Th17 cells and neutrophils: Close collaborators in chronic Leishmania mexicana infections leading to disease severity

Parasite Immunology

Volumn 39, Issue 4, 2017, Pages

  Pedraza Zamora, C P ^a   Delgado Dominguez J ^a   Zamora Chimal, J ^a   Becker, I ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

IL 17; inflammation; Leishmania mexicana; neutrophils; Th17 cells

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 17;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC INFLAMMATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; FEMALE; FLOW CYTOMETRY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INFECTION SENSITIVITY; LEISHMANIA MEXICANA; LYMPHOCYTE DIFFERENTIATION; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE; QUANTITATIVE ANALYSIS; SKIN LEISHMANIASIS; TH17 CELL; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CHRONIC DISEASE; DISEASE MODEL; DISEASE PREDISPOSITION; IMMUNOLOGY; NEUTROPHIL CHEMOTAXIS; PARASITOLOGY; PHYSIOLOGY; SPECIES DIFFERENCE;

ANIMALS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; FEMALE; LEISHMANIA MEXICANA; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; NEUTROPHILS; SPECIES SPECIFICITY; TH17 CELLS;

EID: 85017546108     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12420     Document Type: Article

References (68)

1. World Health Organization - Fact sheet 375: Leishmaniasis [homepage on the internet]. WHO; c2016 [updated September 2016]. http://www.who.int/mediacentre/factsheets/fs375/en/. Accessed May 23, 2016.
2. Bates P. Transmission of leishmania metacyclic promastigotes by phlebotomine sand flies. Int J Parasitol. 2007;37:1097-1106.
3. Flisser Steinbruch A, Pérez Tamayo R. Leishmaniosis (capítulo escrito por Ingeborg Becker). En. Aprendizaje de la parasitología basado en problemas.1ª edición. México: Editorial Manual Moderno; 2006. P.394-409.
4. Desjeux P, Ghosh RS, Dhalaria P, Strub-Wourgaft N, Zijlstra EE. Report of the Post Kala-azar Dermal Leishmaniasis (PKDL) Consortium Meeting, New Delhi, India, 27–29 June 2012. Parasit Vectors. 2013;6:196.
5. López-Céspedes A, Longoni SS, Sauri-Arceo CH, et al. Leishmania spp. epidemiology of canine leishmaniasis in the Yucatan Peninsula. Sci World J. 2012. doi:10.1100/2012/945871.
6. Vinetz JM, Soong L. Leishmania mexicana infection of the eyelid in a traveler to Belize. Braz J Infect Dis. 2007;11:149-152.
7. WHO Leishmaniasis in Guatemala [database in the Internet]. WHO. http://www.who.int/leishmaniasis/resources/GUATEMALA.pdf. Accessed May 23, 2016.
8. Cedillos RA, Romero JE, Romero CJ, Gavidia ME. Leishmaniasis en el Salvador. Minerva Revista en línea CIC-UES. Enero-Julio. 2014;4:33-44.
9. Organización Panamericana de la Salud. Leishmaniasis en las Américas Recomendaciones para el tratamiento [database in the Internet]. Washington D.C.: OPS; c2013. http://www.facmed.unam.mx/deptos/microbiologia/pdf/Leishmaniasis-Tratamiento-Americas-2013-Guia_OPS.pdf. Accessed May 23, 2016.
10. Kedzierski L. Leishmaniasis vaccine: where are we today? J Glob Infect Dis. 2010;2:177-185.
11. Nylen S, Gautam S. Immunological perspectives of leishmaniasis. J Glob Infect Dis. 2010;2:135-146.
12. Ueno N, Wilson ME. Receptor-mediated phagocytosis of leishmania: implications for intracellular survival. Trends Parasitol. 2012;28:335-344.
13. Nordenfelt P, Tapper H. Phagosome dynamics during phagocytosis by neutrophils. J Leukoc Biol. 2011;90:271-284.
14. Filardy AA, Pires DR, DosReis GA. Macrophages and neutrophils cooperate in immune responses to leishmania infection. Cell Mol Life Sci. 2011;68:1863-1870.
15. Peters NC, Sacks DL. The impact of vector mediated neutrophil recruitment on cutaneous leishmaniasis. Cell Microbiol. 2009;11:1290-1296.
16. Charmoy M, Brunner-Agten S, Aebischer D, et al. Neutrophil-derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of leishmania major inoculation in resistant mice. PLoS Pathog. 2010;6:e1000755.
17. Laskay T, van Zandbergen G, Solbach W. Neutrophil granulocytes – Trojan horses for leishmania major and other intracellular microbes? Trends Microbiol. 2003;11:210-214.
18. Freitas-Lopes M, Costa-da-Silva AC, Alexandre DG. Innate immunity to leishmania infection: within phagocytes. Mediators Inflamm. 2014. doi: 10.1155/2014/754965.
19. Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations. Annu Rev Immunol. 2010;28:445-489.
20. Mosmann TR, Coffman RL. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol. 1989;7:145-173.
21. Lohoff M, Gessner A, Bogdan C, Röllinghoff M. Experimental murine leishmaniasis and the Th1/Th2 cell concept. Tokai J Exp Clin Med. 1998;23:347-350.
22. Becker I, Salaiza N, Aguirre M, et al. Leishmania lipophosphoglycan (LPG) activates NK cells through toll-like receptor-2. Mol Biochem Parasitol. 2003;130:65-74.
23. Ashok D, Schuster S, Ronet C, et al. Cross-presenting dendritic cells are required for control of leishmania major infection. Eur J Immunol. 2014;44:1422-1432.
24. Belkaid Y, Mendez S, Lira R, Kadambi N, Milon G, Sacks D. 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. 2000;165:969-977.
25. Alexander J, Kaye PM. Immunoregulatory pathways in murine leishmaniasis: different regulatory control during Leishmania mexicana mexicana and Leishmania major infections. Clin Exp Immunol. 1985;61:674-682.
26. Aguilar TF, Lambot MA, Laman JD, et al. Parasitic load and histopathology of cutaneous lesions, lymph node, spleen, and liver from BALB/c and C57BL/6 mice infected with Leishmania mexicana. Am J Trop Med Hyg. 2002;66:273-279.
27. Rosas L, Keiser T, Barbi J, et al. Genetic background influences immune responses and disease outcome of cutaneous L. mexicana infection in mice. Int Immunol. 2005;17:1347-1357.
28. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol. 2009;27:485-517.
29. H17 and regulatory T cells. Nature. 2006;441:235-238.
30. Roark CL, Simonian PL, Fontenot AP, Born WK, O'Brien RL. gammadelta T cells: an important source of IL-17. Curr Opin Immunol. 2008;20:353-357.
31. Bacellar O, Faria D, Nascimento M, et al. IL-17 Production in patients with American cutaneous leishmaniasis. J Infect Dis. 2009;200:75-78.
32. Adriouch S, Dox D, Welge V, Seman M, Koch-Nolte F, Haag F. Cutting edge: a natural P451L mutation in the cytoplasmic domain impairs the function of the mouse P2X7 receptor. J Immunol. 2002;169:4108-4112.
33. Shio MT, Christian JG, Jung JY, Chang K-P, Olivier M. PKC/ROS-mediated NLRP3 inflammasome activation is attenuated by leishmania zinc-metalloprotease during infection. PLoS Negl Trop Dis. 2015;9:e0003868.
34. Idzko M, Ferrari D, Eltzschig HK. Nucleotide signalling during inflammation. Nature. 2014;509:310-317.
35. 7 receptors mediate NLRP3 inflammasome-dependent IL-1B secretion in response to ATP. Nature. 2016;7:10555.
36. Horta MF, Pinheiro Mendes B, Roma EH, et al. Reactive oxygen species and nitric oxide in cutaneous leishmaniasis. J Parasitol Res. 2012. doi:10.1155/2012/203818.
37. Charmoy M, Megnekou R, Allenbach C, et al. Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol. 2007;82:288-299.
38. Kruger P, Saffarzadeh M, Weber ANR, et al. Neutrophils: between host defence, immune modulation, and tissue injury. PLoS Pathog. 2015;11:e1004651.
39. Ribeiro-Gomes FL, Peters NC, Debrabant A, Sacks DL. Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response. PLoS Pathog. 2012;8:e1002536.
40. Sousa LM, Carneiro MB, Resende ME, et al. Neutrophils have a protective role during early stages of Leishmania amazonensis infection in BALB/c mice. Parasite Immunol. 2014;36:13-31.
41. Guimarães-Costa AB, Nascimento MTC, Froment GS, et al. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci USA. 2009;106:6748-6753.
42. Mócsai A. Diverse novel functions of neutrophils in immunity, inflammation and beyond. J Exp Med. 2013;210:1283-1299.
43. Summers C, Rankin SM, Condliffe AM, et al. Neutrophil kinetics in health and disease. Trends Immunol. 2010;31:318-324.
44. Iba T, Hashiguchi N, Nagaoka I, Tabe Y, Murai M. Neutrophil cell death in response to infection and its relation to coagulation. J Intensive Care. 2013;1:13.
45. Papayannopoulos V, Zychlinsky A. NETs: a new strategy for using old weapons. Trends Immunol. 2009;30:513-521.
46. Caielli S, Banchereau J, Pascual V. Neutrophils come of age in chronic inflammation. Curr Opin in Immunol. 2012;24:671-677.
47. Hoenderdos K, Condliffe A. The neutrophil in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2013;48:531-539.
48. Wright HL, Moots RJ, Bucknall RC, Edwards SW. Neutrophil function in inflammation and inflammatory diseases. Rheumatology. 2010;49:1618-1631.
49. Segel GB, Halterman MW, Lichtman MA. The paradox of the neutrophil's role in tissue injury. J Leukoc Biol. 2011;89:359-372.
50. Nobuhiro DD, Jackson R, Grasemann H, Palaniyar N. Innate immune collectin surfactant protein d simultaneously binds both neutrophil extracellular traps and carbohydrate ligands and promotes bacterial trapping. J Immunol. 2011;187:1856-1865.
51. Lin AM, Rubin CJ, Khandpur R, et al. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J Immunol. 2011;187:490-500.
52. Chrysanthopoulou A, Mitroulis I, Apostolidou E, et al. Neutrophil extracellular traps promote differentiation and function of fibroblasts. J Pathol. 2014;233:294-307.
53. Lögters T, Margraf S, Altrichter J, et al. The clinical value of neutrophil extracellular traps. Med Microbiol Immunol. 2009;198:211-219.
54. Warnatsch A, Ioannou M, Wang Q, Papayannopoulos V. Neutrophil extracellular traps license macrophages and Th17 cells for cytokine production in atherosclerosis. Science. 2015;349:316-320.
55. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13:159-175.
56. Kleinewietfeld M, Manzel A, Titze J, et al. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature. 2013;496:518-522.
57. Silva MT. Neutrophils and macrophages work in concert as inducers and effectors of adaptive immunity against extracellular and intracellular microbial pathogens. J Leukoc Biol. 2010;87:805-813.
58. Abi Abdallah DS, Egan CE, Butcher BA, Denkers EY. Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int Immunol. 2011;23:317-326.
59. Pitta M, Romano A, Cabantous S, et al. IL-17 and IL-22 are associated with protection against human kala azar caused by Leishmania donovani. J Clin Invest. 2009;119:2379-2387.
60. Evans HG, Gullik NJ, Kelly S, et al. In vivo activated monocytes from the site of inflammation in humans specifically promote Th17 responses. Proc Natl Acad Sci USA. 2009;106:6232-6237.
61. Boaventura VS, Santos CS, Cardoso CR, et al. Human mucosal leishmaniasis: neutrophils infiltrate areas of tissue damage that express high levels of Th17-related cytokines. Eur J Immunol. 2010;40:2830-2836.
62. Oliveira WN, Ribeiro LE, Schrieffer A, Machado P, Carvalho EM, Bacellar O. The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of human tegumentary leishmaniasis. Cytokine. 2014;66:127-132.
63. Khader SA, Gaffen SL, Kolls JK. Th17 cells at the cross roads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol. 2009;2:403-411.
64. Caruso R, Fina D, Paoluzi OA, et al. IL-23-mediated regulation of IL-17 production in Helicobacter pylori-infected gastric mucosa. Eur J Immunol. 2008;38:470-478.
65. Lopez Kostka S, Dinges S, Griewank K, Iwakura Y, Udey MC, von Stebut E. IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. J Immunol. 2009;182:3039-3046.
66. Terrazas C, Varikuti S, Kimble J, Moretti E, Boyaka PN, Satoskar AR. IL-17A promotes susceptibility during experimental visceral leishmaniasis caused by Leishmania donovani. FASEB J. 2016;30:1135-1143.
67. Wu W, Huang L, Mendez S. A live Leishmania major vaccine containing CpG motifs induces the de novo generation of Th17 cells in C57BL/6 mice. Eur J Immunol. 2010;40:2517-2527.
68. Nascimento MS, Carregaro V, Lima-Júnior DS, et al. Interleukin 17A acts synergistically with interferon γ to promote protection against Leishmania infantum infection. J Infect Dis. 2015;211:1015-1026.