A new function of the Fas-FasL pathway in macrophage activation

Journal of Leukocyte Biology

Volumn 86, Issue 1, 2009, Pages 81-90

  Chakour, Reza ^a   Allenbach, Cindy ^a   Desgranges, Florian ^a   Charmoy, Mélanie ^a   Mauel, Jacques ^a   Garcia, Irène ^c   Launois, Pascal ^a   Louis, Jacques ^a,b   Tacchini Cottier, Fabienne ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Leishmania; Toll like receptors; Tumor necrosis factor (TNF)

Indexed keywords

FAS ANTIGEN; FAS LIGAND; GAMMA INTERFERON; INTERLEUKIN 4; INTERLEUKIN 6; NITRIC OXIDE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL KILLING; CONTROLLED STUDY; CYTOKINE RELEASE; HOMEOSTASIS; LEISHMANIA MAJOR; MACROPHAGE ACTIVATION; MICROBIAL ACTIVITY; MODULATION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; IMMUNOLOGY; MACROPHAGE; METABOLISM; PARASITOLOGY; SECRETION;

LEISHMANIA MAJOR; MUS; PROTOZOA;

ANIMALS; ANTIGENS, CD95; FAS LIGAND PROTEIN; INTERFERON-GAMMA; INTERLEUKIN-4; LEISHMANIA MAJOR; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED BALB C; SIGNAL TRANSDUCTION;

EID: 68849125850     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1008590     Document Type: Article

References (55)

1. Wei, X. Q., Charles, I. G., Smith, A., Ure, J., Feng, G. J., Huang, F. P., Xu, D., Muller, W., Moncada, S., Liew, F. Y. (1995) Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375, 408-411.
2. Swihart, K., Fruth, U., Messmer, N., Hug, K., Behin, R., Huang, S., Del Giudice, G., Aguet, M., Louis, J. A. (1995) Mice from a genetically resistant background lacking the interferon γ receptor are susceptible to infection with Leishmania major but mount a polarized T helper cell 1-type CD4+ T cell response. J. Exp. Med. 181, 961-971.
3. Wang, Z. E., Zheng, S., Corry, D. B., Dalton, D. K., Seder, R. A., Reiner, S. L., Locksley, R. M. (1994) Interferon γ-independent effects of interleukin 12 administered during acute or established infection due to Leishmania major. Proc. Natl. Acad. Sci. USA 91, 12932-12936.
4. Liew, F. Y., Millott, S., Parkinson, C., Palmer, R. M., Moncada, S. (1990) Macrophage killing of Leishmania parasite in vivo is mediated by nitric oxide from L-arginine. J. Immunol. 144, 4794-4797. (Pubitemid 20224118)
5. Mitchell, G. F., Curtis, J. M., Handman, E., McKenzie, I. F. (1980) Cutaneous leishmaniasis in mice: disease patterns in reconstituted nude mice of several genotypes infected with Leishmania tropica. Aust. J. Exp. Biol. Med. Sci. 58, 521-532. (Pubitemid 11082912)
6. Holaday, B. J., Sadick, M. D., Wang, Z. E., Reiner, S. L., Heinzel, F. P., Parslow, T. G., Locksley, R. M. (1991) Reconstitution of Leishmania immunity in severe combined immunodeficient mice using Th1- and Th2-like cell lines. J. Immunol. 147, 1653-1658.
7. Liew, F. Y., Millott, S., Li, Y., Lelchuk, R., Chan, W. L., Ziltener, H. (1989) Macrophage activation by interferon-γ from host-protective T cells is inhibited by interleukin (IL)3 and IL4 produced by disease-promoting T cells in leishmaniasis. Eur. J. Immunol. 19, 1227-1232. (Pubitemid 19196900)
8. Ohmori, Y., Hamilton, T. A. (1997) IL-4-induced STAT6 suppresses IFN-γ-stimulated STAT1-dependent transcription in mouse macrophages. J. Immunol. 159, 5474-5482. (Pubitemid 127470075)
9. Holscher, C., Arendse, B., Schwegmann, A., Myburgh, E., Brombacher, F. (2006) Impairment of alternative macrophage activation delays cutaneous leishmaniasis in nonhealing BALB/c mice. J. Immunol. 176, 1115-1121. (Pubitemid 43099713)
10. Conceicao-Silva, F., Hahne, M., Schroter, M., Louis, J., Tschopp, J. (1998) The resolution of lesions induced by Leishmania major in mice requires a functional Fas (APO-1, CD95) pathway of cytotoxicity. Eur. J. Immunol. 28, 237-245. (Pubitemid 28048294)
11. Huang, F. P., Xu, D., Esfandiari, E. O., Sands, W., Wei, X. Q., Liew, F. Y. (1998) Mice defective in Fas are highly susceptible to Leishmania major infection despite elevated IL-12 synthesis, strong Th1 responses, and enhanced nitric oxide production. J. Immunol. 160, 4143-4147. (Pubitemid 28217264)
12. Eidsmo, L., Nylen, S., Khamesipour, A., Hedblad, M. A., Chiodi, F., Akuffo, H. (2005) The contribution of the Fas/FasL apoptotic pathway in ulcer formation during Leishmania major-induced cutaneous leishmaniasis. Am. J. Pathol. 166, 1099-1108. (Pubitemid 40524434)
13. Eidsmo, L., Wolday, D., Berhe, N., Sabri, F., Satti, I., El Hassan, A. M., Sundar, S., Chiodi, F., Akuffo, H. (2002) Alteration of Fas and Fas ligand expression during human visceral leishmaniasis. Clin. Exp. Immunol. 130, 307-313. (Pubitemid 35286219)
14. Ashkenazi, A., Dixit, V. M. (1998) Death receptors: signaling and modulation. Science 281, 1305-1308.
15. Krammer, P. H. (2000) CD95's deadly mission in the immune system. Nature 407, 789-795.
16. Nagata, S. (1997) Apoptosis by death factor. Cell 88, 355-365.
17. Lens, S. M., Kataoka, T., Fortner, K. A., Tinel, A., Ferrero, I., MacDonald, R. H., Hahne, M., Beermann, F., Attinger, A., Orbea, H. A., Budd, R. C., Tschopp, J. (2002) The caspase 8 inhibitor c-FLIP(L) modulates T-cell receptor-induced proliferation but not activation-induced cell death of lymphocytes. Mol. Cell. Biol. 22, 5419-5433. (Pubitemid 34755753)
18. Kabra, N. H., Kang, C., Hsing, L. C., Zhang, J., Winoto, A. (2001) T cell-specific FADD-deficient mice: FADD is required for early T cell development. Proc. Natl. Acad. Sci. USA 98, 6307-6312. (Pubitemid 32488235)
19. Thome, M., Tschopp, J. (2001) Regulation of lymphocyte proliferation and death by FLIP. Nat. Rev. Immunol. 1, 50-58. (Pubitemid 33741975)
20. 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. (Pubitemid 37070776)
21. Desbarats, J., Stone, J. E., Lin, L., Zakeri, Z. F., Davis, G. S., Pfeiffer, L. M., Titus, R. G., Newell, M. K. (2000) Rapid early onset lymphocyte cell death in mice resistant, but not susceptible to Leishmania major infection. Apoptosis 5, 189-196. (Pubitemid 30399393)
22. Wilhelm, P., Wiede, F., Meissner, A., Donhauser, N., Bogdan, C., Korner, H. (2005) TNF but not Fas ligand provides protective anti-L. major immunity in C57BL/6 mice. Microbes Infect. 7, 1461-1468. (Pubitemid 41785720)
23. Hu, W. H., Johnson, H., Shu, H. B. (2000) Activation of NF-κB by FADD, Casper, and caspase-8. J. Biol. Chem. 275, 10838-10844. (Pubitemid 30212715)
24. Hoshino, K., Takeuchi, O., Kawai, T., Sanjo, H., Ogawa, T., Takeda, Y., Takeda, K., Akira, S. (1999) Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162, 3749-3752. (Pubitemid 29314747)
25. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagami, M., Nakanishi, K., Akira, S. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9, 143-150. (Pubitemid 28361303)
26. Fruth, U., Solioz, N., Louis, J. A. (1993) Leishmania major interferes with antigen presentation by infected macrophages. J. Immunol. 150, 1857-1864. (Pubitemid 23129662)
27. 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. (Pubitemid 10135897)
28. Garcia, I., Miyazaki, Y., Araki, K., Araki, M., Lucas, R., Grau, G. E., Milon, G., Belkaid, Y., Montixi, C., Lesslauer, W., et al. (1995) Transgenic mice expressing high levels of soluble TNF-R1 fusion protein are protected from lethal septic shock and cerebral malaria, and are highly sensitive to Listeria monocytogenes and Leishmania major infections. Eur. J. Immunol. 25, 2401-2407.
29. Vercelli, D., Jabara, H. H., Lee, B. W., Woodland, N., Geha, R. S., Leung, D. Y. (1988) Human recombinant interleukin 4 induces Fc ε R2/CD23 on normal human monocytes. J. Exp. Med. 167, 1406-1416. (Pubitemid 18121712)
30. Ding, A. H., Nathan, C. F., Stuehr, D. J. (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141, 2407-2412.
31. 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. (Pubitemid 43787849)
32. Aliprantis, A. O., Weiss, D. S., Zychlinsky, A. (2001) Toll-like receptor-2 transduces signals for NF-κ B activation, apoptosis and reactive oxygen species production. J. Endotoxin Res. 7, 287-291.
33. Aliprantis, A. O., Yang, R. B., Weiss, D. S., Godowski, P., Zychlinsky, A. (2000) The apoptotic signaling pathway activated by Toll-like receptor-2. EMBO J. 19, 3325-3336. (Pubitemid 30428210)
34. Horng, T., Medzhitov, R. (2001) Drosophila MyD88 is an adapter in the Toll signaling pathway. Proc. Natl. Acad. Sci. USA 98, 12654-12658. (Pubitemid 33020001)
35. Fukui, M., Imamura, R., Umemura, M., Kawabe, T., Suda, T. (2003) Pathogen-associated molecular patterns sensitize macrophages to Fas ligand-induced apoptosis and IL-1 β release. J. Immunol. 171, 1868-1874. (Pubitemid 36966469)
36. Ma, Y., Liu, H., Tu-Rapp, H., Thiesen, H. J., Ibrahim, S. M., Cole, S. M., Pope, R. M. (2004) Fas ligation on macrophages enhances IL-1R1-Toll-like receptor 4 signaling and promotes chronic inflammation. Nat. Immunol. 5, 380-387. (Pubitemid 38500086)
37. Bogdan, C., Rollinghoff, M., Diefenbach, A. (2000) Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr. Opin. Immunol. 12, 64-76. (Pubitemid 30093452)
38. Rittig, M. G., Bogdan, C. (2000) Leishmania-host-cell interaction: complexities and alternative views. Parasitol. Today 16, 292-297.
39. Perlman, H., Pagliari, L. J., Georganas, C., Mano, T., Walsh, K., Pope, R. M. (1999) FLICE-inhibitory protein expression during macrophage differentiation confers resistance to fas-mediated apoptosis. J. Exp. Med. 190, 1679-1688. (Pubitemid 30002349)
40. Ahn, J. H., Park, S. M., Cho, H. S., Lee, M. S., Yoon, J. B., Vilcek, J., Lee, T. H. (2001) Non-apoptotic signaling pathways activated by soluble Fas ligand in serum-starved human fibroblasts. Mitogen-activated protein kinases and NF-κB-dependent gene expression. J. Biol. Chem. 276, 47100-47106. (Pubitemid 37373085)
41. Kataoka, T., Budd, R. C., Holler, N., Thome, M., Martinon, F., Irmler, M., Burns, K., Hahne, M., Kennedy, N., Kovacsovics, M., Tschopp, J. (2000) The caspase-8 inhibitor FLIP promotes activation of NF-κB and Erk signaling pathways. Curr. Biol. 10, 640-648. (Pubitemid 30354699)
42. Park, D. R., Thomsen, A. R., Frevert, C. W., Pham, U., Skerrett, S. J., Kiener, P. A., Liles, W. C. (2003) Fas (CD95) induces proinflammatory cytokine responses by human monocytes and monocyte-derived macrophages. J. Immunol. 170, 6209-6216. (Pubitemid 36682605)
43. Ribeiro-Gomes, F. L., Moniz-de-Souza, M. C., Borges, V. M., Nunes, M. P., Mantuano-Barradas, M., D'Avila, H., Bozza, P. T., Calich, V. L., DosReis, G. A. (2005) Turnover of neutrophils mediated by Fas ligand drives Leishmania major infection. J. Infect. Dis. 192, 1127-1134. (Pubitemid 41266813)
44. Shi, S., Nathan, C., Schnappinger, D., Drenkow, J., Fuortes, M., Block, E., Ding, A., Gingeras, T. R., Schoolnik, G., Akira, S., Takeda, K., Ehrt, S. (2003) MyD88 primes macrophages for full-scale activation by interferon-γ yet mediates few responses to Mycobacterium tuberculosis. J. Exp. Med. 198, 987-997. (Pubitemid 37248615)
45. Bagchi, A., Herrup, E. A., Warren, H. S., Trigilio, J., Shin, H. S., Valentine, C., Hellman, J. (2007) MyD88-dependent and MyD88-independent pathways in synergy, priming, and tolerance between TLR agonists. J. Immunol. 178, 1164-1171. (Pubitemid 46095190)
46. Olivier, M., Gregory, D. J., Forget, G. (2005) Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin. Microbiol. Rev. 18, 293-305. (Pubitemid 40548295)
47. Blos, M., Schleicher, U., Soares Rocha, F. J., Meissner, U., Rollinghoff, M., Bogdan, C. (2003) Organ-specific and stage-dependent control of Leishmania major infection by inducible nitric oxide synthase and phagocyte NADPH oxidase. Eur. J. Immunol. 33, 1224-1234. (Pubitemid 36609140)
48. Michaelson, J. S. (2000) The Daxx enigma. Apoptosis 5, 217-220.
49. Brune, B., Sandau, K., von Knethen, A. (1998) Apoptotic cell death and nitric oxide: activating and antagonistic transducing pathways. Biochemistry (Mosc.) 63, 817-825. (Pubitemid 128588111)
50. Niinobu, T., Fukuo, K., Yasuda, O., Tsubakimoto, M., Mogi, M., Nishimaki, H., Morimoto, S., Ogihara, T. (2000) Negative feedback regulation of activated macrophages via Fas-mediated apoptosis. Am. J. Physiol. Cell Physiol. 279, C504-C509. (Pubitemid 30679589)
51. Suda, T., Okazaki, T., Naito, Y., Yokota, T., Arai, N., Ozaki, S., Nakao, K., Nagata, S. (1995) Expression of the Fas ligand in cells of T cell lineage. J. Immunol. 154, 3806-3813.
52. Zhang, X., Brunner, T., Carter, L., Dutton, R. W., Rogers, P., Bradley, L., Sato, T., Reed, J. C., Green, D., Swain, S. L. (1997) Unequal death in T helper cell (Th)1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J. Exp. Med. 185, 1837-1849. (Pubitemid 27242205)
53. Ashany, D., Song, X., Lacy, E., Nikolic-Zugic, J., Friedman, S. M., Elkon, K. B. (1995) Th1 CD4+ lymphocytes delete activated macrophages through the Fas/APO-1 antigen pathway. Proc. Natl. Acad. Sci. USA 92, 11225-11229.
54. Dockrell, D. H., Badley, A. D., Villacian, J. S., Heppelmann, C. J., Algeciras, A., Ziesmer, S., Yagita, H., Lynch, D. H., Roche, P. C., Leibson, P. J., Paya, C. V. (1998) The expression of Fas ligand by macrophages and its upregulation by human immunodeficiency virus infection. J. Clin. Invest. 101, 2394-2405. (Pubitemid 28270434)
55. Ramsdell, F., Seaman, M. S., Miller, R. E., Picha, K. S., Kennedy, M. K., Lynch, D. H. (1994) Differential ability of Th1 and Th2 T cells to express Fas ligand and to undergo activation-induced cell death. Int. Immunol. 6, 1545-1553. (Pubitemid 24317863)