Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection

Journal of Immunology

Volumn 183, Issue 12, 2009, Pages 8088-8098

  Novais, Fernanda O ^a   Santiago, Rômulo C ^a   Báfica, André ^b   Khouri, Ricardo ^a   Afonso, Lilian ^a   Borges, Valéria M ^a,c   Brodskyn, Cláudia ^a,c,d   Barral Netto, Manoel ^a,c,d   Barral, Aldina ^a,c,d   De Oliveira, Camila I ^a,c  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^c Institute de Investigação em Imunologia iii   (Brazil)

^d FEDERAL UNIVERSITY OF BAHIA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXPERIMENTAL MODEL; FEMALE; HISTOLOGY; HOST RESISTANCE; HUMAN; HUMAN CELL; IN VITRO STUDY; LEISHMANIA BRAZILIENSIS; LEISHMANIASIS; LYMPH NODE; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; TH1 CELL; TH2 CELL; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL COMMUNICATION; CELL CULTURE; COCULTURE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INNATE IMMUNITY; MOUSE MUTANT; NEUTROPHIL CHEMOTAXIS; PARASITOLOGY; PATHOLOGY; PERITONEUM MACROPHAGE; SKIN LEISHMANIASIS; TRANSPLANTATION;

ANIMALS; CELL COMMUNICATION; CELLS, CULTURED; COCULTURE TECHNIQUES; FEMALE; HUMANS; IMMUNITY, INNATE; LEISHMANIA BRAZILIENSIS; LEISHMANIASIS, DIFFUSE CUTANEOUS; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NEUTROPHILS;

EID: 76249105131     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803720     Document Type: Article

References (53)

1. Bittencourt, A., N. Silva, A. Straatmann, V. L. Nunes, I. Follador, and R. Badaro. 2003. Post-kala-azar dermal leishmaniasis associated with AIDS. Braz. J. Infect. Dis. 7: 229-233.
2. Grimaldi, G., Jr., M. J. Soares, and P. L. Moriearty. 1984. Tissue eosinophilia and Leishmania mexicana mexicana eosinophil interactions in murine cutaneous leishmaniasis. Parasite Immunol. 6: 397-408.
3. de Magalhaes, A. V., M. A. Moraes, A. N. Raick, A. Llanos-Cuentas, J. M. Costa, C. C. Cuba, and P. D. Marsden. 1986. [Histopathology of cutaneous leishmaniasis by Leishmania braziliensis braziliensis: 1. Histopathological patterns and study of the course of the lesions]. Rev. Inst. Med. Trop. Sao Paulo 28: 253-262.
4. Faurschou, M., and N. Borregaard. 2003. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 5: 1317-1327. (Pubitemid 37410245)
5. Nauseef, W. M. 2007. How human neutrophils kill and degrade microbes: an integrated view. Immunol. Rev. 219: 88-102.
6. Appelberg, R. 2007. Neutrophils and intracellular pathogens: beyond phagocytosis and killing. Trends Microbiol. 15: 87-92. (Pubitemid 46199185)
7. Nathan, C. 2006. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6: 173-182.
8. Chen, L., Z. H. Zhang, T. Watanabe, T. Yamashita, T. Kobayakawa, A. Kaneko, H. Fujiwara, and F. Sendo. 2005. The involvement of neutrophils in the resistance to Leishmania major infection in susceptible but not in resistant mice. Parasitol. Int. 54: 109-118. (Pubitemid 40615209)
9. Lima, G. M., A. L. Vallochi, U. R. Silva, E. M. Bevilacqua, M. M. Kiffer, and I. A. Abrahamsohn. 1998. The role of polymorphonuclear leukocytes in the resistance to cutaneous leishmaniasis. Immunol. Lett. 64: 145-151. (Pubitemid 28553025)
10. Ribeiro-Gomes, F. L., A. C. Otero, N. A. Gomes, M. C. Moniz-De-Souza, L. Cysne-Finkelstein, A. C. Arnholdt, V. L. Calich, S. G. Coutinho, M. F. Lopes, and G. A. DosReis. 2004. Macrophage interactions with neutrophils regulate Leishmania major infection. J. Immunol. 172: 4454-4462.
11. + Th2 response in BALB/c mice infected with Leishmania major. J. Immunol. 165: 2628-2636.
12. Charmoy, M., R. Megnekou, C. Allenbach, C. Zweifel, C. Perez, K. Monnat, M. Breton, C. Ronet, P. Launois, and F. Tacchini-Cottier. 2007. Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J. Leukocyte Biol. 82: 288-299. (Pubitemid 47230640)
13. Rocha, F. J., U. Schleicher, J. Mattner, G. Alber, and C. Bogdan. 2007. Cytokines, signaling pathways, and effector molecules required for the control of Leishmania (Viannia) braziliensis in mice. Infect. Immun. 75: 3823-3832.
14. de Moura, T. R., F. O. Novais, F. Oliveira, J. Clarencio, A. Noronha, A. Barral, C. Brodskyn, and C. I. de Oliveira. 2005. Toward a novel experimental model of infection to study American cutaneous leishmaniasis caused by Leishmania braziliensis. Infect. Immun. 73: 5827-5834.
15. Afonso, L., V. M. Borges, H. Cruz, F. Ribeiro-Gomes, A. DosReis, A. Noronha-Dutra, C. I. de Oliveira, A. Barral, M. Barral-Netto, and C. Brodskyn. 2008. Interactions with apoptotic but not with necrotic neutrophils increase parasite burden in human macrophages infected with Leishmania amazonensis. J. Leukocyte Biol. 84: 389-396.
16. Spath, G. F., and S. M. Beverley. 2001. A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Exp. Parasitol. 99: 97-103.
17. Tateda, K., T. A. Moore, J. C. Deng, M. W. Newstead, X. Zeng, A. Matsukawa, M. S. Swanson, K. Yamaguchi, and T. J. Standiford. 2001. Early recruitment of neutrophils determines subsequent T1/T2 host responses in a murine model of Legionella pneumophila pneumonia. J. Immunol. 166: 3355-3361. (Pubitemid 33117336)
18. Titus, R. G., M. Marchand, T. Boon, and J. A. Louis. 1985. A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol. 7: 545-555.
19. Henson, P. M., D. L. Bratton, and V. A. Fadok. 2001. Apoptotic cell removal. Curr. Biol. 11: R795-R805.
20. Miranda, K. M., M. G. Espey, and D. A. Wink. 2001. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5: 62-71.
21. Elstner, E. F., and A. Heupel. 1976. Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal. Biochem. 70: 616-620.
22. Khouri, R., A. Bafica, P. Silva Mda, A. Noronha, J. P. Kolb, J. Wietzerbin, A. Barral, M. Barral-Netto, and J. Van Weyenbergh. 2009. IFN-β impairs superoxide-dependent parasite killing in human macrophages: evidence for a deleterious role of SOD1 in cutaneous leishmaniasis. J. Immunol. 182: 2525-2531.
23. McFarlane, E., C. Perez, M. Charmoy, C. Allenbach, K. C. Carter, J. Alexander, and F. Tacchini-Cottier. 2008. Neutrophils contribute to development of a protective immune response during onset of infection with Leishmania donovani. Infect. Immun. 76: 532-541.
24. Murray, H. W. 1982. Cell-mediated immune response in experimental visceral leishmaniasis: II. Oxygen-dependent killing of intracellular Leishmania donovani amastigotes. J. Immunol. 129: 351-357.
25. Liew, F. Y., S. Millott, C. Parkinson, R. M. Palmer, and S. Moncada. 1990. Macrophage killing of Leishmania parasite in vivo is mediated by nitric oxide from L-arginine. J. Immunol. 144: 4794-4797.
26. 4 is mediated by a reactive oxygen species-extracellular signal-regulated kinase-linked cascade. J. Immunol. 170: 6273-6279.
27. Sayles, P. C., and L. L. Johnson. 1996. Exacerbation of toxoplasmosis in neutrophil- depleted mice. Nat. Immunol. 15: 249-258.
28. Pedrosa, J., B. M. Saunders, R. Appelberg, I. M. Orme, M. T. Silva, and A. M. Cooper. 2000. Neutrophils play a protective nonphagocytic role in systemic Mycobacterium tuberculosis infection of mice. Infect. Immun. 68: 577-583.
29. + cells. Infect. Immun. 73: 4522-4529.
30. + cells play an essential role in an experimental model of disseminated histoplasmosis. Microbes Infect. 9: 1393-1401.
31. Takeuchi, D., V. C. Jones, M. Kobayashi, and F. Suzuki. 2008. Cooperative role of macrophages and neutrophils in host antiprotozoan resistance in mice acutely infected with Cryptosporidium parvum. Infect. Immun. 76: 3657-3663.
32. Peters, N. C., J. G. Egen, N. Secundino, A. Debrabant, N. Kimblin, S. Kamhawi, P. Lawyer, M. P. Fay, R. N. Germain, and D. Sacks. 2008. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321: 970-974.
33. Smith, D. F., C. S. Peacock, and A. K. Cruz. 2007. Comparative genomics: from genotype to disease phenotype in the leishmaniases. Int. J. Parasitol. 37: 1173-1186.
34. Pompeu, M. L., L. A. Freitas, M. L. Santos, M. Khouri, and M. Barral-Netto. 1991. Granulocytes in the inflammatory process of BALB/c mice infected by Leishmania amazonensis: a quantitative approach. Acta Trop. 48: 185-193.
35. Bomfim, G., B. B. Andrade, S. Santos, J. Clarencio, M. Barral-Netto, and A. Barral. 2007. Cellular analysis of cutaneous leishmaniasis lymphadenopathy: insights into the early phases of human disease. Am. J. Trop. Med. Hyg. 77: 854-859.
36. Guimaraes-Costa, A. B., M. T. Nascimento, G. S. Froment, R. P. Soares, F. N. Morgado, F. Conceicao-Silva, and E. M. Saraiva. 2009. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc. Natl. Acad. Sci. USA 106: 6748-6753.
37. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2: 965-975.
38. Sacks, D. L., and P. V. Perkins. 1984. Identification of an infective stage of Leishmania promastigotes. Science 223: 1417-1419.
39. Cassatella, M. A. 1995. The production of cytokines by polymorphonuclear neutrophils. Immunol. Today 16: 21-26.
40. Allenbach, C., C. Zufferey, C. Perez, P. Launois, C. Mueller, and F. Tacchini-Cottier. 2006. Macrophages induce neutrophil apoptosis through membrane TNF, a process amplified by Leishmania major. J. Immunol. 176: 6656-6664.
41. Silva, M. T., M. N. Silva, and R. Appelberg. 1989. Neutrophil-macrophage cooperation in the host defence against mycobacterial infections. Microb. Pathog. 6: 369-380.
42. Heifets, L., K. Imai, and M. B. Goren. 1980. Expression of peroxidase-dependent iodination by macrophages ingesting neutrophil debris. J. Reticuloendothel. Soc. 28: 391-404.
43. Tan, B. H., C. Meinken, M. Bastian, H. Bruns, A. Legaspi, M. T. Ochoa, S. R. Krutzik, B. R. Bloom, T. Ganz, R. L. Modlin, and S. Stenger. 2006. Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens. J. Immunol. 177: 1864-1871.
44. Venuprasad, K., P. P. Banerjee, S. Chattopadhyay, S. Sharma, S. Pal, P. B. Parab, D. Mitra, and B. Saha. 2002. Human neutrophil-expressed CD28 interacts with macrophage B7 to induce phosphatidylinositol 3-kinase-dependent IFN-γ secretion and restriction of Leishmania growth. J. Immunol. 169: 920-928.
45. Rogers, K. A., G. K. DeKrey, M. L. Mbow, R. D. Gillespie, C. I. Brodskyn, and R. G. Titus. 2002. Type 1 and type 2 responses to Leishmania major. FEMS Microb. Lett. 209: 1-7.
46. Maioli, T. U., E. Takane, R. M. Arantes, J. L. Fietto, and L. C. Afonso. 2004. Immune response induced by New World Leishmania species in C57BL/6 mice. Parasitol. Res. 94: 207-212.
47. Gantt, K. R., T. L. Goldman, M. L. McCormick, M. A. Miller, S. M. Jeronimo, E. T. Nascimento, B. E. Britigan, and M. E. Wilson. 2001. Oxidative responses of human and murine macrophages during phagocytosis of Leishmania chagasi. J. Immunol. 167: 893-901.
48. Goossens, V., J. Grooten, K. De Vos, and W. Fiers. 1995. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc. Natl. Acad. Sci. USA 92: 8115-8119.
49. Speer, C. P., M. J. Pabst, H. B. Hedegaard, R. F. Rest, and R. B. Johnston, Jr. 1984. Enhanced release of oxygen metabolites by monocyte-derived macrophages exposed to proteolytic enzymes: activity of neutrophil elastase and cathepsin G. J. Immunol. 133: 2151-2156.
50. Fadok, V. A., D. L. Bratton, L. Guthrie, and P. M. Henson. 2001. Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: role of proteases. J. Immunol. 166: 6847-6854.
51. Ribeiro-Gomes, F. L., M. C. Moniz-de-Souza, M. S. Alexandre-Moreira, W. B. Dias, M. F. Lopes, M. P. Nunes, G. Lungarella, and G. A. DosReis. 2007. Neutrophils activate macrophages for intracellular killing of Leishmania major through recruitment of TLR4 by neutrophil elastase. J. Immunol. 179: 3988-3994.
52. Smelt, S. C., S. E. Cotterell, C. R. Engwerda, and P. M. Kaye. 2000. B celldeficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. J. Immunol. 164: 3681-3688.
53. Rousseau, D., S. Demartino, B. Ferrua, J. F. Michiels, F. Anjuere, K. Fragaki, Y. Le Fichoux, and J. Kubar. 2001. In vivo involvement of polymorphonuclear neutrophils in Leishmania infantum infection. BMC Microbiol. 1: 17.