Cystatin cures visceral leishmaniasis by NF-κB-mediated proinflammatory response through co-ordination of TLR/MyD88 signaling with p105-Tpl2-ERK pathway

European Journal of Immunology

Volumn 41, Issue 1, 2011, Pages 116-127

  Kar, Susanta ^a   Ukil, Anindita ^b   Das, Pijush K ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b UNIVERSITY OF CALCUTTA   (India)

Author keywords

Cystatin; Leishmaniasis; Macrophage; NF kB; Tumor progression locus 2

Indexed keywords

CELL PROTEIN; CYSTATIN; GAMMA INTERFERON; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN P105; PROTEIN TP12; PROTEIN TPL 2; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; UBIQUITINATION; VISCERAL LEISHMANIASIS;

ANIMALS; CYSTATINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; I-KAPPA B KINASE; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; LEISHMANIASIS, VISCERAL; MACROPHAGES; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED BALB C; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; PROTO-ONCOGENE PROTEINS; TOLL-LIKE RECEPTORS;

EID: 78650365533     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040533     Document Type: Article

References (45)

1. Barton, G. M. and Medzhitov, R., Toll-like receptor signaling pathways. Science 2003. 300: 1524-1525.
2. Qin, J., Jiang, Z., Qian, Y., Casanova, J. L. and Li, X., IRAK4 kinase activity is redundant for interleukin-1 (IL-1) receptor-associated kinase phosphorylation and IL-1 responsiveness. J. Biol. Chem. 2004. 279: 26748-26753.
3. Burns, K., Janssens, S., Brissoni, B., Olivos, N., Beyaert, R. and Tschopp, J., Inhibition of interleukin 1 receptor/Toll-like receptor signaling through the alternatively spliced, short form of MyD88 is due to its failure to recruit IRAK-4. J. Exp. Med. 2003. 197: 263-268.
4. Li, S., Strelow, A., Fontana, E. J. and Wesche, H., IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc. Natl. Acad. Sci. USA 2002. 99: 5567-5572.
5. Jiang, Z., Ninomiya-Tsuji, J., Qian, Y., Matsumoto, K. and Li, X., Interleukin-1 (IL-1) receptor-associated kinase-dependent IL-1-induced signaling complexes phosphorylate TAK1 and TAB2 at the plasma membrane and activate TAK1 in the cytosol. Mol. Cell. Biol. 2002. 22: 7158-7167.
6. Takaesu, G., Kishida, S., Hiyama, A., Yamaguchi, K., Shibuya, H., Irie, K., Ninomiya-Tsuji, J. and Matsumoto, K., TAB2, a novel adaptor protein, mediates activation of TAK1 MAPKKK by linking TAK1 to TRAF6 in the IL-1 signal transduction pathway. Mol. Cell 2000. 5: 649-658.
7. Lamothe, B., Besse, A., Campos, A. D., Webster, W. K., Wu, H. and Darnay, B. G., Site-specific Lys-63-linked tumor necrosis factor receptor-associated factor 6 auto-ubiquitination is a critical determinant of I kappa B kinase activation. J. Biol. Chem. 2007. 282: 4102-4112.
8. Kanayama, A., Seth, R. B., Sun, L., Ea, C. K., Hong, M., Shaito, A., Chiu, Y. H. et al., TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol. Cell 2004. 15: 535-548.
9. Dumitru, C. D., Ceci, J. D., Tsatsanis, C., Kontoyiannis, D., Stamatakis, K., Lin, J. H., Patriotis, C. et al., TNF-alpha induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 2000. 103: 1071-1083.
10. Watford, W. T., Hissong, B. D., Durant, L. R., Yamane, H., Muul, L. M., Kanno, Y., Tato, C. M. and Ramos, H. L., Tpl2 kinase regulates T cell interferon-gamma production and host resistance to Toxoplasma gondii. J. Exp. Med. 2008. 205: 2803-2812.
11. Mielke, L. A., Elkins, K. L., Wei, L., Starr, R., Tsichlis, P. N., O'Shea, J. J. and Watford, W. T., Tumor progression locus 2 (Map3k8) is critical for host defense against Listeria monocytogenes and IL-1 beta production. J. Immunol. 2009. 183: 7984-7993.
12. Salmeron, A., Ahmad, T. B., Carlile, G. W., Pappin, D., Narsimhan, R. P. and Ley, S. C., Activation of MEK-1 and SEK-1 by Tpl-2 proto-oncoprotein, a novel MAP kinase kinase kinase. EMBO J. 1996. 15: 817-826.
13. Eliopoulos, A. G., Wang, C. C., Dumitru, C. D. and Tsichlis, P. N., Tpl2 transduces CD40 and TNF signals that activate ERK and regulates IgE induction by CD40. EMBO J. 2003. 22: 3855-3864.
14. Beinke, S., Robinson, M. J., Salmeron, A., Hugunin, M., Allen, H. and Ley, S. C., Lipopolysaccharide activation of the TPL-2/MEK/extracellular signal-regulated kinase mitogen-activated protein kinase cascade is regulated by IkappaB kinase-induced proteolysis of NF-kappaB1 p105. Mol. Cell. Biol. 2004. 24: 9658-9667.
15. Karin, M. and Ben-Neriah, Y., Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 2000. 18: 621-663.
16. Nicholas, C., Batra, S., Vargo, M. A., Voss, O. H., Gavrilin, M. A., Wewers, M. D., Guttridge, D. C. et. al., Apigenin blocks lipopolysaccharide-induced lethality in vivo and proinflammatory cytokines expression by inactivating NF-{kappa}B through the suppression of p65 phosphorylation. J. Immunol. 2007. 179: 7121-7127.
17. Sacks, D. and Sher, A., Evasion of innate immunity by parasitic protozoa. Nat. Immunol. 2002. 3: 1041-1047.
18. Tuon, F. F., Amato, V. S., Bacha, H. A., Almusawi, T., Duarte, M. I. and Amato Neto, V., Toll-like receptors and leishmaniasis. Infect. Immun. 2008. 76: 866-872.
19. Hawn, T. R., Ozinsky, A., Underhill, D. M., Buckner, F. S., Akira, S. and Aderem, A., Leishmania major activates IL-1 alpha expression in macrophages through a MyD88-dependent pathway. Microbes Infect. 2002. 4: 763-771.
20. De Veer, M. J., Curtis, J. M., Baldwin, T. M., DiDonato, J. A., Sexton, A., McConville, M. J., Handman, E. and Schofield, L., MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signaling. Eur. J. Immunol. 2003. 33: 2822-2831.
21. Kropf, P., Freudenberg, M. A., Modolell, M., Price, H. P., Herath, S., Antoniazi, S., Galanos, C. et al., Toll-like receptor 4 contributes to efficient control of infection with the protozoan parasite Leishmania major. Infect. Immun. 2004. 72: 1920-1928.
22. Liese, J., Schleicher, U. and Bogdan, C., TLR9 signaling is essential for the innate NK cell response in murine cutaneous leishmaniasis. Eur. J. Immunol. 2007. 37: 3424-3434.
23. Schleicher, U., Liese, J., Knippertz, I., Kurzmann, C., Hesse, A., Heit, A., Fishcer, J. A. and Weiss, S., NK cell activation in visceral leishmaniasis requires TLR9, myeloid DCs, and IL-12, but is independent of plasmacytoid DCs. J. Exp. Med. 2007. 204: 893-906.
24. Becker, I., Salaiza, N., Aguirre, M., Delgado, J., Carrillo-Carrasco, N., Kobeh, L. G., Ruiz, A. et al., Leishmania lipophosphoglycan (LPG) activates NK cells through Toll-like receptor-2. Mol. Biochem. Parasitol. 2003. 130: 65-74.
25. Flandin, J. F., Chano, F. and Descoteaux, A., RNA interference reveals a role for TLR2 and TLR3 in the recognition of Leishmania donovani promastigotes by interferon-gamma-primed macrophages. Eur. J. Immunol. 2006. 36: 411-420.
26. Vargas-Inchaustegui, D. A., Tai, W., Xin, L., Hogg, A. E., Corry, D. B. and Soong, L., Distinct roles for MyD88 and Toll-like receptor 2 during Leishmania braziliensis infection in mice. Infect. Immun. 2009. 77: 2948-2956.
27. Das, L., Datta, N., Bandyopadhyay, S. and Das, P. K., Successful therapy of lethal murine visceral leishmaniasis with cystatin involves up-regulation of nitric oxide and a favorable T cell response. J. Immunol. 2001. 166: 4020-4028.
28. Kar, S., Ukil, A. and Das, P. K., Signaling events leading to the curative effect of cystatin on experimental visceral leishmaniasis: involvement of ERK1/2, NF-kappaB and JAK/STAT pathways. Eur. J. Immunol. 2009. 39: 1-11.
29. Abu-Dayyeh, I., Shio, M. T., Sato, S., Akira, S., Cousineau, B. and Olivier, M., Leishmania-induced IRAK-1 inactivation is mediated by SHP-1 interacting with an evolutionarily conserved KTIM motif. Plos. Negl. Trop. Dis. 2008. 2: e305.
30. Mukherjee, S., Ukil, A. and Das, P. K., Immunomodulatory peptide from cystatin, a natural cysteine protease inhibitor, using leishmaniasis as model macrophage disease. Antimicrob. Agents Chemother. 2007. 51: 1700-1707.
31. Tato, C. M. and Hunter, C. A., Host-pathogen interactions: subversion and utilization of the NF-kappa B pathway during infection. Infect. Immun. 2002. 70: 3311-3317.
32. Artis, D., Speirs, K., Joyce, K., Goldsmidt, M., Camaano, J., Hunter, A. and Scott, P., NF-kappa B1 is required for optimal CD4+Th1 cell development and resistance to Leishmania major. J. Immunol. 2003. 170: 1995-2003.
33. Speirs, K., Camaano, J., Goldsmidt, M. H., Hunter, C. A. and Scott, P., NF-kappa B2 is required for optimal CD40-induced IL-12 production but dispensable for Th1 cell Differentiation. J. Immunol. 2002. 168: 4406-4413.
34. Kontgen, F., Grumont, R. J., Strasser, A., Metcalf, D., Li, R., Tarlinton, D. and Gerondakis, S., Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 1995. 9: 1965-1977.
35. Grigoriadis, G., Zhan, Y., Grumont, R. J., Metcalf, D., Handman, E., Cheers, C. and Gerondakis, S., The Rel subunit of NF-kappaB-like transcription factors is a positive and negative regulator of macrophage gene expression: distinct roles for Rel in different macrophage populations. EMBO J. 1996. 15: 7099-7107.
36. Eliopoulos, A. G., Dumitru, C. D., Wang, C. C., Cho, J. and Tsichlis, P. N., Induction of COX-2 by LPS in macrophages is regulated by Tpl2-dependent CREB activation signals. EMBO J. 2002. 21: 4831-4840.
37. Swantek, J. L., Christerson, L. and Cobb, M. H., Lipopolysaccharide-induced tumor necrosis factor-alpha promoter activity is inhibitor of nuclear factor-kappaB kinase-dependent. J. Biol. Chem. 1999. 274: 11667-11671.
38. Udalova, I. A., Knight, J. C., Vidal, V., Nedospasov, S. A. and Kwiatkowski, D., Complex NF-kappaB interactions at the distal tumor necrosis factor promoter region in human monocytes. J. Biol. Chem. 1998. 273: 21178-21186.
39. Muzio, M., Ni, J., Feng, P. and Dixit, V. M., IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 1997. 278: 1612-1615.
40. Jensen, L. E., Muzio, M., Mantovani, A. and Whitehead, A. S., IL-1 signaling cascade in liver cells and the involvement of a soluble form of the IL-1 receptor accessory protein 2. J. Immunol. 2000. 164: 5277-5286.
41. Ishida, T., Mizushima, S., Azuma, S., Kobayashi, N., Tojo, T., Suzuki, K., Aizawa, S. et al., Identification of TRAF6, a novel TNF receptor-associated factor protein that mediates signaling from an amino-terminal domain of the CD40 cytoplasmic region. J. Biol. Chem. 1996. 271: 28745-28748.
42. Shibuya, H., Yamaguchi, K., Shirakabe, K., Tonegawa, A., Gotoh, Y., Ueno, N., Irie, K. et al., TAB1: an activator of the TAK1 MAPKKK in TGF-beta signal transduction. Science 1996. 272:1179-1182.
43. Deak, M., Clifton, A. D., Lucocq, L. M. and Alessi, D. R., Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 1998. 17: 4426-4441.
44. Kar, S., Ukil, A., Sharma, G. and Das, P. K., MAPK-directed phosphatases preferentially regulate pro- and anti-inflammatory cytokines in experimental visceral leishmaniasis: involvement of distinct protein kinase C isoforms. J. Leukoc. Biol. 2010. 88: 9-20.
45. Ukil, A., Biswas, A., Das, T. and Das, P. K., 18 Beta-glycyrrhetinic acid triggers curative Th1 response and nitric oxide up-regulation in experimental visceral leishmaniasis associated with the activation of NF-kappa B. J. Immunol. 2005. 175: 1161-1169.