T cell-macrophage interactions and granuloma formation in vasculitis

Frontiers in Immunology

Volumn 5, Issue SEP, 2014, Pages

  Hilhorst, Marc ^a   Shirai, Tsuyoshi ^a   Berry, Gerald ^a   Goronzy, Jörg J ^a   Weyand, Cornelia M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dendritic cell; Granuloma; Macrophage; T cell; Vasculitis

Indexed keywords

CD14 ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROSTAGLANDIN E2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; CD4+ CD25+ T LYMPHOCYTE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; DENDRITIC CELL; DOWN REGULATION; GRANULOMA; GRANULOMATOSIS; IMMUNE DEFICIENCY; MACROPHAGE; MICROENVIRONMENT; MICROSCOPIC POLYANGIITIS; REVIEW; T LYMPHOCYTE; UPREGULATION; VASCULITIS; VITAMIN D INTOXICATION;

EID: 84919427792     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00432     Document Type: Review

References (168)

1. Krutzik SR, Tan B, Li H, Ochoa MT, Liu PT, Sharfstein SE, et al. TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat Med (2005) 11:653-60. doi:10.1038/nm1246
2. Nathan C. Metchnikoff's legacy in 2008. Nat Immunol (2008) 9:695-8. doi:10.1038/ni0708-695
3. Ramakrishnan L. Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol (2012) 12:352-66. doi:10.1038/nri3211
4. Gordon S. Alternative activation of macrophages. Nat Rev Immunol (2003) 3:23-35. doi:10.1038/nri978
5. Shi C, Pamer E. Monocyte recruitment during infection and inflammation. Nat Rev Immunol (2011) 11:762-74. doi:10.1038/nri3070
6. Hume D. Macrophages as APC and the dendritic cell myth. J Immunol (2008) 181:5829-35. doi:10.4049/jimmunol.181.9.5829
7. Vodovotz Y, Bogdan C, Paik J, Xie QW, Nathan C. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor beta. J Exp Med (1993) 178:605-13. doi:10.1084/jem.178.2.605
8. Mills C. M1 and M2 macrophages: oracles of health and disease. Crit Rev Immunol (2012) 32:463-88. doi:10.1615/CritRevImmunol.v32.i6.10
9. Stout R. Editorial: macrophage functional phenotypes: no alternatives in dermal wound healing? J Leukoc Biol (2010) 87:19-21. doi:10.1189/jlb.0509311
10. Mosser D, Edwards J. Exploring the full spectrum of macrophage activation. Nat Rev Immunol (2008) 8:958-69. doi:10.1038/nri2448
11. Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity (2011) 34:637-50. doi:10.1016/j.immuni.2011.05.006
12. Beutler B. TLRs and innate immunity. Blood (2009) 113:1399-407. doi:10.1182/blood-2008-07-019307
13. Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science (2010) 327:291-5. doi:10.1126/science.1183021
14. Mills K. TLR-dependent T cell activation in autoimmunity. Nat Rev Immunol (2011) 11:807-22. doi:10.1038/nri3095
15. Miller Y, Choi SH, Wiesner P, Fang L, Harkewicz R, Hartvigsen K, et al. Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res (2011) 108:235-48. doi:10.1161/CIRCRESAHA.110.223875
16. Moore KJ, Sheedy FJ, Fisher EA. Macrophages in atherosclerosis: a dynamic balance. Nat Rev Immunol (2013) 13:709-21. doi:10.1038/nri3520
17. Reynolds JM, Pappu BP, Peng J, Martinez GJ, Zhang Y, Chung Y, et al. Toll-like receptor 2 signaling in CD4+ T lymphocytes promotes T helper 17 responses and regulates the pathogenesis of autoimmune disease. Immunity (2010) 32:692-702. doi:10.1016/j.immuni.2010.04.010
18. Unanue E. Antigen-presenting function of the macrophage. Annu Rev Immunol (1984) 2:395-428. doi:10.1146/annurev.iy.02.040184.002143
19. Janeway C. The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol Today (1992) 13:11-6. doi:10.1016/0167-5699(92)90198-G
20. Rosenthal A, Shevach E. Function of macrophages in antigen recognition by guinea pig T lymphocytes. I. Requirement for histocompatible macrophages and lymphocytes. J Exp Med (1973) 138:1194-212. doi:10.1084/jem.138.5.1194
21. Blum JS, Wearsch PA, Cresswell P. Pathways of antigen processing. Annu Rev Immunol (2013) 31:443-73. doi:10.1146/annurev-immunol-032712-095910
22. Liu Y, Janeway C. Cells that present both specific ligand and costimulatory activity are the most efficient inducers of clonal expansion of normal CD4 T cells. Proc Natl Acad Sci U S A (1992) 89:3845-9. doi:10.1073/pnas.89.9.3845
23. Miga A, Masters S, Gonzalez M, Noelle RJ. The role of CD40-CD154 interactions in the regulation of cell mediated immunity. Immunol Invest (2000) 29:111-4. doi:10.3109/08820130009062292
24. Chen L, Flies D. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol (2013) 13:227-42. doi:10.1038/nri3405
25. Mahnke YD, Brodie TM, Sallusto F, Roederer M, Lugli E. The who's who of T-cell differentiation: human memory T-cell subsets. Eur J Immunol (2013) 43:2797-809. doi:10.1002/eji.201343751
26. Zhu J, Paul W. Peripheral CD4+ T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol Rev (2010) 238:247-62. doi:10.1111/j.1600-065X.2010.00951.x
27. Pozzi LA, Maciaszek JW, Rock KL. Both dendritic cells and macrophages can stimulate naive CD8 T cells in vivo to proliferate, develop effector function, and differentiate into memory cells. J Immunol (2005) 175:2071-81. doi:10.4049/jimmunol.175.4.2071
28. Rothoeft T, Gonschorek A, Bartz H, Anhenn O, Schauer U. Antigen dose, type of antigen-presenting cell and time of differentiation contribute to the T helper 1/T helper 2 polarization of naive T cells. Immunology (2003) 110:430-9. doi:10.1111/j.1365-2567.2003.01758.x
29. Itano A, Jenkins M. Antigen presentation to naive CD4 T cells in the lymph node. Nat Immunol (2003) 4:733-9. doi:10.1038/ni957
30. Macatonia SE, Hosken NA, Litton M, Vieira P, Hsieh CS, Culpepper JA, et al. Dendritic cells produce IL-12 and direct the development of Th1 cells from naive CD4+ T cells. J Immunol (1995) 154:5071-9.
31. Hsieh C, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science (1993) 260:547-9. doi:10.1126/science.8097338
32. Spörri R, Reis e Sousa C. Inflammatory mediators are insufficient for full dendritic cell activation and promote expansion of CD4+ T cell populations lacking helper function. Nat Immunol (2005) 6:163-70. doi:10.1038/ni1162
33. Segura E, Touzot M, Bohineust A, Cappuccio A, Chiocchia G, Hosmalin A, et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity (2013) 38:336-48. doi:10.1016/j.immuni.2012.10.018
34. Francisco LM, Salinas VH, Brown KE, Vanguri VK, Freeman GJ, Kuchroo VK, et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med (2009) 206:3015-29. doi:10.1084/jem.20090847
35. Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol (2007) 8:1086-94. doi:10.1038/ni1511
36. Walunas TL, Lenschow DJ, Bakker CY, Linsley PS, Freeman GJ, Green JM, et al. CTLA-4 can function as a negative regulator of T cell activation. Immunity (1994) 1:405-13. doi:10.1016/1074-7613(94)90071-X
37. Ueda H, Howson JM, Esposito L, Heward J, Snook H, Chamberlain G, et al. Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease. Nature (2003) 423:506-11. doi:10.1038/nature01621
38. Nishimura H, Nose M, Hiai H, Minato N, Honjo T. Development of Lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity (1999) 11:141-51. doi:10.1016/S1074-7613(00)80089-8
39. Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Sharpe AH. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity (1995) 3:541. doi:10.1016/1074-7613(95)90125-6
40. Brown JA, Dorfman DM, Ma FR, Sullivan EL, Munoz O, Wood CR, et al. Blockade of programmed death-1 ligands on dendritic cells enhances T cell activation and cytokine production. J Immunol (2003) 170:1257-66. doi:10.4049/jimmunol.170.3.1257
41. Castiblanco J, Arcos-Burgos M, Anaya JM. What is next after the genes for autoimmunity? BMC Med (2013) 11:197. doi:10.1186/1741-7015-11-197
42. Rai E, Wakeland E. Genetic predisposition to autoimmunity - what have we learned? Sem Immunol (2011) 23:67-83. doi:10.1016/j.smim.2011.01.015
43. Hoves S, Krause SW, Schütz C, Halbritter D, Schölmerich J, Herfarth H, et al. Monocyte-derived human macrophages mediate anergy in allogeneic T cells and induce regulatory T cells. J Immunol (2006) 177:2691-8. doi:10.4049/jimmunol.177.4.2691
44. Taylor MD, Harris A, Nair MG, Maizels RM, Allen JE. F4/80+ alternatively activated macrophages control CD4+ T cell hyporesponsiveness at sites peripheral to filarial infection. J Immunol (2006) 176:6918-27. doi:10.4049/jimmunol.176.11.6918
45. Dillon S, Agrawal S, Banerjee K, Letterio J, Denning TL, Oswald-Richter K, et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J Clin Invest (2006) 116:916-28. doi:10.1172/JCI27203
46. Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. Induction of interleukin 10-producing, nonproliferating CD4+ T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med (2000) 192:1213-22. doi:10.1084/jem.192.9.1213
47. Doedens AL, Stockmann C, Rubinstein MP, Liao D, Zhang N, DeNardo DG, et al. Macrophage expression of hypoxia-inducible factor-1a suppresses T-cell function and promotes tumor progression. Cancer Res (2010) 70:7465-75. doi:10.1158/0008-5472.CAN-10-1439
48. Dang EV, Barbi J, Yang HY, Jinasena D, Yu H, Zheng Y, et al. Control of TH17/Treg balance by hypoxia-inducible factor 1. Cell (2011) 146:772-84. doi:10.1016/j.cell.2011.07.033
49. Konisti S, Kiriakidis S, Paleolog EM. Hypoxia - a key regulator of angiogenesis and inflammation in rheumatoid arthritis. Nat Rev Rheumatol (2012) 8:153-62. doi:10.1038/nrrheum.2011.205
50. Stout RD, Jiang C, Matta B, Tietzel I, Watkins SK, Suttles J. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J Immunol (2005) 175:342-9. doi:10.4049/jimmunol.175.1.342
51. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol (2000) 164:6166-73. doi:10.4049/jimmunol.164.12.6166
52. Modolell M, Corraliza IM, Link F, Soler G, Eichmann K. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by Th1 and Th2 cytokines. Eur J Immunol (1995) 25:1101-4. doi:10.1002/eji.1830250436
53. Jovanovic DV, Di Battista JA, Martel-Pelletier J, Jolicoeur FC, He Y, Zhang M, et al. IL-17 Stimulates the production and expression of proinflammatory cytokines, IL-1b and TNF-a, by human macrophages. J Immunol (1998) 160:3513-21.
54. Zizzo G, Cohen P. IL-17 Stimulates differentiation of human anti-Inflammatory macrophages and phagocytosis of apoptotic neutrophils in response to IL-10 and glucocorticoids. J Immunol (2013) 190:5237-46. doi:10.4049/jimmunol.1203017
55. Lin AM, Rubin CJ, Khandpur R, Wang JY, Riblett M, Yalavarthi S, et al. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J Immunol (2011) 187:490-500. doi:10.4049/jimmunol.1100123
56. Coury F, Annels N, Rivollier A, Olsson S, Santoro A, Speziani C, et al. Langerhans cell histiocytosis reveals a new IL-17A-dependent pathway of dendritic cell fusion. Nat Med (2008) 14:81-7. doi:10.1038/nm1694
57. + immunoregulatory T cells is antigen nonspecific. J Immunol (2000) 164:183-90. doi:10.4049/jimmunol.164.1.183
58. Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJ, John S, Taams LS. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci U S A (2007) 104:19446-51. doi:10.1073/pnas.0706832104
59. Taams LS, van Amelsfort JM, Tiemessen MM, Jacobs KM, de Jong EC, Akbar AN, et al. Modulation of monocyte/macrophage function by human CD4+CD25+ regulatory T cells. Hum Immunol (2005) 66:222-30. doi:10.1016/j.humimm.2004.12.006
60. Kim KD, Zhao J, Auh S, Yang X, Du P, Tang H, et al. Adaptive immune cells temper initial innate responses. Nat Med (2007) 13:1248-52. doi:10.1038/nm1633
61. Guarda G, Dostert C, Staehli F, Cabalzar K, Castillo R, Tardivel A, et al. T cells dampen innate immune responses through inhibition of NLRP1 and NLRP3 inflammasomes. Nature (2009) 460:269-74. doi:10.1038/nature08100
62. Petersen H, Smith A. The role of the innate immune system in granulomatous disorders. Front Immunol (2013) 4:120. doi:10.3389/fimmu.2013.00120
63. Adams D. The granulomatous inflammatory response. Am J Pathol (1976) 84:164-92.
64. Williams G, Williams W. Granulomatous inflammation - a review. J Clin Pathol (1983) 36:723-33. doi:10.1136/jcp.36.7.723
65. Zumla A, Raviglione M, Hafner R, von Reyn CF. Tuberculosis. N Engl J Med (2013) 368:745-55. doi:10.1056/NEJMra1200894
66. Ulrichs T, Kaufmann S. New insights into the function of granulomas in human tuberculosis. J Pathol (2006) 208:261-9. doi:10.1002/path.1906
67. Saunders B, Britton W. Life and death in the granuloma: immunopathology of tuberculosis. Immunol Cell Biol (2007) 85:103-11. doi:10.1038/sj.icb.7100027
68. Weinberg JB, Hobbs MM, Misukonis MA. Recombinant human gamma-interferon induces human monocyte polykaryon formation. Proc Natl Acad Sci U S A (1984) 81:4554-7. doi:10.1073/pnas.81.14.4554
69. Broos C, van Nimwegen M, Hoogsteden HC, Hendriks RW, Kool M, van den Blink B. Granuloma formation in pulmonary sarcoidosis. Front Immunol (2013) 4:437. doi:10.3389/fimmu.2013.00437
70. Christophi GP, Caza T, Curtiss C, Gumber D, Massa PT, Landas SK. Gene expression profiles in granuloma tissue reveal novel diagnostic markers in sarcoidosis. Exp Mol Pathol (2014) 96:393-9. doi:10.1016/j.yexmp.2014.04.006
71. Kindler V, Sappino AP, Grau GE, Piguet PF, Vassalli P. The inducing role of tumor necrosis factor in the development of bactericidal granulomas during BCG infection. Cell (1989) 56:731-40. doi:10.1016/0092-8674(89)90676-4
72. Bean AG, Roach DR, Briscoe H, France MP, Korner H, Sedgwick JD, et al. Structural deficiencies in granuloma formation in TNF gene-targeted mice underlie the heightened susceptibility to aerosol Mycobacterium tuberculosis infection, which is not compensated for by lymphotoxin. J Immunol (1999) 162:3504-11.
73. Garcia Vidal C, Rodríguez Fernández S, Martínez Lacasa J, Salavert M, Vidal R, Rodríguez Carballeira M, et al. Paradoxical response to antituberculous therapy in infliximab-treated patients with disseminated tuberculosis. Clin Infect Dis (2005) 40:756-9. doi:10.1086/427941
74. Visvanathan S, Rahman MU, Hoffman GS, Xu S, García-Martínez A, Segarra M, et al. Tissue and serum markers of inflammation during the follow-up of patients with giant-cell arteritis - a prospective longitudinal study. Rheumatology (2011) 50:2061-70. doi:10.1093/rheumatology/ker163
75. Ten Berge B, Paats MS, Bergen IM, van denBlink B, Hoogsteden HC, Lambrecht BN, et al. Increased IL-17A expression in granulomas and in circulating memory T cells in sarcoidosis. Rheumatology (2012) 51:37-46. doi:10.1093/rheumatology/ker316
76. Rieber N, Hector A, Kuijpers T, Roos D, Hartl D. Current concepts of hyperinflammation in chronic granulomatous disease. Clin Dev Immunol (2012) 2012:252460. doi:10.1155/2012/252460
77. Baehner R, Nathan D. Leukocyte oxidase: defective activity in chronic granulomatous disease. Science (1967) 155:835-6. doi:10.1126/science.155.3764.835
78. Fernandez-Boyanapalli RF, Frasch SC, McPhillips K, Vandivier RW, Harry BL, Riches DW, et al. Impaired apoptotic cell clearance in CGD due to altered macrophage programming is reversed by phosphatidylserine-dependent production of IL-4. Blood (2009) 113:2047-55. doi:10.1182/blood-2008-05-160564
79. Adams J, Gacad M. Characterization of 1 alpha-hydroxylation of vitamin D3 sterols by cultured alveolar macrophages from patients with sarcoidosis. J Exp Med (1985) 161:755-65. doi:10.1084/jem.161.4.755
80. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, et al. Toll-like receptor triggering of a vitamin d-mediated human antimicrobial response. Science (2006) 311:1770-3. doi:10.1126/science.1123933
81. Fabri M, Stenger S, Shin DM, Yuk JM, Liu PT, Realegeno S, et al. Vitamin D is required for IFN-γ-mediated antimicrobial activity of human macrophages. Sci Transl Med (2011) 3:104ra2. doi:10.1126/scitranslmed.3003045
82. Gatenby PA, Lucas RM, Engelsen O, Ponsonby AL, Clements M. Antineutrophil cytoplasmic antibody-associated vasculitides: could geographic patterns be explained by ambient ultraviolet radiation? Arthritis Rheum (2009) 61:1417-24. doi:10.1002/art.24790
83. de Lindvan Wijngaarden RA, van Rijn L, Hagen EC, Watts RA, Gregorini G, Tervaert JW, et al. Hypotheses on the etiology of antineutrophil cytoplasmic autoantibody-associated vasculitis: the cause is hidden, but the result is known. Clin J Am Soc Nephrol (2008) 3:237-52. doi:10.2215/CJN.03550807
84. Salvarani C, Cantini F, Hunder GG. Polymyalgia rheumatica and giant-cell arteritis. Lancet (2008) 372:234-45. doi:10.1016/S0140-6736(08)61077-6
85. Weyand CM, Liao YJ, Goronzy JJ. The immunopathology of giant cell arteritis: diagnostic and therapeutic implications. J Neuroophthalmol (2012) 32:259-65. doi:10.1097/WNO.0b013e318268aa9b
86. Weyand C, Goronzy J. Clinical practice. Giant-cell arteritis and polymyalgia rheumatica. N Engl J Med (2014) 371:50-7. doi:10.1056/NEJMcp1214825
87. Weyand C, Goronzy J. Immune mechanisms in medium and large-vessel vasculitis. Nat Rev Rheumatol (2013) 9:731-40. doi:10.1038/nrrheum.2013.161
88. Sewell GW, Marks DJ, Segal AW. The immunopathogenesis of Crohn's disease: a three-stage model. Curr Opin Immunol (2009) 21:506-13. doi:10.1016/j.coi.2009.06.003
89. Abraham C, Cho J. Inflammatory bowel disease. N Engl J Med (2009) 361:2066-78. doi:10.1056/NEJMra0804647
90. Bhatt AS, Manzo VE, Pedamallu CS, Duke F, Cai D, Bienfang DC, et al. Brief report: in search of a candidate pathogen for giant cell arteritis: sequencing-based characterization of the giant cell arteritis microbiome. Arthritis Rheumatol (2014) 66:1939-44. doi:10.1002/art.38631
91. Rodríguez-Pla A, Stone JH. Vasculitis and systemic infections. Curr Opin Rheumatol (2006) 18:39-47. doi:10.1097/01.bor.0000197999.58073.2e
92. Krupa WM, Dewan M, Jeon MS, Kurtin PJ, Younge BR, Goronzy JJ, et al. Trapping of misdirected dendritic cells in the granulomatous lesions of giant cell arteritis. Am J Pathol (2002) 161:1815-23. doi:10.1016/S0002-9440(10)64458-6
93. Deng J, Younge BR, Olshen RA, Goronzy JJ, Weyand CM. Th17 and Th1 T-cell responses in giant cell arteritis. Circulation (2010) 121:906-15. doi:10.1161/CIRCULATIONAHA.109.872903
94. Weyand CM, Younge BR, Goronzy JJ. IFN-γ and IL-17: the two faces of T-cell pathology in giant cell arteritis. Curr Opin Rheumatol (2011) 23:43-9. doi:10.1097/BOR.0b013e32833ee946
95. + dendritic cells secrete high levels of IL-12 and potently prime cytotoxic T-cell responses. Blood (2013) 122:932-42. doi:10.1182/blood-2013-04-495424
96. Ghosh P, Borg FA, Dasgupta B. Current understanding and management of giant cell arteritis and polymyalgia rheumatica. Expert Rev Clin Immunol (2010) 6:913-28. doi:10.1586/eci.10.59
97. Deng J, Ma-Krupa W, Gewirtz AT, Younge BR, Goronzy JJ, Weyand CM. Toll-like receptors 4 and 5 induce distinct types of vasculitis. Circ Res (2009) 104:488-95. doi:10.1161/CIRCRESAHA.108.185777
98. Baldassare JJ, Bi Y, Bellone CJ. The role of p38 mitogen-activated protein kinase in IL-1 ß transcription. J Immunol (1999) 162:5367-73.
99. Dasgupta B, Panayi G. Interleukin-6 in serum of patients with polymyalgia rheumatica and giant cell arteritis. Br J Rheumatol (1990) 29:456-8. doi:10.1093/rheumatology/29.6.456
100. Roche NE, Fulbright JW, Wagner AD, Hunder GG, Goronzy JJ, Weyand CM. Correlation of interleukin-6 production and disease activity in polymyalgia rheumatica and giant cell arteritis. Arthritis Rheum (1993) 36:1286-94. doi:10.1002/art.1780360913
101. Baldini M, Maugeri N, Ramirez GA, Giacomassi C, Castiglioni A, Prieto-González S, et al. Selective up-regulation of the soluble pattern-recognition receptor pentraxin 3 and of vascular endothelial growth factor in giant cell arteritis. Arthritis Rheum (2012) 64:854-65. doi:10.1002/art.33411
102. Wagner AD, Goronzy JJ, Weyand CM. Functional profile of tissue-infiltrating and circulating CD68+ cells in giant cell arteritis. Evidence for two components of the disease. J Clin Invest (1994) 94:1134-40. doi:10.1172/JCI117428
103. Emilie D, Liozon E, Crevon MC, Lavignac C, Portier A, Liozon F, et al. Production of interleukin 6 by granulomas of giant cell arteritis. Hum Immunol (1994) 39:17-24. doi:10.1016/0198-8859(94)90096-5
104. Weyand CM, Wagner AD, Björnsson J, Goronzy JJ. Correlation of the topographical arrangement and the functional pattern of tissue-infiltrating macrophages in giant cell arteritis. J Clin Invest (1996) 98:1642-9. doi:10.1172/JCI118959
105. Ciccia F, Alessandro R, Rizzo A, Raimondo S, Giardina A, Raiata F, et al. IL-33 is overexpressed in the inflamed arteries of patients with giant cell arteritis. Ann Rheum Dis (2013) 72:258-64. doi:10.1136/annrheumdis-2012-201309
106. Kurowska-Stolarska M, Stolarski B, Kewin P, Murphy G, Corrigan CJ, Ying S, et al. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J Immunol (2009) 183:6469-77. doi:10.4049/jimmunol.0901575
107. Ciccia F, Alessandro R, Rizzo A, Principe S, Raiata F, Cavazza A, et al. Expression of interleukin-32 in the inflamed arteries of patients with giant cell arteritis. Arthritis Rheum (2011) 63:2097-104. doi:10.1002/art.30374
108. Espígol-Frigolé G, Corbera-Bellalta M, Planas-Rigol E, Lozano E, Segarra M, García-Martínez A, et al. Increased IL-17A expression in temporal artery lesions is a predictor of sustained response to glucocorticoid treatment in patients with giant-cell arteritis. Ann Rheum Dis (2013) 72:1481-7. doi:10.1136/annrheumdis-2012-201836
109. Samson M, Audia S, Fraszczak J, Trad M, Ornetti P, Lakomy D, et al. Th1 and Th17 lymphocytes expressing CD161 are implicated in giant cell arteritis and polymyalgia rheumatica pathogenesis. Arthritis Rheum (2012) 64:3788-98. doi:10.1002/art.34647
110. Mangan P, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, Elson CO, et al. Transforming growth factor-b induces development of the TH17 lineage. Nature (2006) 441:231-4. doi:10.1038/nature04754
111. Noack M, Miossec P. Th17 and regulatory T cell balance in autoimmune and inflammatory diseases. Autoimmun Rev (2014) 13:668-77. doi:10.1016/j.autrev.2013.12.004
112. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature (2006) 441:235-8. doi:10.1038/nature04753
113. Sonderegger I, Iezzi G, Maier R, Schmitz N, Kurrer M, Kopf M. GM-CSF mediates autoimmunity by enhancing IL-6 - dependent Th17 cell development and survival. J Exp Med (2008) 205:2281-94. doi:10.1084/jem.20071119
114. El-Behi M, Ciric B, Dai H, Yan Y, Cullimore M, Safavi F, et al. The encephalitogenicity of TH17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat Immunol (2011) 12:568-76. doi:10.1038/ni.2031
115. Hoffman GS, Cid MC, Rendt-Zagar KE, Merkel PA, Weyand CM, Stone JH, et al. Infliximab for maintenance of glucocorticosteroid-induced remission of giant cell arteritis: a randomized trial. Ann Intern Med (2007) 146:621-30. doi:10.7326/0003-4819-146-9-200705010-00004
116. Kanzler H, Barrat FJ, Hessel EM, Coffman RL. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat Med (2007) 13:552-9. doi:10.1038/nm1589
117. Ulevitch R. New therapeutic targets revealed through investigations of innate immunity. Crit Care Med (2001) 29:S8-12. doi:10.1097/00003246-200107001-00004
118. Jennette JC, Falk RJ, Bacon PA, Basu N, Cid MC, Ferrario F, et al. 2012 revised international Chapel Hill consensus conference nomenclature of vasculitides. Arthritis Rheum (2013) 65:1-11. doi:10.1002/art.37715
119. Scott D, Watts R. Epidemiology and clinical features of systemic vasculitis. Clin Exp Nephrol (2013) 17:607-10. doi:10.1007/s10157-013-0830-8
120. Hilhorst M, Wilde B, van Paassen P, Winkens B, van Breda Vriesman P, Cohen Tervaert JW, et al. Improved outcome in anti-neutrophil cytoplasmic antibody (ANCA)-associated glomerulonephritis: a 30-year follow-up study. Nephrol Dial Transplant (2013) 28:373-9. doi:10.1093/ndt/gfs428
121. Ntatsaki E, Watts RA, Scott DG. Epidemiology of ANCA-associated vasculitis. Rheum Dis Clin North Am (2010) 36:447-61. doi:10.1016/j.rdc.2010.04.002
122. Harper L. L42. Morbidity in patients with ANCA-associated vasculitis. Presse Med (2013) 42:612-6. doi:10.1016/j.lpm.2013.01.040
123. Holl-Ulrich K. L18. Granuloma formation in granulomatosis with polyangiitis. Presse Med (2013) 42:555-8. doi:10.1016/j.lpm.2013.01.017
124. Csernok E, Ernst M, Schmitt W, Bainton DF, Gross WL. Activated neutrophils express proteinase 3 on their plasma membrane in vitro and in vivo. Clin Exp Immunol (1994) 95:244-50. doi:10.1111/j.1365-2249.1994.tb06518.x
125. Weidner S, Neupert W, Goppelt-Struebe M, Rupprecht HD. Antineutrophil cytoplasmic antibodies induce human monocytes to produce oxygen radicals in vitro. Arthritis Rheum (2001) 44:1698-706. doi:10.1002/1529-0131(200107)44:7<1698::AID-ART294>3.0.CO;2-J
126. Tervaert JW, van der Woude FJ, Fauci AS, Ambrus JL, Velosa J, Keane WF, et al. Association between active Wegener's granulomatosis and anticytoplasmic antibodies. Arch Int Med (1989) 149:2461-5. doi:10.1001/archinte.149.11.2461
127. Hattar K, van Bürck S, Bickenbach A, Grandel U, Maus U, Lohmeyer J, et al. Anti-proteinase 3 antibodies (c-ANCA) prime CD14-dependent leukocyte activation. J Leukoc Biol (2005) 78:992-1000. doi:10.1189/jlb.0902442
128. Rasmussen N, Petersen J. Reactivity of antineutrophil cytoplasmic antibodies with mononuclear phagocytes. J Leukoc Biol (1992) 51:65-8.
129. Falk RJ, Terrell RS, Charles LA, Jennette JC. Anti-neutrophil cytoplasmic autoantibodies induce neutrophils to degranulate and produce oxygen radicals in vitro. Proc Natl Acad Sci U S A (1990) 87:4115-9. doi:10.1073/pnas.87.11.4115
130. Sangaletti S, Tripodo C, Chiodoni C, Guarnotta C, Cappetti B, Casalini P, et al. Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity. Blood (2012) 120:3007-18. doi:10.1182/blood-2012-03-416156
131. Moosig F, Csernok E, Kumanovics G, Gross WL. Opsonization of apoptotic neutrophils by anti-neutrophil cytoplasmic antibodies (ANCA) leads to enhanced uptake by macrophages and increased release of tumour necrosis factor-alpha (TNF-a). Clin Exp Immunol (2000) 122:499-503. doi:10.1046/j.1365-2249.2000.01410.x
132. Rastaldi MP, Ferrario F, Crippa A, Dell'Antonio G, Casartelli D, Grillo C, et al. Glomerular monocyte-macrophage features in ANCA-positive renal vasculitis and cryoglobulinemic nephritis. J Am Soc Nephrol (2000) 11:2036-43.
133. Hewins P, Morgan MD, Holden N, Neil D, Williams JM, Savage CO, et al. IL-18 is upregulated in the kidney and primes neutrophil responsiveness in ANCA-associated vasculitis. Kidney Int (2006) 69:605-15. doi:10.1038/sj.ki.5000167
134. Weidner S, Carl M, Riess R, Rupprecht HD. Histologic analysis of renal leukocyte infiltration in antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheum (2004) 50:3651-7. doi:10.1002/art.20607
135. Wilde B, van Paassen P, Damoiseaux J, Heerings-Rewinkel P, van Rie H, Witzke O, et al. Dendritic cells in renal biopsies of patients with ANCA-associated vasculitis. Nephrol Dial Transplant (2009) 24:2151-6. doi:10.1093/ndt/gfp019
136. Nogueira E, Hamour S, Sawant D, Henderson S, Mansfield N, Chavele KM, et al. Serum IL-17 and IL-23 levels and autoantigen-specific Th17 cells are elevated in patients with ANCA-associated vasculitis. Nephrol Dial Transplant (2010) 25:2209-17. doi:10.1093/ndt/gfp783
137. Grönhagen-Riska C, Teppo AM, Honkanen E, Ikäheimo R. Alpha-1-antitrypsin, CRP and interleukin-6 in ANCA-positive vasculitis. Adv Exp Med Biol (1993) 336:337-40. doi:10.1007/978-1-4757-9182-2_55
138. Wikman A, Fagergren A, Gunnar O, Johansson S, Lundahl J, Jacobson SH. Monocyte activation and relationship to anti-proteinase 3 in acute vasculitis. Nephrol Dial Transplant (2003) 18:1792-9. doi:10.1093/ndt/gfg216
139. Muller Kobold AC, van Wijk RT, Franssen CF, Molema G, Kallenberg CG, Tervaert JW. In vitro up-regulation of E-selectin and induction of interleukin-6 in endothelial cells by autoantibodies in Wegener's granulomatosis and microscopic polyangiitis. Clin Exp Rheumatol (1999) 17:433-40.
140. Noronha IL, Krüger C, Andrassy K, Ritz E, Waldherr R. In situ production of TNF-alpha, IL-1 beta and IL-2R in ANCA-positive glomerulonephritis. Kidney Int (1993) 43:682-92. doi:10.1038/ki.1993.98
141. Schreiber A, Pham CT, Hu Y, Schneider W, Luft FC, Kettritz R. Neutrophil serine proteases promote IL-1b generation and injury in necrotizing crescentic glomerulonephritis. J Am Soc Nephrol (2012) 23:470-82. doi:10.1681/ASN.2010080892
142. Novick D, Rubinstein M, Azam T, Rabinkov A, Dinarello CA, Kim SH. Proteinase 3 is an IL-32 binding protein. Proc Natl Acad Sci U S A (2006) 103:3316-21. doi:10.1073/pnas.0511206103
143. Csernok E, Holle JU, Gross WL. Proteinase 3, protease-activated receptor-2 and interleukin-32: linking innate and autoimmunity in Wegener's granulomatosis. Clin Exp Rheumatol (2008) 26:S112-7.
144. Uehara A, Sato T, Iwashiro A, Yokota S. PR3-ANCA in Wegener's granulomatosis prime human mononuclear cells for enhanced activation via TLRs and NOD1/2. Diagn Pathol (2009) 4:23. doi:10.1186/1746-1596-4-23
145. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cézard JP, Belaiche J, et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature (2001) 411:599-603. doi:10.1038/35079107
146. Newman B, Rubin LA, Siminovitch KA. NOD2/CARD15 gene mutation is not associated with susceptibility to Wegener's granulomatosis. J Rheumatol (2003) 30:305-7.
147. Husmann CA, Holle JU, Moosig F, Mueller S, Wilde B, Cohen Tervaert JW, et al. Genetics of toll like receptor 9 in ANCA associated vasculitides. Ann Rheum Dis (2014) 73:890-6. doi:10.1136/annrheumdis-2012-202803
148. Summers SA, Steinmetz OM, Gan PY, Ooi JD, Odobasic D, Kitching AR, et al. Toll-like receptor 2 induces Th17 myeloperoxidase autoimmunity while Toll-like receptor 9 drives Th1 autoimmunity in murine vasculitis. Arthritis Rheum (2011) 63:1124-35. doi:10.1002/art.30208
149. Stegeman CA, Tervaert JW, Sluiter WJ, Manson WL, de Jong PE, Kallenberg CG. Association of chronic nasal carriage of Staphylococcus aureus and higher relapse rates in Wegener granulomatosis. Ann Intern Med (1994) 120:12-7. doi:10.7326/0003-4819-120-1-199401010-00003
150. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol (2003) 21:335-76. doi:10.1146/annurev.immunol.21.120601.141126
151. Tadema H, Abdulahad WH, Stegeman CA, Kallenberg CG, Heeringa P. Increased expression of Toll-like receptors by monocytes and natural killer cells in ANCA-associated vasculitis. PLoS One (2011) 6:e24315. doi:10.1371/journal.pone.0024315
152. Martorana D, Maritati F, Malerba G, Bonatti F, Alberici F, Oliva E, et al. PTPN22 R620W polymorphism in the ANCA-associated vasculitides. Rheumatology (2012) 51:805-12. doi:10.1093/rheumatology/ker446
153. Nau GJ, Guilfoile P, Chupp GL, Berman JS, Kim SJ, Kornfeld H, et al. A chemoattractant cytokine associated with granulomas in tuberculosis and silicosis. Proc Natl Acad Sci U S A (1997) 94:6414-9. doi:10.1073/pnas.94.12.6414
154. Lorenzen J, Lovric S, Krämer R, Haller H, Haubitz M. Osteopontin in antineutrophil cytoplasmic autoantibody-associated vasculitis: relation to disease activity, organ manifestation and immunosuppressive therapy. Ann Rheum Dis (2009) 69:1169-71. doi:10.1136/ard.2009.113621
155. Hudkins K, Giachelli CM, Eitner F, Couser WG, Johnson RJ, Alpers CE. Osteopontin expression in human crescentic glomerulonephritis. Kidney Int (2000) 57:105-16. doi:10.1046/j.1523-1755.2000.00813.x
156. Christakos S, Dhawan P, Benn B, Porta A, Hediger M, Oh GT, et al. Vitamin D: molecular mechanism of action. Ann N Y Acad Sci (2007) 1116:340-8. doi:10.1196/annals.1402.070
157. Inoue M, Arikawa T, Chen YH, Moriwaki Y, Price M, Brown M, et al. T cells down-regulate macrophage TNF production by IRAK1-mediated IL-10 expression and control innate hyperinflammation. Proc Natl Acad Sci U S A (2014) 111:5295-300. doi:10.1073/pnas.1321427111
158. Laurino S, Chaudhry A, Booth A, Conte G, Jayne D. Prospective study of TNFa blockade with adalimumab in ANCA-associated systemic vasculitis with renal involvement. Nephrol Dial Transplant (2010) 25:3307-14. doi:10.1093/ndt/gfq187
159. Wegener's Granulomatosis Etanercept Trial (WGET) Research Group. Etanercept plus standard therapy for Wegener's granulomatosis. N Engl J Med (2005) 352:351-61. doi:10.1056/NEJMoa041884
160. Jones RB, Tervaert JW, Hauser T, Luqmani R, Morgan MD, Peh CA, et al. Rituximab versus cyclophosphamide in ANCA-associated renal vasculitis. N Engl J Med (2010) 363:211-20. doi:10.1056/NEJMoa0909169
161. Mueller A, Holl-Ulrich K, Gross WL. Granuloma in ANCA-associated vasculitides: another reason to distinguish between syndromes? Curr Rheumatol Rep (2013) 15:376. doi:10.1007/s11926-013-0376-5
162. Godman G, Churg J. Wegener's granulomatosis: pathology and review of the literature. AMA Arch Pathol (1954) 58:533-53.
163. Martinez-Taboada V, Brack A, Hunder GG, Goronzy JJ, Weyand CM. The inflammatory infiltrate in giant cell arteritis selects against B lymphocytes. J Rheumatol (1996) 23:1011-4.
164. Voswinkel J, Assmann G, Held G, Pitann S, Gross WL, Holl-Ulrich K, et al. Single cell analysis of B lymphocytes from Wegener's granulomatosis: B cell receptors display affinity maturation within the granulomatous lesions. Clin Exp Immunol (2008) 154:339-45. doi:10.1111/j.1365-2249.2008.03775.x
165. Voswinkel J, Müller A, Lamprecht P. Is PR3-ANCA formation initiated in Wegener's granulomatosis lesions? Granulomas as potential lymphoid tissue maintaining autoantibody production. Ann N Y Acad Sci (2005) 1051:12-9. doi:10.1196/annals.1361.042
166. Tomasson G, Grayson PC, Mahr AD, Lavalley M, Merkel PA. Value of ANCA measurements during remission to predict a relapse of ANCA-associated vasculitis - a meta-analysis. Rheumatology (2012) 51:100-9. doi:10.1093/rheumatology/ker280
167. Kaiser M, Weyand CM, Björnsson J, Goronzy JJ. Platelet-derived growth factor, intimal hyperplasia, and ischemic complications in giant cell arteritis. Arthritis Rheum (1998) 41:623-33. doi:10.1002/1529-0131(199804)41:4<623::AID-ART9>3.3.CO;2-Y
168. Kaiser M, Younge B, Björnsson J, Goronzy JJ, Weyand CM. Formation of new vasa vasorum in vasculitis. Production of angiogenic cytokines by multinucleated giant cells. Am J Pathol (1999) 155:765-74. doi:10.1016/S0002-9440(10)65175-9