MPO-ANCA induces IL-17 production by activated neutrophils in vitro via its Fc region- and complement-dependent manner

Journal of Autoimmunity

Volumn 31, Issue 1, 2008, Pages 79-89

  Hoshino, Akiyoshi ^a,b,c   Nagao, Tomokazu ^c,d   Nagi Miura, Noriko ^e   Ohno, Naohito ^e   Yasuhara, Masato ^b   Yamamoto, Kenji ^a,b   Nakayama, Toshinori ^d   Suzuki, Kazuo ^c,d  

^a NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

Author keywords

Glucan; ANCA; Autoantibodies; Autoimmunity; Candida albicans; Chemokine; Complement; Coronary arteritis; Crescentic glomerulonephritis; Cytokine; Fungal infection; IL 17A; IL 23; Inflammation; Mannoprotein; Myeloperoxidase; Neutrophils; Vasculitis

Indexed keywords

CYTOKINE; INTERLEUKIN 17; INTERLEUKIN 17 A; INTERLEUKIN 23; INTERLEUKIN 6; MANNOPROTEIN; MYELOPEROXIDASE; NEUTROPHIL CYTOPLASMIC ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; COMPLEMENT CLASSICAL PATHWAY; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYSTEMIC VASCULITIS;

ANIMALS; ANTIBODIES, ANTINEUTROPHIL CYTOPLASMIC; AUTOANTIBODIES; CELLS, CULTURED; COMPLEMENT PATHWAY, CLASSICAL; INTERLEUKIN-17; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; NEUTROPHIL ACTIVATION; NEUTROPHILS; PEROXIDASE; VASCULITIS;

EID: 43649100486     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2008.03.006     Document Type: Article

References (57)

1. Aratani Y., Kura F., Watanabe H., Akagawa H., Takano Y., Suzuki K., et al. Critical role of myeloperoxidase and nicotinamide adenine dinucleotide phosphate-oxidase in high-burden systemic infection of mice with Candida albicans. J Infect Dis 185 (2002) 1833-1837
2. El Messaoudi K., Verheyden A.M., Thiry L., Fourez S., Tasiaux N., Bollen A., et al. Human recombinant myeloperoxidase antiviral activity on cytomegalovirus. J Med Virol 66 (2002) 218-223
3. Klebanoff S.J., and Coombs R.W. Viricidal effect of polymorphonuclear leukocytes on human immunodeficiency virus-1. Role of the myeloperoxidase system. J Clin Invest 89 (1992) 2014-2017
4. Moguilevsky N., Steens M., Thiriart C., Prieels J.P., Thiry L., and Bollen A. Lethal oxidative damage to human immunodeficiency virus by human recombinant myeloperoxidase. FEBS Lett 302 (1992) 209-212
5. Aratani Y., Kura F., Watanabe H., Akagawa H., Takano Y., Suzuki K., et al. Relative contributions of myeloperoxidase and NADPH-oxidase to the early host defense against pulmonary infections with Candida albicans and Aspergillus fumigatus. Med Mycol 40 (2002) 557-563
6. Gross W.L., Schmitt W.H., and Csernok E. ANCA and associated diseases: immunodiagnostic and pathogenetic aspects. Clin Exp Immunol 91 (1993) 1-12
7. Lesavre P., Noel L.H., Gayno S., Nusbaum P., Reumaux D., Erlinger S., et al. Atypical autoantigen targets of perinuclear antineutrophil cytoplasm antibodies (P-ANCA): specificity and clinical associations. J Autoimmun 6 (1993) 185-195
8. Muso E., Ito-Ihara T., Ono T., Imai E., Yamagata K., Akamatsu A., et al. Intravenous immunoglobulin (IVIg) therapy in MPO-ANCA related polyangiitis with rapidly progressive glomerulonephritis in Japan. Jpn J Infect Dis 57 (2004) S17-S18
9. Heeringa P., Huugen D., and Tervaert J.W. Anti-neutrophil cytoplasmic autoantibodies and leukocyte-endothelial interactions: a sticky connection?. Trends Immunol 26 (2005) 561-564
10. Aratani Y., Kura F., Watanabe H., Akagawa H., Takano Y., Suzuki K., et al. Differential host susceptibility to pulmonary infections with bacteria and fungi in mice deficient in myeloperoxidase. J Infect Dis 182 (2000) 1276-1279
11. Ichimori K., Fukuyama N., Nakazawa H., Aratani Y., Koyama H., Takizawa S., et al. Myeloperoxidase has directly-opposed effects on nitration reaction - study on myeloperoxidase-deficient patient and myeloperoxidase-knockout mice. Free Radic Res 37 (2003) 481-489
12. Xiao H., Heeringa P., Hu P., Liu Z., Zhao M., Aratani Y., et al. Antineutrophil cytoplasmic autoantibodies specific for myeloperoxidase cause glomerulonephritis and vasculitis in mice. J Clin Invest 110 (2002) 955-963
13. Harper L., Radford D., Plant T., Drayson M., Adu D., and Savage C.O. IgG from myeloperoxidase-antineutrophil cytoplasmic antibody-positive patients stimulates greater activation of primed neutrophils than IgG from proteinase 3-antineutrophil cytosplasmic antibody-positive patients. Arthritis Rheum 44 (2001) 921-930
14. Hoshino A., Nagao T., Ito-Ihara T., Ishida-Okawara A., Uno K., Muso E., et al. Trafficking of QD-conjugated MPO-ANCA in murine systemic vasculitis and glomerulonephritis model mice. Microbiol Immunol 51 (2007) 551-566
15. Ishida-Okawara A., Ito-Ihara T., Muso E., Ono T., Saiga K., Nemoto K., et al. Neutrophil contribution to the crescentic glomerulonephritis in SCG/Kj mice. Nephrol Dial Transplant 19 (2004) 1708-1715
16. Hamano Y., Tsukamoto K., Abe M., Sun G.D., Zhang D., Fujii H., et al. Genetic dissection of vasculitis, myeloperoxidase-specific antineutrophil cytoplasmic autoantibody production, and related traits in spontaneous crescentic glomerulonephritis-forming/Kinjoh mice. J Immunol 176 (2006) 3662-3673
17. McKenzie B.S., Kastelein R.A., and Cua D.J. Understanding the IL-23-IL-17 immune pathway. Trends Immunol 27 (2006) 17-23
18. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201 (2005) 233-240
19. Murphy C.A., Langrish C.L., Chen Y., Blumenschein W., McClanahan T., Kastelein R.A., et al. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 198 (2003) 1951-1957
20. Ferretti S., Bonneau O., Dubois G.R., Jones C.E., and Trifilieff A. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J Immunol 170 (2003) 2106-2112
21. Nagao T., Matsumura M., Mabuchi A., Ishida-Okawara A., Koshio O., Nakayama T., et al. Up-regulation of adhesion molecule expression in glomerular endothelial cells by anti-myeloperoxidase antibody. Nephrol Dial Transplant 22 (2007) 77-87
22. Csernok E. Anti-neutrophil cytoplasmic antibodies and pathogenesis of small vessel vasculitides. Autoimmun Rev 2 (2003) 158-164
23. Little M.A., Smyth C.L., Yadav R., Ambrose L., Cook H.T., Nourshargh S., et al. Antineutrophil cytoplasm antibodies directed against myeloperoxidase augment leukocyte-microvascular interactions in vivo. Blood 106 (2005) 2050-2058
24. Kurihara K., Shingo Y., Miura N.N., Horie S., Usui Y., Adachi Y., et al. Effect of CAWS, a mannoprotein-beta-glucan complex of Candida albicans, on leukocyte, endothelial cell, and platelet functions in vitro. Biol Pharm Bull 26 (2003) 233-240
25. Hoshino A., Ohnishi N., Yasuhara M., Yamamoto K., and Kondo A. Separation of murine neutrophils and macrophages by thermoresponsive magnetic nanoparticles. Biotechnol Prog 23 (2007) 1513-1516
26. Ishida-Okawara A., Nagi-Miura N., Oharaseki T., Takahashi K., Okumra A., Tachikawa H., et al. Neutrophil activation and arteritis induced by C. albicans water-soluble mannoprotein-beta-glucan complex (CAWS). Exp Mol Pathol 82 (2007) 220-226
27. Khanna D., Aggarwal A., Bhakuni D.S., Dayal R., and Misra R. Bactericidal/permeability-increasing protein and cathepsin G are the major antigenic targets of antineutrophil cytoplasmic autoantibodies in systemic sclerosis. J Rheumatol 30 (2003) 1248-1252
28. Hoshino A., Nagao T., Nakasuga A., Ishida-Okawara A., Suzuki K., Yasuhara M., et al. Nanocrystal quantum dot-conjugated anti-myeloperoxidase antibody as the detector of activated neutrophils. IEEE Trans Nanobiosci 6 (2007) 341-345
29. Lavigne L.M., Albina J.E., and Reichner J.S. Beta-glucan is a fungal determinant for adhesion-dependent human neutrophil functions. J Immunol 177 (2006) 8667-8675
30. Shinohara H., Nagi-Miura N., Ishibashi K., Adachi Y., Ishida-Okawara A., Oharaseki T., et al. Beta-mannosyl linkages negatively regulate anaphylaxis and vasculitis in mice, induced by CAWS, fungal PAMPS composed of mannoprotein-beta-glucan complex secreted by Candida albicans. Biol Pharm Bull 29 (2006) 1854-1861
31. Buhl A.M., Avdi N., Worthen G.S., and Johnson G.L. Mapping of the C5a receptor signal transduction network in human neutrophils. Proc Natl Acad Sci U S A 91 (1994) 9190-9194
32. Rollins T.E., Siciliano S., Kobayashi S., Cianciarulo D.N., Bonilla-Argudo V., Collier K., et al. Purification of the active C5a receptor from human polymorphonuclear leukocytes as a receptor-Gi complex. Proc Natl Acad Sci U S A 88 (1991) 971-975
33. Siciliano S.J., Rollins T.E., and Springer M.S. Interaction between the C5a receptor and Gi in both the membrane-bound and detergent-solubilized states. J Biol Chem 265 (1990) 19568-19574
34. Kolls J.K., and Linden A. Interleukin-17 family members and inflammation. Immunity 21 (2004) 467-476
35. Gafa V., Lande R., Gagliardi M.C., Severa M., Giacomini E., Remoli M.E., et al. Human dendritic cells following Aspergillus fumigatus infection express the CCR7 receptor and a differential pattern of interleukin-12 (IL-12), IL-23, and IL-27 cytokines, which lead to a Th1 response. Infect Immun 74 (2006) 1480-1489
36. Huang W., Na L., Fidel P.L., and Schwarzenberger P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 190 (2004) 624-631
37. Kleinschek M.A., Muller U., Brodie S.J., Stenzel W., Kohler G., Blumenschein W.M., et al. IL-23 enhances the inflammatory cell response in Cryptococcus neoformans infection and induces a cytokine pattern distinct from IL-12. J Immunol 176 (2006) 1098-1106
38. Uchiyama M., Ohno N., Miura N.N., Adachi Y., Aizawa M.W., Tamura H., et al. Chemical and immunochemical characterization of limulus factor G-activating substance of Candida spp. FEMS Immunol Med Microbiol 24 (1999) 411-420
39. Taylor P.R., Tsoni S.V., Willment J.A., Dennehy K.M., Rosas M., Findon H., et al. Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol 8 (2007) 31-38
40. Saijo S., Fujikado N., Furuta T., Chung S.H., Kotaki H., Seki K., et al. Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat Immunol 8 (2007) 39-46
41. Willment J.A., Gordon S., and Brown G.D. Characterization of the human beta-glucan receptor and its alternatively spliced isoforms. J Biol Chem 276 (2001) 43818-43823
42. Brown G.D., Taylor P.R., Reid D.M., Willment J.A., Williams D.L., Martinez-Pomares L., et al. Dectin-1 is a major beta-glucan receptor on macrophages. J Exp Med 196 (2002) 407-412
43. Gantner B.N., Simmons R.M., Canavera S.J., Akira S., and Underhill D.M. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med 197 (2003) 1107-1117
44. Brown G.D., Herre J., Williams D.L., Willment J.A., Marshall A.S., and Gordon S. Dectin-1 mediates the biological effects of beta-glucans. J Exp Med 197 (2003) 1119-1124
45. Rogers N.C., Slack E.C., Edwards A.D., Nolte M.A., Schulz O., Schweighoffer E., et al. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22 (2005) 507-517
46. Leibundgut-Landmann S., Gross O., Robinson M.J., Osorio F., Slack E.C., Tsoni S.V., et al. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat Immunol 8 (2007) 549-551
47. Happel K.I., Zheng M., Young E., Quinton L.J., Lockhart E., Ramsay A.J., et al. Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. J Immunol 170 (2003) 4432-4436
48. Jefford M., Schnurr M., Toy T., Masterman K.A., Shin A., Beecroft T., et al. Functional comparison of DCs generated in vivo with Flt3 ligand or in vitro from blood monocytes: differential regulation of function by specific classes of physiologic stimuli. Blood 102 (2003) 1753-1763
49. Smits H.H., van Beelen A.J., Hessle C., Westland R., de Jong E., Soeteman E., et al. Commensal Gram-negative bacteria prime human dendritic cells for enhanced IL-23 and IL-27 expression and enhanced Th1 development. Eur J Immunol 34 (2004) 1371-1380
50. Fedele G., Stefanelli P., Spensieri F., Fazio C., Mastrantonio P., and Ausiello C.M. Bordetella pertussis-infected human monocyte-derived dendritic cells undergo maturation and induce Th1 polarization and interleukin-23 expression. Infect Immun 73 (2005) 1590-1597
51. Zhou L., Ivanov I.I., Spolski R., Min R., Shenderov K., Egawa T., et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 8 (2007) 967-974
52. Nurieva R., Yang X.O., Martinez G., Zhang Y., Panopoulos A.D., Ma L., et al. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448 (2007) 480-483
53. Korn T., Bettelli E., Gao W., Awasthi A., Jager A., Strom T.B., et al. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448 (2007) 484-487
54. Kaneko Y., Nimmerjahn F., and Ravetch J.V. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313 (2006) 670-673
55. Park-Min K.H., Serbina N.V., Yang W., Ma X., Krystal G., Neel B.G., et al. FcgammaRIII-dependent inhibition of interferon-gamma responses mediates suppressive effects of intravenous immune globulin. Immunity 26 (2007) 67-78
56. Ishida-Okawara A., Oharaseki T., Takahashi K., Hashimoto Y., Aratani Y., Koyama H., et al. Contribution of myeloperoxidase to coronary artery vasculitis associated with MPO-ANCA production. Inflammation 25 (2001) 381-387
57. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., et al. Neutrophil extracellular traps kill bacteria. Science 303 (2004) 1532-1535