voll R, et al. (2006) Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc Natl Acad Sci U S A 103: 13837-13842.
48. Soong L, (2008) Modulation of dendritic cell function by Leishmania parasites. J Immunol 180: 4355-4360.
49. Van Ginderachter JA, Beschin A, De Baetselier P, Raes G, (2010) Myeloid-derived suppressor cells in parasitic infections. Eur J Immunol 40: 2976-2985.
50. Gabrilovich DI, Nagaraj S, (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9: 162-174.
51. Chen L, Zhang ZH, Watanabe T, Yamashita T, Kobayakawa T, et al. (2005) The involvement of neutrophils in the resistance to Leishmania major infection in susceptible but not in resistant mice. Parasitol Int 54: 109-118.
52. Ribeiro-Gomes FL, Otero AC, Gomes NA, Moniz-De-Souza MC, Cysne-Finkelstein L, et al. (2004) Macrophage interactions with neutrophils regulate Leishmania major infection. J Immunol 172: 4454-4462.
53. Tacchini-Cottier F, Zweifel C, Belkaid Y, Mukankundiye C, Vasei M, et al. (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.
54. Kimblin N, Peters N, Debrabant A, Secundino N, Egen J, et al. (2008) Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proc Natl Acad Sci U S A 105: 10125-10130.
55. Bertholet S, Debrabant A, Afrin F, Caler E, Mendez S, et al. (2005) Antigen requirements for efficient priming of CD8+ T cells by Leishmania major-infected dendritic cells. Infect Immun 73: 6620-6628.