Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection

Journal of Leukocyte Biology

Volumn 82, Issue 2, 2007, Pages 288-299

  Charmoy, Mélanie ^a   Megnekou, Rosette ^a,b   Allenbach, Cindy ^a   Zweifel, Christine ^a   Perez, Cynthia ^a   Monnat, Katia ^a   Breton, Mélanie ^a   Ronet, Catherine ^a   Launois, Pascal ^a   Tacchini Cottier, Fabienne ^a,c  

^a WORLD HEALTH ORGANIZATION   (Switzerland)

^b UNIVERSITY OF YAOUNDÉ I   (Cameroon)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

IL 10; IL 12; Toll like receptors

Indexed keywords

ALPHA4 INTEGRIN; CD11B ANTIGEN; GAMMA INTERFERON; INTEGRIN; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 23; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL INFECTION; BONE MARROW; CONTROLLED STUDY; FEMALE; IMMUNE RESPONSE; INFECTION RESISTANCE; INFECTION SENSITIVITY; INOCULATION; LEISHMANIA MAJOR; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION;

ANIMALS; CELLS, CULTURED; DISEASE SUSCEPTIBILITY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNITY, NATURAL; INTERFERON TYPE II; INTERLEUKIN-10; INTERLEUKIN-12 SUBUNIT P40; LEISHMANIA MAJOR; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEUTROPHILS; NITRITES; PHENOTYPE; RNA, MESSENGER; TOLL-LIKE RECEPTORS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

LEISHMANIA MAJOR; MUS;

EID: 34547814686     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0706440     Document Type: Article

References (50)

1. Sacks, D., Noben-Trauth, N. (2002) The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2, 845-858.
2. Beil, W. J., Meinardus-Hager, G., Neugebauer, D. C., 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.
3. Sunderkotter, C., Kunz, M., Steinbrink, K., Meinardus-Hager, G., Goebeler, M., Bildau, H., Sorg, C. (1993) Resistance of mice to experimental leishmaniasis is associated with more rapid appearance of mature macrophages in vitro and in vivo. J. Immunol. 151, 4891-4901.
4. Tacchini-Cottier, F., Zweifel, C., Belkaid, Y., Mukankundiye, C., Vasei, M., Launois, P., Milon, G., Louis, J. A. (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.
5. Lima, G. M., Vallochi, A. L., Silva, U. R., Bevilacqua, E. M., Kiffer, M. M., Abrahamsohn, I. A. (1998) The role of polymorphonuclear leukocytes in the resistance to cutaneous leishmaniasis. Immunol. Lett. 64, 145-151.
6. Allenbach, C., Zufferey, C., Perez, C., Launois, P., Mueller, C., Tacchini-Cottier, F. (2006) Macrophages induce neutrophil apoptosis through membrane TNF, a process amplified by Leishmania major. J. Immunol. 176, 6656-6664.
7. Cassatella, M. A. (1999) Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol. 73, 369-509.
8. Louis, J., Moedder, E., Behin, R., Engers, H. (1979) Recognition of protozoan parasite antigens by murine T lymphocytes. I. Induction of specific T lymphocyte-dependent proliferative response to Leishmania tropica. Eur. J. Immunol. 9, 841-847.
9. Lopez, A. F., Strath, M., Sanderson, C. J. (1984) Differentiation antigens on mouse eosinophils and neutrophils identified by monoclonal antibodies. Br. J. Haematol. 57, 489-494.
10. Reiner, S. L., Zheng, S., Corry, D. B., Locksley, R. M. (1993) Constructing polycompetitor cDNAs for quantitative PCR. J. Immunol. Methods 165, 37-46.
11. Otten, L. A., Tacchini-Cottier, F., Lohoff, M., Annunziato, F., Cosmi, L., Scarpellino, L., Louis, J., Steimle, V., Reith, W., Acha-Orbea, H. (2003) Deregulated MHC class II transactivator expression leads to a strong Th2 bias in CD4(+) T lymphocytes. J. Immunol. 170, 1150-1157.
12. Heinzel, F. P., Hujer, A. M., Ahmed, F. N., Rerko, R. M. (1997) In vivo production and function of IL-12 p40 homodimers. J. Immunol. 158, 4381-4388.
13. Van Waarde, M. A., van Assen, A. J., Kampinga, H. H., Konings, A. W., Vujaskovic, Z. (1997) Quantification of transforming growth factor-β in biological material using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal. Biochem. 247, 45-51.
14. Chakour, R., Guler, R., Bugnon, M., Allenbach, C., Garcia, I., Mauel, J., Louis, J., Tacchini-Cottier, F. (2003) Both the Fas ligand and inducible nitric oxide synthase are needed for control of parasite replication within lesions in mice infected with Leishmania major whereas the contribution of tumor necrosis factor is minimal. Infect. Immun. 71, 5287-5295.
15. Coxon, A., Rieu, P., Barkalow, F. J., Askari, S., Sharpe, A. H., von Andrian, U. H., Arnaout, M. A., Mayadas, T. N. (1996) A novel role for the β 2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity 5, 653-666.
16. Rosenthal, L. A., Sutterwala, F. S., Kehrli, M. E., Mosser, D. M. (1996) Leishmania major-human macrophage interactions: cooperation between Mac-1 (CD11b/CD18) and complement receptor type 1 (CD35) in promastigote adhesion. Infect. Immun. 64, 2206-2215.
17. Tsuda, Y., Takahashi, H., Kobayashi, M., Hanafusa, T., Herndon, D. N., Suzuki, F. (2004) Three different neutrophil subsets exhibited in mice with different susceptibilities to infection by methicillin-resistant Staphylococcus aureus. Immunity 21, 215-226.
18. Yang, G. X., Hagmann, W. K. (2003) VLA-4 antagonists: potent inhibitors of lymphocyte migration. Med. Res. Rev. 23, 369-392.
19. Akira, S. (2006) TLR signaling. Curr. Top. Microbiol. Immunol. 311, 1-16.
20. Kropf, P., Freudenberg, M. A., Modolell, M., Price, H. P., Herath, S., Antoniazi, S., Galanos, C., Smith, D. F., Muller, I. (2004) Toll-like receptor 4 contributes to efficient control of infection with the protozoan parasite Leishmania major. Infect. Immun. 72, 1920-1928.
21. De Veer, M. J., Curtis, J. M., Baldwin, T. M., DiDonato, J. A., Sexton, A., McConville, M. J., Handman, E., Schofield, L. (2003) MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signaling. Eur. J. Immunol. 33, 2822-2831.
22. Calkins, C. M., Barsness, K., Bensard, D. D., Vasquez-Torres, A., Raeburn, C. D., Meng, X., McIntyre Jr., R. C. (2002) Toll-like receptor-4 signaling mediates pulmonary neutrophil sequestration in response to gram-positive bacterial enterotoxin. J. Surg. Res. 104, 124-130.
23. Fan, J., Malik, A. B. (2003) Toll-like receptor-4 (TLR4) signaling augments chemokine-induced neutrophil migration by modulating cell surface expression of chemokine receptors. Nat. Med. 9, 315-321.
24. Bellocchio, S., Moretti, S., Perruccio, K., Fallarino, F., Bozza, S., Montagnoli, C., Mosci, P., Lipford, G. B., Pitzurra, L., Romani, L. (2004) TLRs govern neutrophil activity in aspergillosis. J. Immunol. 173, 7406-7415.
25. Francois, S., El Benna, J., Dang, P. M., Pedruzzi, E., Gougerot-Pocidalo, M. A., Elbim, C. (2005) Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF- B signaling pathways, leading to increased levels of Mcl-1, A1, and phosphorylated Bad. J. Immunol. 174, 3633-3642.
26. Cassone, A., Chiani, P., Quinti, I., Torosantucci, A. (1997) Possible participation of polymorphonuclear cells stimulated by microbial immunomodulators in the dysregulated cytokine patterns of AIDS patients. J. Leukoc. Biol. 62, 60-66.
27. Hunter, C. A. (2005) New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat. Rev. Immunol. 5, 521-531.
28. Moore, K. W., de Waal Malefyt, R., Coffman, R. L., O'Garra, A. (2001) Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683-765.
29. Cassatella, M. A., Meda, L., Bonora, S., Ceska, M., Constantin, G. (1993) Interleukin 10 (IL-10) inhibits the release of proinflammatory cytokines from human polymorphonuclear leukocytes. Evidence for an autocrine role of tumor necrosis factor and IL-1 β in mediating the production of IL-8 triggered by lipopolysaccharide. J. Exp. Med. 178, 2207-2211.
30. Nathan, C. (2006) Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173-182.
31. Henderson Jr., W. R., Chi, E. Y., Albert, R. K., Chu, S. J., Lamm, W. J., Rochon, Y., Jonas, M., Christie, P. E., Harlan, J. M. (1997) Blockade of CD49d (α4 integrin) on intrapulmonary but not circulating leukocytes inhibits airway inflammation and hyperresponsiveness in a mouse model of asthma. J. Clin. Invest. 100, 3083-3092.
32. Parker, L. C., Whyte, M. K., Dower, S. K., Sabroe, I. (2005) The expression and roles of Toll-like receptors in the biology of the human neutrophil. J. Leukoc. Biol. 77, 886-892.
33. Hayashi, F., Means, T. K., Luster, A. D. (2003) Toll-like receptors stimulate human neutrophil function. Blood 102, 2660-2669.
34. Becker, I., Salaiza, N., Aguirre, M., Delgado, J., Carrillo-Carrasco, N., Kobeh, L. G., Ruiz, A., Cervantes, R., Torres, A. P., Cabrera, N., Gonzalez, A., Maldonado, C., Isibasi, A. (2003) Leishmania lipophosphoglycan (LPG) activates NK cells through Toll-like receptor-2. Mol. Biochem. Parasitol. 130, 65-74.
35. Flandin, J. F., Chano, F., Descoteaux, A. (2006) RNA interference reveals a role for TLR2 and TLR3 in the recognition of Leishmania donovani promastigotes by interferon-γ-primed macrophages. Eur. J. Immunol. 36, 411-420.
36. Shoda, L. K., Kegerreis, K. A., Suarez, C. E., Mwangi, W., Knowles, D. P., Brown, W. C. (2001) Immunostimulatory CpG-modified plasmid DNA enhances IL-12, TNF-α, and NO production by bovine macrophages. J. Leukoc. Biol. 70, 103-112.
37. Harris, T. H., Cooney, N. M., Mansfield, J. M., Paulnock, D. M. (2006) Signal transduction, gene transcription, and cytokine production triggered in macrophages by exposure to trypanosome DNA. Infect. Immun. 74, 4530-4537.
38. Trinchieri, G. (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3, 133-146.
39. Du, C., Sriram, S. (1998) Mechanism of inhibition of LPS-induced IL-12p40 production by IL-10 and TGF-β in ANA-1 cells. J. Leukoc. Biol. 64, 92-97.
40. Kato, K., Shimozato, O., Hoshi, K., Wakimoto, H., Hamada, H., Yagita, H., Okumura, K. (1996) Local production of the p40 subunit of interleukin 12 suppresses T-helper 1-mediated immune responses and prevents allogeneic myoblast rejection. Proc. Natl. Acad. Sci. USA 93, 9085-9089.
41. Ling, P., Gately, M. K., Gubler, U., Stern, A. S., Lin, P., Hollfelder, K., Su, C., Pan, Y. C., Hakimi, J. (1995) Human IL-12 p40 homodimer binds to the IL-12 receptor but does not mediate biologic activity. J. Immunol. 154, 116-127.
42. Hino, A., Kweon, M. N., Fujihashi, K., McGhee, J. R., Kiyono, H. (2004) Pathological role of large intestinal IL-12p40 for the induction of Th2-type allergic diarrhea. Am. J. Pathol. 164, 1327-1335.
43. Obata, F., Hoshino, A., Toyama, A. (2006) Hydrogen peroxide increases interleukin-12 p40/p70 molecular ratio and induces Th2-predominant responses in mice. Scand. J. Immunol. 63, 125-130.
44. Mattner, F., Di Padova, K., Alber, G. (1997) Interleukin-12 is indispensable for protective immunity against Leishmania major. Infect. Immun. 65, 4378-4383.
45. Oppmann, B., Lesley, R., Blom, B., Timans, J. C., Xu, Y., Hunte, B., Vega, F., Yu, N., Wang, J., Singh, K., et al. (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13, 715-725.
46. Aste-Amezaga, M., Ma, X., Sartori, A., Trinchieri, G. (1998) Molecular mechanisms of the induction of IL-12 and its inhibition by IL-10. J. Immunol. 160, 5936-5944.
47. Groux, H., Cottrez, F., Rouleau, M., Mauze, S., Antonenko, S., Hurst, S., McNeil, T., Bigler, M., Roncarolo, M. G., Coffman, R. L. (1999) A transgenic model to analyze the immunoregulatory role of IL-10 secreted by antigen-presenting cells. J. Immunol. 162, 1723-1729.
48. Hagenbaugh, A., Sharma, S., Dubinett, S. M., Wei, S. H., Aranda, R., Cheroutre, H., Fowell, D. J., Binder, S., Tsao, B., Locksley, R. M., Moore, K. W., Kronenberg, M. (1997) Altered immune responses in interleukin 10 transgenic mice. J. Exp. Med. 185, 2101-2110.
49. Chen, L., Zhang, Z. H., Watanabe, T., Yamashita, T., Kobayakawa, T., Kaneko, A., Fujiwara, H., Sendo, F. (2005) The involvement of neutrophils in the resistance to Leishmania major infection in susceptible but not in resistant mice. Parasitol. Int. 54, 109-118.
50. Ribeiro-Gomes, F. L., Otero, A. C., Gomes, N. A., Moniz-De-Souza, M. C., Cysne-Finkelstein, L., Arnholdt, A. C., Calich, V. L., Coutinho, S. G., Lopes, M. F., DosReis, G. A. (2004) Macrophage interactions with neutrophils regulate Leishmania major infection. J. Immunol. 172, 4454-4462.