Cathepsin B in Antigen-Presenting Cells Controls Mediators of the Th1 Immune Response during Leishmania major Infection

PLoS Neglected Tropical Diseases

Volumn 8, Issue 9, 2014, Pages

  Gonzalez Leal, Iris J ^a   Röger, Bianca ^a   Schwarz, Angela ^a   Schirmeister, Tanja ^b   Reinheckel, Thomas ^c   Lutz, Manfred B ^a   Moll, Heidrun ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CATHEPSIN B; CATHEPSIN L; CD40 ANTIGEN; CD86 ANTIGEN; CELL SURFACE MARKER; ENHANCED GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NITROUS OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; CELL POLARIZATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; IMMUNE RESPONSE; LEISHMANIASIS; MACROPHAGE; MOUSE; NONHUMAN; PARASITE EXAMINATION; PHENOTYPE; POLARIZATION; PROTEIN EXPRESSION; QUALITY CONTROL; REAL TIME POLYMERASE CHAIN REACTION; TH1 CELL; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTIGEN PRESENTATION; BAGG ALBINO MOUSE; BIOSYNTHESIS; DEFICIENCY; DISEASE MODEL; IMMUNOLOGY; LEISHMANIA MAJOR; TRANSGENIC MOUSE;

ANIMALS; ANTIGEN PRESENTATION; CATHEPSIN B; CATHEPSIN L; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; INTERLEUKIN-12; LEISHMANIA MAJOR; LEISHMANIASIS; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; TH1 CELLS; UP-REGULATION;

EID: 84907588630     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003194     Document Type: Article

References (66)

1. World Health Organization (2010) Control of the leishmaniasis: report of a meeting of the WHO Expert Commitee on the Control of Leishmaniases. Geneva: World Health Organization 949: : 949.
2. World Health Organization (2012) Leishmaniasis: worldwide epidemiological and drug access update. WHO. Available: http://www.who.int/leishmaniasis/resources/Leishmaniasis_worldwide_epidemiological_and_drug_access_update.pdf.
3. Mitchell GF, Anders RF, Brown GV, Handman E, Roberts-Thomson IC, et al. (1982) Analysis of infection characteristics and antiparasite immune responses in resistant compared with susceptible hosts. Immunol Rev 61: 137–188.
4. Stebut von E, (2007) Immunology of cutaneous leishmaniasis: the role of mast cells, phagocytes and dendritic cells for protective immunity. Eur J Dermatol 17: 115–122.
5. Moll H, Fuchs H, Blank C, Röllinghoff M, (1993) Langerhans cells transport Leishmania major from the infected skin to the draining lymph node for presentation to antigen-specific T cells. Eur J Immunol 23: 1595–1601.
6. Ritter U, Meissner A, Scheidig C, Körner H, (2004) CD8 alpha- and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. Eur J Immunol 34: 1542–1550.
7. Iezzi G, Fröhlich A, Ernst B, Ampenberger F, Saeland S, et al. (2006) Lymph node resident rather than skin-derived dendritic cells initiate specific T cell responses after Leishmania major infection. J Immunol 177: 1250–1256.
8. León B, López-Bravo M, Ardavín C, (2007) Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26: 519–531.
9. Petritus PM, Manzoni-de-Almeida D, Gimblet C, Lombana CG, Scott P, (2012) Leishmania mexicana induces limited recruitment and activation of monocytes and monocyte-derived dendritic cells early during infection. PLoS Negl Trop Dis 6: e1858.
10. Lutz MB, (2013) How quantitative differences in dendritic cell maturation can direct TH1/TH2-cell polarization. Oncoimmunology 2: e22796.
11. Mattner F, Magram J, Ferrante J, Launois P, Di Padova K, et al. (1996) Genetically resistant mice lacking interleukin-12 are susceptible to infection with Leishmania major and mount a polarized Th2 cell response. Eur J Immunol 26: 1553–1559.
12. Satoskar AR, Rodig S, Telford SR, Satoskar AA, Ghosh SK, et al. (2000) IL-12 gene-deficient C57BL/6 mice are susceptible to Leishmania donovani but have diminished hepatic immunopathology. Eur J Immunol 30: 834–839.
13. Heinzel FP, Schoenhaut DS, Rerko RM, Rosser LE, Gately MK, (1993) Recombinant interleukin 12 cures mice infected with Leishmania major. J Exp Med 177: 1505–1509.
14. Stebut von E, Belkaid Y, Jakob T, Sacks DL, Udey MC, (1998) Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skin-derived dendritic cells: implications for the initiation of anti-Leishmania immunity. J Exp Med 188: 1547–1552.
15. Zahn S, Kirschsiefen P, Jonuleit H, Steinbrink K, Stebut von E, (2010) Human primary dendritic cell subsets differ in their IL-12 release in response to Leishmania major infection. Exp Dermatol 19: 924–926.
16. Piedrafita D, Proudfoot L, Nikolaev AV, Xu D, Sands W, et al. (1999) Regulation of macrophage IL-12 synthesis by Leishmania phosphoglycans. Eur J Immunol 29: 235–244.
17. Carrera L, Gazzinelli RT, Badolato R, Hieny S, Muller W, et al. (1996) Leishmania promastigotes selectively inhibit interleukin 12 induction in bone marrow-derived macrophages from susceptible and resistant mice. J Exp Med 183: 515–526.
18. Belkaid Y, Butcher B, Sacks DL, (1998) Analysis of cytokine production by inflammatory mouse macrophages at the single-cell level: selective impairment of IL-12 induction in Leishmania-infected cells. Eur J Immunol 28: 1389–1400.
19. Nicholas J Lapara BLK, III (2010) Suppression of LPS-induced inflammatory responses in macrophages infected with Leishmania. Journal of Inflammation (London, England) 7: 8.
20. Silva-Almeida M, Pereira BA, Ribeiro-Guimarães M, Alves C, (2012) Proteinases as virulence factors in Leishmania spp. infection in mammals. Parasit Vectors 5: 160.
21. Cameron P, McGachy A, Anderson M, Paul A, Coombs GH, et al. (2004) Inhibition of lipopolysaccharide-induced macrophage IL-12 production by Leishmania mexicana amastigotes: the role of cysteine peptidases and the NF-kappaB signaling pathway. J Immunol 173: 3297–3304.
22. Williams RA, Tetley L, Mottram JC, Coombs GH, (2006) Cysteine peptidases CPA and CPB are vital for autophagy and differentiation in Leishmania mexicana. Mol Microbiol 61: 655–674.
23. Ponte-Sucre A, Vicik R, Schultheis M, Schirmeister T, Moll H, (2006) Aziridine-2,3-dicarboxylates, peptidomimetic cysteine protease inhibitors with antileishmanial activity. Antimicrob Agents Chemother 50: 2439–2447.
24. Schurigt U, Schad C, Glowa C, Baum U, Thomale K, et al. (2010) Aziridine-2,3-dicarboxylate-based cysteine cathepsin inhibitors induce cell death in Leishmania major associated with accumulation of debris in autophagy-related lysosome-like vacuoles. Antimicrob Agents Chemother 54: 5028–5041.
25. Maekawa Y, Himeno K, Ishikawa H, Hisaeda H, Sakai T, et al. (1998) Switch of CD4+ T cell differentiation from Th2 to Th1 by treatment with cathepsin B inhibitor in experimental leishmaniasis. J Immunol 161: 2120–2127.
26. Maekawa Y, Himeno K, Katunuma N, (1997) Cathepsin B-inhibitor promotes the development of Th1 type protective T cells in mice infected with Leishmania major. J Med Invest 44: 33–39.
27. Zhang T, Maekawa Y, Sakai T, Nakano Y, Hisaeda H, et al. (2001) Treatment with cathepsin L inhibitor potentiates Th2-type immune response in Leishmania major-infected BALB/c mice. Int Immunol 13: 975–982.
28. Onishi K, Li Y, Ishii K, Hisaeda H, Tang L, et al. (2004) Cathepsin L is crucial for a Th1-type immune response during Leishmania major infection. Microbes Infect 6: 468–474.
29. Lutz MB, Kukutsch N, Ogilvie AL, Rössner S, Koch F, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77–92.
30. Bringmann G, Thomale K, Bischof S, Schneider C, Schultheis M, et al. (2013) A novel Leishmania major amastigote assay in 96-well format for rapid drug screening and its use for discovery and evaluation of a new class of leishmanicidal quinolinium salts. Antimicrob Agents Chemother 57: 3003–3011.
31. Deussing J, Roth W, Saftig P, Peters C, Ploegh HL, et al. (1998) Cathepsins B and D are dispensable for major histocompatibility complex class II-mediated antigen presentation. Proc Natl Acad Sci USA 95: 4516–4521.
32. Halangk W, Lerch MM, Brandt-Nedelev B, Roth W, Ruthenbuerger M, et al. (2000) Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J Clin Invest 106: 773–781.
33. Roth W, Deussing J, Botchkarev VA, pauly-Evers M, Saftig P, et al. (2000) Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and pertubation of hair follicle cycling. FASEB J 14: 2075–2086.
34. Bogdan C, Moll H, Solbach W, Röllinghoff M, (1990) Tumor necrosis factor-alpha in combination with interferon-gamma, but not with interleukin 4 activates murine macrophages for elimination of Leishmania major amastigotes. Eur J Immunol 20: 1131–1135.
35. Collins TJ, (2007) ImageJ for microscopy. BioTechniques 43: 25–30.
36. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101–1108.
37. Mellman I, Steinman RM, (2001) Dendritic cells: specialized and regulated antigen processing machines. Cell 106: 255–258.
38. Lautwein A, Burster T, Lennon-Duménil A-M, Overkleeft HS, Weber E, et al. (2002) Inflammatory stimuli recruit cathepsin activity to late endosomal compartments in human dendritic cells. Eur J Immunol 32: 3348–3357.
39. Magister Š, Obermajer N, Mirković B, Svajger U, Renko M, et al. (2012) Regulation of cathepsins S and L by cystatin F during maturation of dendritic cells. Eur J Cell Biol 91: 391–401.
40. Ramírez-Pineda JR, Fröhlich A, Berberich C, Moll H, (2004) Dendritic cells (DC) activated by CpG DNA ex vivo are potent inducers of host resistance to an intracellular pathogen that is independent of IL-12 derived from the immunizing DC. J Immunol 172: 6281–6289.
41. Prina E, Abdi SZ, Lebastard M, Perret E, Winter N, et al. (2004) Dendritic cells as host cells for the promastigote and amastigote stages of Leishmania amazonensis: the role of opsonins in parasite uptake and dendritic cell maturation. J Cell Sci 117: 315–325.
42. Zhang T, Maekawa Y, Hanba J, Dainichi T, Nashed BF, et al. (2000) Lysosomal cathepsin B plays an important role in antigen processing, while cathepsin D is involved in degradation of the invariant chain inovalbumin-immunized mice. Immunology 100: 13–20.
43. Riese RJ, Wolf PR, Brömme D, Natkin LR, Villadangos JA, et al. (1996) Essential role for cathepsin S in MHC class II–associated invariant chain processing and peptide loading. Immunity 4: 357–366.
44. Riese RJ, Mitchell RN, Villadangos JA, Shi GP, Palmer JT, et al. (1998) Cathepsin S activity regulates antigen presentation and immunity. J Clin Invest 101: 2351–2363.
45. Shi GP, Villadangos JA, Dranoff G, Small C, Gu L, et al. (1999) Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10: 197–206.
46. Honey K, (2002) Cathepsin L Regulates CD4+ T Cell Selection Independently of Its Effect on Invariant Chain: A Role in the Generation of Positively Selecting Peptide Ligands. Journal of Experimental Medicine 195: 1349–1358.
47. Vidard L, Rock KL, Benacerraf B, (1991) The generation of immunogenic peptides can be selectively increased or decreased by proteolytic enzyme inhibitors. J Immunol 147: 1786–1791.
48. Reich M, Wieczerzak E, Jankowska E, Palesch D, Boehm BO, et al. (2009) Specific cathepsin B inhibitor is cell-permeable and activates presentation of TTC in primary human dendritic cells. Immunol Lett 123: 155–159.
49. Pletinckx K, Stijlemans B, Pavlovic V, Laube R, Brandl C, et al. (2011) Similar inflammatory DC maturation signatures induced by TNF or Trypanosoma brucei antigens instruct default Th2-cell responses. Eur J Immunol 41: 3479–3494.
50. Hosken NA, Shibuya K, Heath AW, Murphy KM, O'Garra A, (1995) The effect of antigen dose on CD4+ T helper cell phenotype development in a T cell receptor-alpha beta-transgenic model. J Exp Med 182: 1579–1584.
51. Bennett CL, Misslitz A, Colledge L, Aebischer T, Blackburn CC, (2001) Silent infection of bone marrow-derived dendritic cells by Leishmania mexicana amastigotes. Eur J Immunol 31: 876–883.
52. Pompei L, Jang S, Zamlynny B, Ravikumar S, McBride A, et al. (2007) Disparity in IL-12 release in dendritic cells and macrophages in response to Mycobacterium tuberculosis is due to use of distinct TLRs. J Immunol 178: 5192–5199.
53. Matsumoto F, Saitoh S-I, Fukui R, Kobayashi T, Tanimura N, et al. (2008) Cathepsins are required for Toll-like receptor 9 responses. Biochem Biophys Res Commun 367: 693–699.
54. Ewald SE, Engel A, Lee J, Wang M, Bogyo M, et al. (2011) Nucleic acid recognition by Toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J Exp Med 208: 643–651.
55. Ha S-D, Martins A, Khazaie K, Han J, Chan BMC, et al. (2008) Cathepsin B is involved in the trafficking of TNF-alpha-containing vesicles to the plasma membrane in macrophages. J Immunol 181: 690–697.
56. Schotte P, (2001) The cathepsin B inhibitor z-FA.fmk inhibits cytokine production in macrophages stimulated by lipopolysaccharide. Journal of Biological Chemistry 276: 21153–21157.
57. Montaser M, Lalmanach G, Mach L, (2002) CA-074, but not its methyl ester CA-074Me, is a selective inhibitor of cathepsin B within living cells. Biological Chemistry 383: 1305–1308.
58. Onishi K, Li Y, Ishii K, Hisaeda H, Tang L, et al. (2004) Cathepsin L is crucial for a Th1-type immune response during Leishmania major infection. Microbes Infect 6: 468–474.
59. Katunuma N, Murata E, Kakegawa H, Matsui A, Tsuzuki H, et al. (1999) Structure based development of novel specific inhibitors for cathepsin L and cathepsin S in vitro and in vivo. FEBS Lett 458: 6–10.
60. Ben-Othman R, Dellagi K, Guizani-Tabbane L, (2009) Leishmania major parasites induced macrophage tolerance: Implication of MAPK and NF-κB pathways. Mol Immunol 46: 3438–3444.
61. Ben-Othman R, Guizani-Tabbane L, Dellagi K, (2008) Leishmania initially activates but subsequently down-regulates intracellular mitogen-activated protein kinases and nuclear factor-κB signaling in macrophages. Mol Immunol 45: 3222–3229.
62. Feng GJ, Goodridge HS, Harnett MM, Wei XQ, Nikolaev AV, et al. (1999) Extracellular signal-related kinase (ERK) and p38 mitogen-activated protein (MAP) kinases differentially regulate the lipopolysaccharide-mediated induction of inducible nitric oxide synthase and IL-12 in macrophages: Leishmania phosphoglycans subvert macrophage IL-12 production by targeting ERK MAP kinase. J Immunol 163: 6403–6412.
63. Contreras I, Gomez MA, Nguyen O, Shio MT, McMaster RW, et al. (2010) Leishmania-induced inactivation of the macrophage transcription factor AP-1 is mediated by the parasite metalloprotease GP63. PLoS Pathog 6: e1001148.
64. Libermann TA, Baltimore D, (1990) Activation of interleukin-6 gene expression through the NF-kappa B transcription factor. Mol Cell Biol 10: 2327–2334.
65. Tedelind S, Poliakova K, Valeta A, Hunegnaw R, Yemanaberhan EL, et al. (2010) Nuclear cysteine cathepsin variants in thyroid carcinoma cells. Biological Chemistry 391: 923–935.
66. Turk B, Turk D, Turk V, (2012) Protease signalling: the cutting edge. EMBO J 31: 1630–1643.