Role of neutrophils in systemic autoimmune diseases

Arthritis Research and Therapy

Volumn 15, Issue 5, 2013, Pages

  Kaplan, Mariana J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHELICIDIN; AUTOANTIBODY;

AEROBIC METABOLISM; ANCA ASSOCIATED VASCULITIS; CELL DEATH; GRANULOCYTE FUNCTION; HUMAN; LEUKOCYTE ACTIVATION; NEUTROPENIA; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; REVIEW; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; UPREGULATION; APOPTOSIS; AUTOIMMUNITY; IMMUNOLOGY;

ANTI-NEUTROPHIL CYTOPLASMIC ANTIBODY-ASSOCIATED VASCULITIS; APOPTOSIS; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; AUTOIMMUNITY; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; NEUTROPHILS;

EID: 84887557925     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4325     Document Type: Review

References (118)

1. Kessenbrock K, Frohlich L, Sixt M, Lammermann T, Pfister H, Bateman A, Belaaouaj A, Ring J, Ollert M, Fassler R, Jenne DE. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J Clin Invest 2008, 118:2438-2447. 2430496, 18568075.
2. Borregaard N, Sorensen OE, Theilgaard-Monch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol 2007, 28:340-345. 10.1016/j.it.2007.06.002, 17627888.
3. Huber AR, Kunkel SL, Todd RF, Weiss SJ. Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science 1991, 254:99-102. 10.1126/science.1718038, 1718038.
4. Borregaard N. Neutrophils, from marrow to microbes. Immunity 2010, 33:657-670. 10.1016/j.immuni.2010.11.011, 21094463.
5. Jaeger BN, Donadieu J, Cognet C, Bernat C, Ordonez-Rueda D, Barlogis V, Mahlaoui N, Fenis A, Narni-Mancinelli E, Beaupain B, Bellanné-Chantelot C, Bajénoff M, Malissen B, Malissen M, Vivier E, Uqolini S. Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J Exp Med 2012, 209:565-580. 10.1084/jem.20111908, 3302230, 22393124.
6. Micheletti A, Costantini C, Calzetti F, Camuesco D, Costa S, Tamassia N, Cassatella MA. Neutrophils promote 6-sulfo LacNAc+ dendritic cell (slanDC) survival. J Leukoc Biol 2013, [Epub ahead of print].
7. Park SJ, Burdick MD, Mehrad B. Neutrophils mediate maturation and efflux of lung dendritic cells in response to Aspergillus fumigatus germ tubes. Infect Immun 2012, 80:1759-1765. 10.1128/IAI.00097-12, 3347458, 22392929.
8. Abi Abdallah DS, Egan CE, Butcher BA, Denkers EY. Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int Immunol 2011, 23:317-326. 10.1093/intimm/dxr007, 3082529, 21422151.
9. Puga I, Cols M, Barra CM, He B, Cassis L, Gentile M, Comerma L, Chorny A, Shan M, Xu W, Magri G, Knowles DM, Tam W, Chiu A, Bussel JB, Serrano S, Lorente JA, Bellosillo B, Lloreta J, Juanpere N, Alameda F, Baró T, de Heredia CD, Torán N, Català A, Torrebadell M, Fortuny C, Cusí V, Carreras C, Diaz GA, et al. B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat Immunol 2012, 13:170-180.
10. Derycke L, Zhang N, Holtappels G, Dutre T, Bachert C. IL-17A as a regulator of neutrophil survival in nasal polyp disease of patients with and without cystic fibrosis. J Cyst Fibros 2012, 11:193-200. 10.1016/j.jcf.2011.11.007, 22178076.
11. Kinsey GR, Sharma R, Huang L, Li L, Vergis AL, Ye H, Ju ST, Okusa MD. Regulatory T cells suppress innate immunity in kidney ischemia-reperfusion injury. J Am Soc Nephrol 2009, 20:1744-1753. 10.1681/ASN.2008111160, 2723989, 19497969.
12. Schuster S, Hurrell B, Tacchini-Cottier F. Crosstalk between neutrophils and dendritic cells: a context-dependent process. J Leukoc Biol 2012, [Epub ahead of print].
13. Kasten KR, Muenzer JT, Caldwell CC. Neutrophils are significant producers of IL-10 during sepsis. Biochem Biophys Res Commun 2010, 393:28-31. 10.1016/j.bbrc.2010.01.066, 2830356, 20097159.
14. Ren Y, Savill J. Proinflammatory cytokines potentiate thrombospondin-mediated phagocytosis of neutrophils undergoing apoptosis. J Immunol 1995, 154:2366-2374.
15. Prince LR, Whyte MK, Sabroe I, Parker LC. The role of TLRs in neutrophil activation. Curr Opin Pharmacol 2011, 11:397-403. 10.1016/j.coph.2011.06.007, 21741310.
16. Yang D, de la Rosa G, Tewary P, Oppenheim JJ. Alarmins link neutrophils and dendritic cells. Trends Immunol 2009, 30:531-537. 10.1016/j.it.2009.07.004, 2767430, 19699678.
17. Shirafuji N, Matsuda S, Ogura H, Tani K, Kodo H, Ozawa K, Nagata S, Asano S, Takaku F. Granulocyte colony-stimulating factor stimulates human mature neutrophilic granulocytes to produce interferon-alpha. Blood 1990, 75:17-19.
18. Tamassia N, Le Moigne V, Rossato M, Donini M, McCartney S, Calzetti F, Colonna M, Bazzoni F, Cassatella MA. Activation of an immunoregulatory and antiviral gene expression program in poly(I:C)-transfected human neutrophils. J Immunol 2008, 181:6563-6573.
19. Tamassia N, Cassatella MA. Cytoplasmic receptors recognizing nucleic acids and mediating immune functions in neutrophils. Curr Opin Pharmacol 2013, 13:547-554. 10.1016/j.coph.2013.05.003, 23725881.
20. Nordenfelt P, Tapper H. Phagosome dynamics during phagocytosis by neutrophils. J Leukoc Biol 2011, 90:271-284. 10.1189/jlb.0810457, 21504950.
21. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535. 10.1126/science.1092385, 15001782.
22. Brinkmann V, Zychlinsky A. Neutrophil extracellular traps: is immunity the second function of chromatin?. J Cell Biol 2012, 198:773-783. 10.1083/jcb.201203170, 3432757, 22945932.
23. Remijsen Q, Kuijpers TW, Wirawan E, Lippens S, Vandenabeele P, Vanden Berghe T. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ 2011, 18:581-588. 10.1038/cdd.2011.1, 3131909, 21293492.
24. Kaplan MJ, Radic M. Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol 2012, 189:2689-2695. 10.4049/jimmunol.1201719, 3439169, 22956760.
25. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007, 176:231-241. 10.1083/jcb.200606027, 2063942, 17210947.
26. Hemmers S, Teijaro JR, Arandjelovic S, Mowen KA. PAD4-mediated neutrophil extracellular trap formation is not required for immunity against influenza infection. PLoS One 2011, 6:e22043. 10.1371/journal.pone.0022043, 3133614, 21779371.
27. Li P, Li M, Lindberg MR, Kennett MJ, Xiong N, Wang Y. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med 2010, 207:1853-1862. 10.1084/jem.20100239, 2931169, 20733033.
28. Wang Y, Li M, Stadler S, Correll S, Li P, Wang D, Hayama R, Leonelli L, Han H, Grigoryev SA, Allis CD, Coonrod SA. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 2009, 184:205-213. 10.1083/jcb.200806072, 2654299, 19153223.
29. Neeli I, Khan SN, Radic M. Histone deimination as a response to inflammatory stimuli in neutrophils. J Immunol 2008, 180:1895-1902.
30. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity 2004, 21:467-476. 10.1016/j.immuni.2004.08.018, 15485625.
31. Scapini P, Bazzoni F, Cassatella MA. Regulation of B-cell-activating factor (BAFF)/B lymphocyte stimulator (BLyS) expression in human neutrophils. Immunol Lett 2008, 116:1-6. 10.1016/j.imlet.2007.11.009, 18155301.
32. El Kebir D, Filep JG. Modulation of neutrophil apoptosis and the resolution of inflammation through beta2 integrins. Front Immunol 2013, 4:60. 3589696, 23508943.
33. Pillay J, den Braber I, Vrisekoop N, Kwast LM, de Boer RJ, Borghans JA, Tesselaar K, Koenderman L. In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 2010, 116:625-627. 10.1182/blood-2010-01-259028, 20410504.
34. Franssen CF, Huitema MG, Muller Kobold AC, Oost-Kort WW, Limburg PC, Tiebosch A, Stegeman CA, Kallenberg CG, Tervaert JW. In vitro neutrophil activation by antibodies to proteinase 3 and myeloperoxidase from patients with crescentic glomerulonephritis. J Am Soc Nephrol 1999, 10:1506-1515.
35. Witko-Sarsat V, Lesavre P, Lopez S, Bessou G, Hieblot C, Prum B, Noel LH, Guillevin L, Ravaud P, Sermet-Gaudelus I, Timsit J, Grünfeld JP, Halbwachs-Mecarelli L. A large subset of neutrophils expressing membrane proteinase 3 is a risk factor for vasculitis and rheumatoid arthritis. J Am Soc Nephrol 1999, 10:1224-1233.
36. Charles LA, Caldas ML, Falk RJ, Terrell RS, Jennette JC. Antibodies against granule proteins activate neutrophils in vitro. J Leukoc Biol 1991, 50:539-546.
37. Yang JJ, Preston GA, Pendergraft WF, Segelmark M, Heeringa P, Hogan SL, Jennette JC, Falk RJ. Internalization of proteinase 3 is concomitant with endothelial cell apoptosis and internalization of myeloperoxidase with generation of intracellular oxidants. Am J Pathol 2001, 158:581-592. 10.1016/S0002-9440(10)64000-X, 1850298, 11159195.
38. Porges AJ, Redecha PB, Kimberly WT, Csernok E, Gross WL, Kimberly RP. Anti-neutrophil cytoplasmic antibodies engage and activate human neutrophils via Fc gamma RIIa. J Immunol 1994, 153:1271-1280.
39. Kocher M, Edberg JC, Fleit HB, Kimberly RP. Antineutrophil cytoplasmic antibodies preferentially engage Fc gammaRIIIb on human neutrophils. J Immunol 1998, 161:6909-6914.
40. Williams JM, Ben-Smith A, Hewins P, Dove SK, Hughes P, McEwan R, Wakelam MJ, Savage CO. Activation of the G(i) heterotrimeric G protein by ANCA IgG F(ab')2 fragments is necessary but not sufficient to stimulate the recruitment of those downstream mediators used by intact ANCA IgG. J Am Soc Nephrol 2003, 14:661-669. 10.1097/01.ASN.0000050223.34749.F4, 12595502.
41. Xiao H, Heeringa P, Hu P, Liu Z, Zhao M, Aratani Y, Maeda N, Falk RJ, Jennette JC. Antineutrophil cytoplasmic autoantibodies specific for myeloperoxidase cause glomerulonephritis and vasculitis in mice. J Clin Invest 2002, 110:955-963. 151154, 12370273.
42. Schreiber A, Xiao H, Falk RJ, Jennette JC. Bone marrow-derived cells are sufficient and necessary targets to mediate glomerulonephritis and vasculitis induced by anti-myeloperoxidase antibodies. J Am Soc Nephrol 2006, 17:3355-3364. 10.1681/ASN.2006070718, 17108314.
43. Pfister H, Ollert M, Frohlich LF, Quintanilla-Martinez L, Colby TV, Specks U, Jenne DE. Antineutrophil cytoplasmic autoantibodies against the murine homolog of proteinase 3 (Wegener autoantigen) are pathogenic in vivo. Blood 2004, 104:1411-1418. 10.1182/blood-2004-01-0267, 15150076.
44. Kain R, Matsui K, Exner M, Binder S, Schaffner G, Sommer EM, Kerjaschki D. A novel class of autoantigens of anti-neutrophil cytoplasmic antibodies in necrotizing and crescentic glomerulonephritis: the lysosomal membrane glycoprotein h-lamp-2 in neutrophil granulocytes and a related membrane protein in glomerular endothelial cells. J Exp Med 1995, 181:585-597. 10.1084/jem.181.2.585, 2191894, 7836914.
45. Kain R, Exner M, Brandes R, Ziebermayr R, Cunningham D, Alderson CA, Davidovits A, Raab I, Jahn R, Ashour O, Spitzauer S, Sunder-Plassmann G, Fukuda M, Klemm P, Rees AJ, Kerjaschki D. Molecular mimicry in pauci-immune focal necrotizing glomerulonephritis. Nat Med 2008, 14:1088-1096. 10.1038/nm.1874, 2751601, 18836458.
46. Gabillet J, Millet A, Pederzoli-Ribeil M, Tacnet-Delorme P, Guillevin L, Mouthon L, Frachet P, Witko-Sarsat V. Proteinase 3, the autoantigen in granulomatosis with polyangiitis, associates with calreticulin on apoptotic neutrophils, impairs macrophage phagocytosis, and promotes inflammation. J Immunol 2012, 189:2574-2583. 10.4049/jimmunol.1200600, 22844112.
47. Hong Y, Eleftheriou D, Hussain AA, Price-Kuehne FE, Savage CO, Jayne D, Little MA, Salama AD, Klein NJ, Brogan PA. Anti-neutrophil cytoplasmic antibodies stimulate release of neutrophil microparticles. J Am Soc Nephrol 2012, 23:49-62. 10.1681/ASN.2011030298, 3269928, 22052057.
48. Holden NJ, Williams JM, Morgan MD, Challa A, Gordon J, Pepper RJ, Salama AD, Harper L, Savage CO. ANCA-stimulated neutrophils release BLyS and promote B cell survival: a clinically relevant cellular process. Ann Rheum Dis 2011, 70:2229-2233. 10.1136/ard.2011.153890, 21859691.
49. Kessenbrock K, Krumbholz M, Schonermarck U, Back W, Gross WL, Werb Z, Grone HJ, Brinkmann V, Jenne DE. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009, 15:623-625. 10.1038/nm.1959, 2760083, 19448636.
50. Nakazawa D, Tomaru U, Suzuki A, Masuda S, Hasegawa R, Kobayashi T, Nishio S, Kasahara M, Ishizu A. Abnormal conformation and impaired degradation of propylthiouracil-induced neutrophil extracellular traps: implications of disordered neutrophil extracellular traps in a rat model of myeloperoxidase antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheum 2012, 64:3779-3787. 10.1002/art.34619, 22777766.
51. Sangaletti S, Tripodo C, Chiodoni C, Guarnotta C, Cappetti B, Casalini P, Piconese S, Parenza M, Guiducci C, Vitali C, Colombo MP. Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity. Blood 2012, 120:3007-3018. 10.1182/blood-2012-03-416156, 22932797.
52. Brandt L, Hedberg H. Impaired phagocytosis by peripheral blood granulocytes in systemic lupus erythematosus. Scand J Haematol 1969, 6:348-353.
53. Abramson SB, Given WP, Edelson HS, Weissmann G. Neutrophil aggregation induced by sera from patients with active systemic lupus erythematosus. Arthritis Rheum 1983, 26:630-636. 10.1002/art.1780260509, 6847725.
54. Ronnefarth VM, Erbacher AI, Lamkemeyer T, Madlung J, Nordheim A, Rammensee HG, Decker P. TLR2/TLR4-independent neutrophil activation and recruitment upon endocytosis of nucleosomes reveals a new pathway of innate immunity in systemic lupus erythematosus. J Immunol 2006, 177:7740-7749.
55. Alves CM, Marzocchi-Machado CM, Louzada-Junior P, Azzolini AE, Polizello AC, de Carvalho IF, Lucisano-Valim YM. Superoxide anion production by neutrophils is associated with prevalent clinical manifestations in systemic lupus erythematosus. Clin Rheumatol 2008, 27:701-708. 10.1007/s10067-007-0768-x, 17955277.
56. Vordenbaumen S, Fischer-Betz R, Timm D, Sander O, Chehab G, Richter J, Bleck E, Schneider M. Elevated levels of human beta-defensin 2 and human neutrophil peptides in systemic lupus erythematosus. Lupus 2010, 19:1648-1653. 10.1177/0961203310377089, 20724351.
57. Armstrong DJ, Crockard AD, Wisdom BG, Whitehead EM, Bell AL. Accelerated apoptosis in SLE neutrophils cultured with anti-dsDNA antibody isolated from SLE patient serum: a pilot study. Rheumatol Int 2006, 27:153-156. 10.1007/s00296-006-0219-z, 17009017.
58. Donnelly S, Roake W, Brown S, Young P, Naik H, Wordsworth P, Isenberg DA, Reid KB, Eggleton P. Impaired recognition of apoptotic neutrophils by the C1q/calreticulin and CD91 pathway in systemic lupus erythematosus. Arthritis Rheum 2006, 54:1543-1556. 10.1002/art.21783, 16645988.
59. Schorn C, Janko C, Krenn V, Zhao Y, Munoz LE, Schett G, Herrmann M. Bonding the foe - NETting neutrophils immobilize the pro-inflammatory monosodium urate crystals. Front Immunol 2012, 3:376. 3517988, 23233855.
60. Knight JS, Kaplan MJ. Lupus neutrophils: 'NET' gain in understanding lupus pathogenesis. Curr Opin Rheumatol 2012, 24:441-450. 10.1097/BOR.0b013e3283546703, 22617827.
61. Kaplan MJ. Neutrophils in the pathogenesis and manifestations of SLE. Nat Rev Rheumatol 2011, 7:691-699. 10.1038/nrrheum.2011.132, 3243068, 21947176.
62. Bennett L, Palucka AK, Arce E, Cantrell V, Borvak J, Banchereau J, Pascual V. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med 2003, 197:711-723. 10.1084/jem.20021553, 2193846, 12642603.
63. Denny MF, Yalavarthi S, Zhao W, Thacker SG, Anderson M, Sandy AR, McCune WJ, Kaplan MJ. A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J Immunol 2010, 184:3284-3297. 10.4049/jimmunol.0902199, 2929645, 20164424.
64. Carmona-Rivera C, Kaplan MJ. Low-density granulocytes: a distinct class of neutrophils in systemic autoimmunity. Semin Immunopathol 2013, 35:455-463. 10.1007/s00281-013-0375-7, 23553215.
65. Villanueva E, Yalavarthi S, Berthier CC, Hodgin JB, Khandpur R, Lin AM, Rubin CJ, Zhao W, Olsen SH, Klinker M, Shealy D, Denny MF, Plumas J, Chaperot L, Kretzler M, Bruce AT, Kaplan MJ. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol 2011, 187:538-552. 10.4049/jimmunol.1100450, 3119769, 21613614.
66. Nakou M, Bertsias G, Stagakis I, Centola M, Tassiulas I, Hatziapostolou M, Kritikos I, Goulielmos G, Boumpas DT, Iliopoulos D. Gene network analysis of bone marrow mononuclear cells reveals activation of multiple kinase pathways in human systemic lupus erythematosus. PLoS One 2010, 5:e13351. 10.1371/journal.pone.0013351, 2954787, 20976278.
67. Garcia-Romo GS, Caielli S, Vega B, Connolly J, Allantaz F, Xu Z, Punaro M, Baisch J, Guiducci C, Coffman RL, Barrat FJ, Banchereau J, Pascual V. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011, 3:73ra20. 10.1126/scitranslmed.3001201, 3143837, 21389264.
68. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, Herrmann M, Voll RE, Zychlinsky A. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci U S A 2010, 107:9813-9818. 10.1073/pnas.0909927107, 2906830, 20439745.
69. Lande R, Ganguly D, Facchinetti V, Frasca L, Conrad C, Gregorio J, Meller S, Chamilos G, Sebasigari R, Riccieri V, Bassett R, Amuro H, Fukuhara S, Ito T, Liu YJ, Gilliet M. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med 2011, 3:73ra19. 10.1126/scitranslmed.3001180, 3399524, 21389263.
70. Leffler J, Martin M, Gullstrand B, Tyden H, Lood C, Truedsson L, Bengtsson AA, Blom AM. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol 2012, 188:3522-3531. 10.4049/jimmunol.1102404, 22345666.
71. Kahlenberg JM, Carmona-Rivera C, Smith CK, Kaplan MJ. Neutrophil extracellular trap-associated protein activation of the NLRP3 inflammasome is enhanced in lupus macrophages. J Immunol 2013, 190:1217-1226. 10.4049/jimmunol.1202388, 23267025.
72. Liu CL, Tangsombatvisit S, Rosenberg JM, Mandelbaum G, Gillespie EC, Gozani OP, Alizadeh AA, Utz PJ. Specific post-translational histone modifications of neutrophil extracellular traps as immunogens and potential targets of lupus autoantibodies. Arthritis Res Ther 2012, 14:R25. 10.1186/ar3707, 3392818, 22300536.
73. Campbell AM, Kashgarian M, Shlomchik MJ. NADPH oxidase inhibits the pathogenesis of systemic lupus erythematosus. Sci Transl Med 2012, 4:157ra141. 10.1126/scitranslmed.3004801, 23100627.
74. Grimm MJ, Vethanayagam RR, Almyroudis NG, Dennis CG, Khan AN, D'Auria AC, Singel KL, Davidson BA, Knight PR, Blackwell TS, Hohl TM, Mansour MK, Vyas JM, Röhm M, Urban CF, Kelkka T, Holmdahl R, Segal BH. Monocyte- and macrophage-targeted NADPH oxidase mediates antifungal host defense and regulation of acute inflammation in mice. J Immunol 2013, 190:4175-4184. 10.4049/jimmunol.1202800, 23509361.
75. Meissner F, Seger RA, Moshous D, Fischer A, Reichenbach J, Zychlinsky A. Inflammasome activation in NADPH oxidase defective mononuclear phagocytes from patients with chronic granulomatous disease. Blood 2010, 116:1570-1573. 10.1182/blood-2010-01-264218, 2938844, 20495074.
76. Pilsczek FH, Salina D, Poon KK, Fahey C, Yipp BG, Sibley CD, Robbins SM, Green FH, Surette MG, Sugai M, Bowden MG, Hussain M, Zhang K, Kubes P. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 2010, 185:7413-7425. 10.4049/jimmunol.1000675, 21098229.
77. Chow OA, von Kockritz-Blickwede M, Bright AT, Hensler ME, Zinkernagel AS, Cogen AL, Gallo RL, Monestier M, Wang Y, Glass CK, Nizet V. Statins enhance formation of phagocyte extracellular traps. Cell Host Microbe 2010, 8:445-454. 10.1016/j.chom.2010.10.005, 3008410, 21075355.
78. Hoffmann MH, Bruns H, Backdahl L, Neregard P, Niederreiter B, Herrmann M, Catrina AI, Agerberth B, Holmdahl R. The cathelicidins LL-37 and rCRAMP are associated with pathogenic events of arthritis in humans and rats. Ann Rheum Dis 2013, 72:1239-1248. 10.1136/annrheumdis-2012-202218, 23172753.
79. Knight JS, Zhao W, Luo W, Subramanian V, O'Dell AA, Yalavarthi S, Hodgin JB, Eitzman DT, Thompson PR, Kaplan MJ. Peptidylarginine deiminase inhibition is immunomodulatory and vasculoprotective in murine lupus. J Clin Invest 2013, 123:2981-2993. 10.1172/JCI67390, 3696545, 23722903.
80. Mehrad B, Park SJ, Akangire G, Standiford TJ, Wu T, Zhu J, Mohan C. The lupus-susceptibility locus, Sle3, mediates enhanced resistance to bacterial infections. J Immunol 2006, 176:3233-3239.
81. den Broeder AA, Wanten GJ, Oyen WJ, Naber T, van Riel PL, Barrera P. Neutrophil migration and production of reactive oxygen species during treatment with a fully human anti-tumor necrosis factor-alpha monoclonal antibody in patients with rheumatoid arthritis. J Rheumatol 2003, 30:232-237.
82. Dularay B, Badesha JS, Dieppe PA, Elson CJ. Oxidative response of polymorphonuclear leucocytes to synovial fluids from patients with rheumatoid arthritis. Ann Rheum Dis 1990, 49:661-664. 10.1136/ard.49.9.661, 1004198, 2173500.
83. Dularay B, Elson CJ, Dieppe PA. Enhanced oxidative response of polymorphonuclear leukocytes from synovial fluids of patients with rheumatoid arthritis. Autoimmunity 1988, 1:159-169.
84. Kitsis E, Weissmann G. The role of the neutrophil in rheumatoid arthritis. Clin Orthop Relat Res 1991, 265:63-72.
85. Pillinger MH, Abramson SB. The neutrophil in rheumatoid arthritis. Rheum Dis Clin North Am 1995, 21:691-714.
86. Barnhart MI, Riddle JM, Bluhm GB. Immunocytology in arthritic joints. Ann Rheum Dis 1967, 26:281-296. 10.1136/ard.26.4.281, 1031061, 4952798.
87. Belcher C, Doherty M, Crouch SP. Synovial fluid neutrophil function in RA: the effect of pregnancy associated proteins. Ann Rheum Dis 2002, 61:379-380. 10.1136/ard.61.4.379, 1754051, 11874852.
88. Hughes JR, Erhardt CC, Clement M. Neutrophilic dermatosis in association with rheumatoid arthritis. Clin Exp Dermatol 1995, 20:168-170. 10.1111/j.1365-2230.1995.tb02676.x, 8565258.
89. Ichikawa MM, Murata Y, Higaki Y, Kawashima M, Furuya T, Saito T. Rheumatoid neutrophilic dermatitis. Eur J Dermatol 1998, 8:347-349.
90. Cines DB, Passero F, Guerry D, Bina M, Dusak B, Schreiber AD. Granulocyte-associated IgG in neutropenic disorders. Blood 1982, 59:124-132.
91. Coremans IE, Hagen EC, van der Voort EA, van der Woude FJ, Daha MR, Breedveld FC. Autoantibodies to neutrophil cytoplasmic enzymes in Felty's syndrome. Clin Exp Rheumatol 1993, 11:255-262.
92. Lassoued S, Sixou L, Oksman F, Pages M, Fournie A. Antineutrophil cytoplasmic antibodies and antibodies to myeloperoxidase in rheumatoid arthritis. Arthritis Rheum 1991, 34:1069-1070.
93. Wipke BT, Allen PM. Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol 2001, 167:1601-1608.
94. Gal I, Bajnok E, Szanto S, Sarraj B, Glant TT, Mikecz K. Visualization and in situ analysis of leukocyte trafficking into the ankle joint in a systemic murine model of rheumatoid arthritis. Arthritis Rheum 2005, 52:3269-3278. 10.1002/art.21532, 16206283.
95. Griffiths RJ, Pettipher ER, Koch K, Farrell CA, Breslow R, Conklyn MJ, Smith MA, Hackman BC, Wimberly DJ, Milici AJ, Scampoli DN, Cheng JB, Pillar JS, Pazoles CJ, Doherty NS, Melvin LS, Reiter LA, Biggars MS, Falkner FC, Mitchell DY, Liston TE, Showell HJ. Leukotriene B4 plays a critical role in the progression of collagen-induced arthritis. Proc Natl Acad Sci U S A 1995, 92:517-521. 10.1073/pnas.92.2.517, 42772, 7831322.
96. Matsubara S, Yamamoto T, Tsuruta T, Takagi K, Kambara T. Complement C4-derived monocyte-directed chemotaxis-inhibitory factor. A molecular mechanism to cause polymorphonuclear leukocyte-predominant infiltration in rheumatoid arthritis synovial cavities. Am J Pathol 1991, 138:1279-1291. 1886006, 2024711.
97. Brennan FM, Zachariae CO, Chantry D, Larsen CG, Turner M, Maini RN, Matsushima K, Feldmann M. Detection of interleukin 8 biological activity in synovial fluids from patients with rheumatoid arthritis and production of interleukin 8 mRNA by isolated synovial cells. Eur J Immunol 1990, 20:2141-2144. 10.1002/eji.1830200938, 2209707.
98. Sadik CD, Kim ND, Iwakura Y, Luster AD. Neutrophils orchestrate their own recruitment in murine arthritis through C5aR and FcgammaR signaling. Proc Natl Acad Sci U S A 2012, 109:E3177-E3185. 10.1073/pnas.1213797109, 3503206, 23112187.
99. Eyles JL, Hickey MJ, Norman MU, Croker BA, Roberts AW, Drake SF, James WG, Metcalf D, Campbell IK, Wicks IP. A key role for G-CSF-induced neutrophil production and trafficking during inflammatory arthritis. Blood 2008, 112:5193-5201. 10.1182/blood-2008-02-139535, 18824600.
100. Cook AD, Turner AL, Braine EL, Pobjoy J, Lenzo JC, Hamilton JA. Regulation of systemic and local myeloid cell subpopulations by bone marrow cell-derived granulocyte-macrophage colony-stimulating factor in experimental inflammatory arthritis. Arthritis Rheum 2011, 63:2340-2351. 10.1002/art.30354, 21809323.
101. Cascão R, Moura RA, Perpétuo I, Canhão H, Vieira-Sousa E, Mourão AF, Rodrigues AM, Polido-Pereira J, Queiroz MV, Rosário HS, Souto-Carneiro MM, Graca L, Fonseca JE. Identification of a cytokine network sustaining neutrophil and Th17 activation in untreated early rheumatoid arthritis. Arthritis Res Ther 2010, 12:R196. 10.1186/ar3168, 2991033, 20961415.
102. Chen M, Lam BK, Luster AD, Zarini S, Murphy RC, Bair AM, Soberman RJ, Lee DM. Joint tissues amplify inflammation and alter their invasive behavior via leukotriene B4 in experimental inflammatory arthritis. J Immunol 2010, 185:5503-5511. 10.4049/jimmunol.1001258, 3690310, 20876351.
103. Vossenaar ER, Nijenhuis S, Helsen MM, van der Heijden A, Senshu T, van den Berg WB, van Venrooij WJ, Joosten LA. Citrullination of synovial proteins in murine models of rheumatoid arthritis. Arthritis Rheum 2003, 48:2489-2500. 10.1002/art.11229, 13130468.
104. Caccavo D, Garzia P, Sebastiani GD, Ferri GM, Galluzzo S, Vadacca M, Rigon A, Afeltra A, Amoroso A. Expression of lactoferrin on neutrophil granulocytes from synovial fluid and peripheral blood of patients with rheumatoid arthritis. J Rheumatol 2003, 30:220-224.
105. Corberand J, Amigues H, de Larrard B, Pradere J. Neutrophil function in rheumatoid arthritis. Scand J Rheumatol 1977, 6:49-52.
106. Chatham WW, Heck LW, Blackburn WD. Lysis of fibrillar collagen by neutrophils in synovial fluid. A role for surface-bound immunoglobulins. Arthritis Rheum 1990, 33:1333-1339. 10.1002/art.1780330905, 2169747.
107. Emery P, Lopez AF, Burns GF, Vadas MA. Synovial fluid neutrophils of patients with rheumatoid arthritis have membrane antigen changes that reflect activation. Ann Rheum Dis 1988, 47:34-39. 10.1136/ard.47.1.34, 1003440, 3278695.
108. Mohr W, Wessinghage D. The relationship between polymorphonuclear granulocytes and cartilage destruction in rheumatoid arthritis. Z Rheumatol 1978, 37:81-86.
109. Cross A, Barnes T, Bucknall RC, Edwards SW, Moots RJ. Neutrophil apoptosis in rheumatoid arthritis is regulated by local oxygen tensions within joints. J Leukoc Biol 2006, 80:521-528. 10.1189/jlb.0306178, 16793915.
110. Chakravarti A, Raquil MA, Tessier P, Poubelle PE. Surface RANKL of Toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood 2009, 114:1633-1644. 10.1182/blood-2008-09-178301, 19546479.
111. Poubelle PE, Chakravarti A, Fernandes MJ, Doiron K, Marceau AA. Differential expression of RANK, RANK-L, and osteoprotegerin by synovial fluid neutrophils from patients with rheumatoid arthritis and by healthy human blood neutrophils. Arthritis Res Ther 2007, 9:R25. 10.1186/ar2137, 1906801, 17341304.
112. Dominical VM, Bertolo MB, Almeida CB, Garrido VT, Miguel LI, Costa FF, Conran N. Neutrophils of rheumatoid arthritis patients on anti-TNF-alpha therapy and in disease remission present reduced adhesive functions in association with decreased circulating neutrophil-attractant chemokine levels. Scand J Immunol 2011, 73:309-318. 10.1111/j.1365-3083.2011.02503.x, 21208248.
113. Khandpur R, Carmona-Rivera C, Vivekanandan-Giri A, Gizinski A, Yalavarthi S, Knight JS, Friday S, Li S, Patel RM, Subramanian V, Thompson P, Chen P, Fox DA, Pennathur S, Kaplan MJ. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med 2013, 5:178ra140.
114. Cesaro A, Anceriz N, Plante A, Page N, Tardif MR, Tessier PA. An inflammation loop orchestrated by S100A9 and calprotectin is critical for development of arthritis. PLoS One 2012, 7:e45478. 10.1371/journal.pone.0045478, 3445527, 23029038.
115. Turesson C, Mathsson L, Jacobsson LT, Sturfelt G, Ronnelid J. Antibodies to modified citrullinated vimentin are associated with severe extra-articular manifestations in rheumatoid arthritis. Ann Rheum Dis 2013, [Epub ahead of print].
116. Willis VC, Gizinski AM, Banda NK, Causey CP, Knuckley B, Cordova KN, Luo Y, Levitt B, Glogowska M, Chandra P, Kulik L, Robinson WH, Arend WP, Thompson PR, Holers VM. N-alpha-benzoyl-N5-(2-chloro-1-iminoethyl)-L-ornithine amide, a protein arginine deiminase inhibitor, reduces the severity of murine collagen-induced arthritis. J Immunol 2011, 186:4396-4404. 10.4049/jimmunol.1001620, 3085980, 21346230.
117. Rohrbach AS, Hemmers S, Arandjelovic S, Corr M, Mowen KA. PAD4 is not essential for disease in the K/BxN murine autoantibody-mediated model of arthritis. Arthritis Res Ther 2012, 14:R104. 10.1186/ar3829, 3446481, 22551352.
118. Dwivedi N, Upadhyay J, Neeli I, Khan S, Pattanaik D, Myers L, Kirou KA, Hellmich B, Knuckley B, Thompson PR, Crow MK, Mikuls TR, Csernok E, Radic M. Felty's syndrome autoantibodies bind to deiminated histones and neutrophil extracellular chromatin traps. Arthritis Rheum 2012, 64:982-992. 10.1002/art.33432, 22034172.