Rapid Sequestration of Leishmania mexicana by Neutrophils Contributes to the Development of Chronic Lesion

PLoS Pathogens

Volumn 11, Issue 5, 2015, Pages

  Hurrell, Benjamin P ^a   Schuster, Steffen ^a   Grün, Eva ^a   Coutaz, Manuel ^a   Williams, Roderick A ^b   Held, Werner ^a   Malissen, Bernard ^c,d   Malissen, Marie ^c,d   Yousefi, Shida ^e   Simon, Hans Uwe ^e   Müller, Andreas J ^a,f   Tacchini Cottier, Fabienne ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF THE WEST OF SCOTLAND   (United Kingdom)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d INSERM   (France)

^e UNIVERSITY OF BERN   (Switzerland)

^f OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CYTOKINE PRODUCTION; DISEASE COURSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENISTA; IMMUNE RESPONSE; INTRAVITAL 2 PHOTON MICROSCOPY; LEISHMANIA MEXICANA; LEISHMANIASIS; LUCIFERASE ASSAY; LUMINESCENCE; MICROENVIRONMENT; MICROSCOPY; MOUSE; NEUTROPENIA; NEUTROPHIL; NONHUMAN; PARASITE CONTROL; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; CHRONIC DISEASE; DENDRITIC CELL; GENETICS; IMMUNOLOGY; METABOLISM; MONOCYTE; NEUTROPHIL CHEMOTAXIS; PARASITOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN LEISHMANIASIS;

GENISTA; LEISHMANIA MEXICANA; MUS; PROTOZOA;

CYTOKINE; MESSENGER RNA;

ANIMALS; CELLS, CULTURED; CHRONIC DISEASE; CYTOKINES; DENDRITIC CELLS; FLOW CYTOMETRY; LEISHMANIA MEXICANA; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MONOCYTES; NEUTROPHIL INFILTRATION; NEUTROPHILS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84930345781     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004929     Document Type: Article

References (72)

1. Sacks D, Noben-Trauth N, (2002) The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol 2: 845–858. 12415308
2. Kaye P, Scott P, (2011) Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol 9: 604–615. doi: 10.1038/nrmicro2608 21747391
3. McMahon-Pratt D, Alexander J, (2004) Does the Leishmania major paradigm of pathogenesis and protection hold for New World cutaneous leishmaniases or the visceral disease? Immunol Rev 201: 206–224. 15361243
4. Hsu AC, Scott P, (2007) Leishmania mexicana infection induces impaired lymph node expansion and Th1 cell differentiation despite normal T cell proliferation. J Immunol 179: 8200–8207. 18056363
5. Petritus PM, Manzoni-de-Almeida D, Gimblet C, Gonzalez Lombana C, Scott P, (2012) Leishmania mexicana induces limited recruitment and activation of monocytes and monocyte-derived dendritic cells early during infection. PLoS Negl Trop Dis 6: e1858. doi: 10.1371/journal.pntd.0001858 23094119
6. Weinheber N, Wolfram M, Harbecke D, Aebischer T, (1998) Phagocytosis of Leishmania mexicana amastigotes by macrophages leads to a sustained suppression of IL-12 production. Eur J Immunol 28: 2467–2477. 9710224
7. Bennett CL, Misslitz A, Colledge L, Aebischer T, Blackburn CC, (2001) Silent infection of bone marrow-derived dendritic cells by Leishmania mexicana amastigotes. Eur J Immunol 31: 876–883. 11241293
8. Rodriguez-Sosa M, Monteforte GM, Satoskar AR, (2001) Susceptibility to Leishmania mexicana infection is due to the inability to produce IL-12 rather than lack of IL-12 responsiveness. Immunol Cell Biol 79: 320–322. 11488977
9. Shweash M, Adrienne McGachy H, Schroeder J, Neamatallah T, Bryant CE, et al. (2011) Leishmania mexicana promastigotes inhibit macrophage IL-12 production via TLR-4 dependent COX-2, iNOS and arginase-1 expression. Mol Immunol 48: 1800–1808. doi: 10.1016/j.molimm.2011.05.013 21664694
10. Contreras I, Estrada JA, Guak H, Martel C, Borjian A, et al. (2014) Impact of Leishmania mexicana infection on dendritic cell signaling and functions. PLoS Negl Trop Dis 8: e3202. doi: 10.1371/journal.pntd.0003202 25255446
11. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532–1535. 15001782
12. Kolaczkowska E, Kubes P, (2013) Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13: 159–175. doi: 10.1038/nri3399 23435331
13. Bardoel BW, Kenny EF, Sollberger G, Zychlinsky A, (2014) The balancing act of neutrophils. Cell Host Microbe 15: 526–536. doi: 10.1016/j.chom.2014.04.011 24832448
14. 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. 1506767
15. 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. 10946291
16. 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. doi: 10.1126/science.1159194 18703742
17. 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. doi: 10.4049/jimmunol.0903273 20483775
18. 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. doi: 10.1128/IAI.00338-10 20937764
19. Ribeiro-Gomes FL, Peters NC, Debrabant A, Sacks DL, (2012) Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response. PLoS Pathog 8: e1002536. doi: 10.1371/journal.ppat.1002536 22359507
20. 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. 15557140
21. Guimaraes-Costa AB, Nascimento MT, Froment GS, Soares RP, Morgado FN, et al. (2009) Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci U S A 106: 6748–6753. doi: 10.1073/pnas.0900226106 19346483
22. Gabriel C, McMaster WR, Girard D, Descoteaux A, (2010) Leishmania donovani promastigotes evade the antimicrobial activity of neutrophil extracellular traps. J Immunol 185: 4319–4327. doi: 10.4049/jimmunol.1000893 20826753
23. Gross S, Gammon ST, Moss BL, Rauch D, Harding J, et al. (2009) Bioluminescence imaging of myeloperoxidase activity in vivo. Nat Med 15: 455–461. doi: 10.1038/nm.1886 19305414
24. Ordonez-Rueda D, Jonsson F, Mancardi DA, Zhao W, Malzac A, et al. (2012) A hypomorphic mutation in the Gfi1 transcriptional repressor results in a novel form of neutropenia. Eur J Immunol 42: 2395–2408. doi: 10.1002/eji.201242589 22684987
25. Blomgran R, Desvignes L, Briken V, Ernst JD, (2012) Mycobacterium tuberculosis inhibits neutrophil apoptosis, leading to delayed activation of naive CD4 T cells. Cell Host Microbe 11: 81–90. doi: 10.1016/j.chom.2011.11.012 22264515
26. Jaeger BN, Donadieu J, Cognet C, Bernat C, Ordonez-Rueda D, et al. (2012) Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J Exp Med 209: 565–580. doi: 10.1084/jem.20111908 22393124
27. Abi Abdallah DS, Denkers EY, (2012) Neutrophils cast extracellular traps in response to protozoan parasites. Front Immunol 3: 382. doi: 10.3389/fimmu.2012.00382 23248631
28. Guimaraes-Costa AB, DeSouza-Vieira TS, Paletta-Silva R, Freitas-Mesquita AL, Meyer-Fernandes JR, et al. (2014) 3'-nucleotidase/nuclease activity allows Leishmania parasites to escape killing by neutrophil extracellular traps. Infect Immun 82: 1732–1740. doi: 10.1128/IAI.01232-13 24516114
29. 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. doi: 10.1073/pnas.0802331105 18626016
30. Belkaid Y, Kamhawi S, Modi G, Valenzuela J, Noben-Trauth N, et al. (1998) Development of a natural model of cutaneous leishmaniasis: powerful effects of vector saliva and saliva preexposure on the long-term outcome of Leishmania major infection in the mouse ear dermis. J Exp Med 188: 1941–1953. 9815271
31. Titus RG, Ribeiro JM, (1988) Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239: 1306–1308. 3344436
32. Rogers ME, Ilg T, Nikolaev AV, Ferguson MA, Bates PA, (2004) Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Nature 430: 463–467. 15269771
33. Rogers M, Kropf P, Choi BS, Dillon R, Podinovskaia M, et al. (2009) Proteophosophoglycans regurgitated by Leishmania-infected sand flies target the L-arginine metabolism of host macrophages to promote parasite survival. PLoS Pathog 5: e1000555. doi: 10.1371/journal.ppat.1000555 19696894
34. Rogers ME, Corware K, Muller I, Bates PA, (2010) Leishmania infantum proteophosphoglycans regurgitated by the bite of its natural sand fly vector, Lutzomyia longipalpis, promote parasite establishment in mouse skin and skin-distant tissues. Microbes Infect 12: 875–879. doi: 10.1016/j.micinf.2010.05.014 20561596
35. Chagas AC, Oliveira F, Debrabant A, Valenzuela JG, Ribeiro JM, et al. (2014) Lundep, a sand fly salivary endonuclease increases Leishmania parasite survival in neutrophils and inhibits XIIa contact activation in human plasma. PLoS Pathog 10: e1003923. doi: 10.1371/journal.ppat.1003923 24516388
36. Mottram JC, Coombs GH, Alexander J, (2004) Cysteine peptidases as virulence factors of Leishmania. Curr Opin Microbiol 7: 375–381. 15358255
37. Buxbaum LU, Denise H, Coombs GH, Alexander J, Mottram JC, et al. (2003) Cysteine protease B of Leishmania mexicana inhibits host Th1 responses and protective immunity. J Immunol 171: 3711–3717. 14500670
38. Pertuz Belloso S, Ostoa Saloma P, Benitez I, Soldevila G, Olivos A, et al. (2004) Entamoeba histolytica cysteine protease 2 (EhCP2) modulates leucocyte migration by proteolytic cleavage of chemokines. Parasite Immunol 26: 237–241. 15491473
39. Cotton JA, Bhargava A, Ferraz JG, Yates RM, Beck PL, et al. (2014) Giardia duodenalis cathepsin B proteases degrade intestinal epithelial interleukin-8 and attenuate interleukin-8-induced neutrophil chemotaxis. Infect Immun 82: 2772–2787. doi: 10.1128/IAI.01771-14 24733096
40. Charmoy M, Megnekou R, Allenbach C, Zweifel C, Perez C, et al. (2007) Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol 82: 288–299. 17449725
41. 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. doi: 10.1371/journal.ppat.1000755 20140197
42. 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. 15034061
43. Sousa LM, Carneiro MB, Resende ME, Martins LS, Dos Santos LM, et al. (2014) Neutrophils have a protective role during early stages of Leishmania amazonensis infection in BALB/c mice. Parasite Immunol 36: 13–31. doi: 10.1111/pim.12078 24102495
44. Webster P, JW IJ Chicoine LM, Fikrig E, (1998) The agent of Human Granulocytic Ehrlichiosis resides in an endosomal compartment. J Clin Invest 101: 1932–1941. 9576758
45. Liu GY, Essex A, Buchanan JT, Datta V, Hoffman HM, et al. (2005) Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J Exp Med 202: 209–215. 16009720
46. Eruslanov EB, Lyadova IV, Kondratieva TK, Majorov KB, Scheglov IV, et al. (2005) Neutrophil responses to Mycobacterium tuberculosis infection in genetically susceptible and resistant mice. Infect Immun 73: 1744–1753. 15731075
47. Barquero-Calvo E, Martirosyan A, Ordonez-Rueda D, Arce-Gorvel V, Alfaro-Alarcon A, et al. (2013) Neutrophils exert a suppressive effect on Th1 responses to intracellular pathogen Brucella abortus. PLoS Pathog 9: e1003167. doi: 10.1371/journal.ppat.1003167 23458832
48. Laskay T, van Zandbergen G, Solbach W, (2003) Neutrophil granulocytes—Trojan horses for Leishmania major and other intracellular microbes? Trends Microbiol 11: 210–214. 12781523
49. Mantovani A, Cassatella MA, Costantini C, Jaillon S, (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11: 519–531. doi: 10.1038/nri3024 21785456
50. Scapini P, Cassatella MA, (2014) Social networking of human neutrophils within the immune system. Blood 124: 710–719. doi: 10.1182/blood-2014-03-453217 24923297
51. 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. 12097394
52. Sarkar A, Aga E, Bussmeyer U, Bhattacharyya A, Moller S, et al. (2013) Infection of neutrophil granulocytes with Leishmania major activates ERK 1/2 and modulates multiple apoptotic pathways to inhibit apoptosis. Med Microbiol Immunol 202: 25–35. doi: 10.1007/s00430-012-0246-1 22661217
53. 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. doi: 10.1155/2010/719361 19884987
54. Schuster S, Hurrell B, Tacchini-Cottier F, (2013) Crosstalk between neutrophils and dendritic cells: a context-dependent process. J Leukoc Biol 94: 671–675. doi: 10.1189/jlb.1012540 23250891
55. Teixeira MJ, Teixeira CR, Andrade BB, Barral-Netto M, Barral A, (2006) Chemokines in host-parasite interactions in leishmaniasis. Trends Parasitol 22: 32–40. 16310413
56. 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. 17412618
57. Ritter U, Moll H, (2000) Monocyte chemotactic protein-1 stimulates the killing of leishmania major by human monocytes, acts synergistically with IFN-gamma and is antagonized by IL-4. Eur J Immunol 30: 3111–3120. 11093125
58. Abadie V, Badell E, Douillard P, Ensergueix D, Leenen PJ, et al. (2005) Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 106: 1843–1850. 15886329
59. Chtanova T, Schaeffer M, Han SJ, van Dooren GG, Nollmann M, et al. (2008) Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29: 487–496. doi: 10.1016/j.immuni.2008.07.012 18718768
60. Maletto BA, Ropolo AS, Alignani DO, Liscovsky MV, Ranocchia RP, et al. (2006) Presence of neutrophil-bearing antigen in lymphoid organs of immune mice. Blood 108: 3094–3102. 16835380
61. 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. doi: 10.4049/jimmunol.1001289 20679530
62. Yang CW, Unanue ER, (2013) Neutrophils control the magnitude and spread of the immune response in a thromboxane A2-mediated process. J Exp Med 210: 375–387. doi: 10.1084/jem.20122183 23337807
63. 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. 10887140
64. Lindquist RL, Shakhar G, Dudziak D, Wardemann H, Eisenreich T, et al. (2004) Visualizing dendritic cell networks in vivo. Nat Immunol 5: 1243–1250. 15543150
65. Schuster S, Hartley MA, Tacchini-Cottier F, Ronet C, (2014) A scoring method to standardize lesion monitoring following intra-dermal infection of Leishmania parasites in the murine ear. Front Cell Infect Microbiol 4: 67. doi: 10.3389/fcimb.2014.00067 24904841
66. Weinkopff T, de Oliveira CI, de Carvalho AM, Hauyon-La Torre Y, Muniz AC, et al. (2014) Repeated exposure to Lutzomyia intermedia sand fly saliva induces local expression of interferon-inducible genes both at the site of injection in mice and in human blood. PLoS Negl Trop Dis 8: e2627. doi: 10.1371/journal.pntd.0002627 24421912
67. Misslitz A, Mottram JC, Overath P, Aebischer T, (2000) Targeted integration into a rRNA locus results in uniform and high level expression of transgenes in Leishmania amastigotes. Mol Biochem Parasitol 107: 251–261. 10779601
68. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE, (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83: 64–70. 17884993
69. Filipe-Santos O, Pescher P, Breart B, Lippuner C, Aebischer T, et al. (2009) A dynamic map of antigen recognition by CD4 T cells at the site of Leishmania major infection. Cell Host Microbe 6: 23–33. doi: 10.1016/j.chom.2009.04.014 19616763
70. Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, et al. (2008) Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 14: 949–953. doi: 10.1038/nm.1855 18690244
71. Yousefi S, Mihalache C, Kozlowski E, Schmid I, Simon HU, (2009) Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ 16: 1438–1444. doi: 10.1038/cdd.2009.96 19609275
72. Dworski R, Simon HU, Hoskins A, Yousefi S, (2011) Eosinophil and neutrophil extracellular DNA traps in human allergic asthmatic airways. J Allergy Clin Immunol 127: 1260–1266. doi: 10.1016/j.jaci.2010.12.1103 21315435