Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus

Journal of Immunology

Volumn 187, Issue 1, 2011, Pages 538-552

  Villanueva, Eneida ^a   Yalavarthi, Srilakshmi ^a   Berthier, Celine C ^a   Hodgin, Jeffrey B ^a   Khandpur, Ritika ^a   Lin, Andrew M ^a   Rubin, Cory J ^a   Zhao, Wenpu ^a   Olsen, Stephen H ^a   Klinker, Matthew ^a   Shealy, David ^b   Denny, Michael F ^a,f   Plumas, Joel ^c,d,e   Chaperot, Laurence ^c,d,e   Kretzler, Matthias ^a   Bruce, Allen T ^a   Kaplan, Mariana J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b CENTOCOR INC   (United States)

^c UNIV GRENOBLE ALPES   (France)

^d INSERM   (France)

^e ETABLISSEMENT FRANÇAIS DU SANG   (France)

^f TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DOUBLE STRANDED DNA; DOUBLE STRANDED DNA ANTIBODY; MESSENGER RNA;

ANTIBODY BLOOD LEVEL; ARTICLE; AUTOIMMUNITY; CELL DENSITY; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; DNA MICROARRAY; ENDOTHELIAL DYSFUNCTION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GRANULOCYTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPATHOGENESIS; IMMUNOSTIMULATION; LOW DENSITY GRANULOCYTE; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL EXTRACELLULAR TRAP; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS;

EID: 79960392810     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100450     Document Type: Article

References (66)

1. Denny, M. F., S. Yalavarthi, W. Zhao, S. G. Thacker, M. Anderson, A. R. Sandy, W. J. McCune, and M. J. Kaplan. 2010. A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J. Immunol. 184: 3284-3297.
2. Hakkim, A., B. G. Fürnrohr, K. Amann, B. Laube, U. A. Abed, V. Brinkmann, M. Herrmann, R. E. Voll, and A. Zychlinsky. 2010. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc. Natl. Acad. Sci. USA 107: 9813-9818.
3. Bennett, L., A. K. Palucka, E. Arce, V. Cantrell, J. Borvak, J. Banchereau, and V. Pascual. 2003. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med. 197: 711-723.
4. Hacbarth, E., and A. Kajdacsy-Balla. 1986. Low density neutrophils in patients with systemic lupus erythematosus, rheumatoid arthritis, and acute rheumatic fever. Arthritis Rheum. 29: 1334-1342. (Pubitemid 17214033)
5. Brinkmann, V., U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, D. S. Weiss, Y. Weinrauch, and A. Zychlinsky. 2004. Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535. (Pubitemid 38314426)
6. Fuchs, T. A., U. Abed, C. Goosmann, R. Hurwitz, I. Schulze, V. Wahn, Y. Weinrauch, V. Brinkmann, and A. Zychlinsky. 2007. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176: 231-241. (Pubitemid 46143263)
7. Gupta, A. K., M. B. Joshi, M. Philippova, P. Erne, P. Hasler, S. Hahn, and T. J. Resink. 2010. Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett. 584: 3193-3197.
8. Neeli, I., S. N. Khan, and M. Radic. 2008. Histone deimination as a response to inflammatory stimuli in neutrophils. J. Immunol. 180: 1895-1902.
9. Papayannopoulos, V., K. D. Metzler, A. Hakkim, and A. Zychlinsky. 2010. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 191: 677-691.
10. Kessenbrock, K., M. Krumbholz, U. Schonermarck, W. Back, W. L. Gross, Z. Werb, H. J. Grone, V. Brinkmann, and D. E. Jenne. 2009. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 191: 677-691.
11. Caielli, S., G. Garcia.-Romo, B. Vega, J. Connolly, F. Xu, Z. Allantaz, M. Punaro, J. Baisch, C. Guiducci, F. Barrat, et al. 2010. Netting neutrophils are major inducers of type 1 IFN production in SLE (PO1.M.11 Abstract of Poster Session). Lupus 19(1 Suppl): 117-118.
12. Fuchs, T. A., A. Brill, D. Duerschmied, D. Schatzberg, M. Monestier, D. D. Myers, Jr., S. K. Wrobleski, T. W. Wakefield, J. H. Hartwig, and D. D. Wagner. 2010. Extracellular DNA traps promote thrombosis. Proc. Natl. Acad. Sci. USA 107: 15880-15885.
13. Hochberg, M. C. 1997. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40: 1725.
14. Bombardier, C., D. D. Gladman, M. B. Urowitz, D. Caron, C. H. Chang; The Committee on Prognosis Studies in SLE. 1992. Derivation of the SLEDAI. A disease activity index for lupus patients. Arthritis Rheum. 35: 630-640.
15. Clark, R. A., and W. M. Nauseef. 2005. Isolation and functional analysis of neutrophils, Unit 7.23. In: Current Protocols in Immunology. J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober, eds. W. John Wiley & Sons, Hoboken, NJ.
16. Johnson, W. E., C. Li, and A. Rabinovic. 2007. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8: 118-127. (Pubitemid 44906106)
17. Saeed, A. I., N. K. Bhagabati, J. C. Braisted, W. Liang, V. Sharov, E. A. Howe, J. Li, M. Thiagarajan, J. A. White, and J. Quackenbush. 2006. TM4 microarray software suite. Methods Enzymol. 411: 134-193.
18. Saeed, A. I., V. Sharov, J. White, J. Li, W. Liang, N. Bhagabati, J. Braisted, M. Klapa, T. Currier, M. Thiagarajan, et al. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378. (Pubitemid 36184095)
19. Chaperot, L., A. Blum, O. Manches, G. Lui, J. Angel, J. P. Molens, and J. Plumas. 2006. Virus or TLR agonists induce TRAIL-mediated cytotoxic activity of plasmacytoid dendritic cells. J. Immunol. 176: 248-255. (Pubitemid 43023269)
20. Weening, J. J., V. D. D'Agati, M. M. Schwartz, S. V. Seshan, C. E. Alpers, G. B. Appel, J. E. Balow, J. A. Bruijn, T. Cook, F. Ferrario, et al; International Society of Nephrology Working Group on the Classification of Lupus Nephritis; Renal Pathology Society Working Group on the Classification of Lupus Nephritis. 2004. The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int. 65: 521-530.
21. Papayannopoulos, V., and A. Zychlinsky. 2009. NETs: a new strategy for using old weapons. Trends Immunol. 30: 513-521.
22. Ganguly, D., G. Chamilos, R. Lande, J. Gregorio, S. Meller, V. Facchinetti, B. Homey, F. J. Barrat, T. Zal, and M. Gilliet. 2009. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J. Exp. Med. 206: 1983-1994.
23. Lande, R., J. Gregorio, V. Facchinetti, B. Chatterjee, Y. H. Wang, B. Homey, W. Cao, Y. H.Wang, B. Su, F. O. Nestle, et al. 2007. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 449: 564-569. (Pubitemid 47525141)
24. Nakou, M., N. Knowlton, M. B. Frank, G. Bertsias, J. Osban, C. E. Sandel, H. Papadaki, A. Raptopoulou, P. Sidiropoulos, I. Kritikos, et al. 2008. Gene expression in systemic lupus erythematosus: bone marrow analysis differentiates active from inactive disease and reveals apoptosis and granulopoiesis signatures. Arthritis Rheum. 58: 3541-3549.
25. Pham, C. T. 2006. Neutrophil serine proteases: specific regulators of inflammation. Nat. Rev. Immunol. 6: 541-550.
26. Cua, D. J., and C. M. Tato. 2010. Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10: 479-489.
27. Hoshino, A., T. Nagao, N. Nagi-Miura, N. Ohno, M. Yasuhara, K. Yamamoto, T. Nakayama, and K. Suzuki. 2008. MPO-ANCA induces IL-17 production by activated neutrophils in vitro via classical complement pathway-dependent manner. J. Autoimmun. 31: 79-89. (Pubitemid 351685761)
28. de Boer, O. J., J. J. van der Meer, P. Teeling, C. M. van der Loos, M. M. Idu, F. van Maldegem, J. Aten, and A. C. van der Wal. 2010. Differential expression of interleukin-17 family cytokines in intact and complicated human atherosclerotic plaques. J. Pathol. 220: 499-508.
29. Lin, A. M., C. J. Rubin, R. Khandpur, J. Y. Wang, M. B. Riblett, S. Yalavarthi, E. C. Villanueva, P. Shah, M. J. Kaplan, and A. T. Bruce. 2011. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J. Immunol. 187: 490-500.
30. Crispín, J. C., and G. C. Tsokos. 2010. IL-17 in systemic lupus erythematosus. J. Biomed. Biotechnol. 2010: 943254.
31. Chen, X. Q., Y. C. Yu, H. H. Deng, J. Z. Sun, Z. Dai, Y. W. Wu, and M. Yang. 2010. Plasma IL-17A is increased in new-onset SLE patients and associated with disease activity. J. Clin. Immunol. 30: 221-225.
32. Edgerton, C., J. C. Crispín, C. M. Moratz, E. Bettelli, M. Oukka, M. Simovic, A. Zacharia, R. Egan, J. Chen, J. J. Dalle Lucca, et al. 2009. IL-17 producing CD4+ T cells mediate accelerated ischemia/reperfusion-induced injury in autoimmunity-prone mice. Clin. Immunol. 130: 313-321.
33. Camussi, G., F. C. Cappio, M. Messina, R. Coppo, P. Stratta, and A. Vercellone. 1980. The polymorphonuclear neutrophil (PMN) immunohistological technique: detection of immune complexes bound to the PMN membrane in acute poststreptococcal and lupus nephritis. Clin. Nephrol. 14: 280-287.
34. Gilliet, M., and R. Lande. 2008. Antimicrobial peptides and self-DNA in autoimmune skin inflammation. Curr. Opin. Immunol. 20: 401-407.
35. Martinelli, S., M. Urosevic, A. Daryadel, P. A. Oberholzer, C. Baumann, M. F. Fey, R. Dummer, H. U. Simon, and S. Yousefi. 2004. Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation. J. Biol. Chem. 279: 44123-44132.
36. Rajagopalan, S., E. C. Somers, R. D. Brook, C. Kehrer, D. Pfenninger, E. Lewis, A. Chakrabarti, B. C. Richardson, E. Shelden, W. J. McCune, and M. J. Kaplan. 2004. Endothelial cell apoptosis in systemic lupus erythematosus: a common pathway for abnormal vascular function and thrombosis propensity. Blood 103: 3677-3683.
37. Cowland, J. B., and N. Borregaard. 1999. The individual regulation of granule protein mRNA levels during neutrophil maturation explains the heterogeneity of neutrophil granules. J. Leukoc. Biol. 66: 989-995.
38. Kessenbrock, K., L. Fröhlich, M. Sixt, T. Lämmermann, H. Pfister, A. Bateman, A. Belaaouaj, J. Ring, M. Ollert, R. Fässler, and D. E. Jenne. 2008. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J. Clin. Invest. 118: 2438-2447.
39. Adkison, A. M., S. Z. Raptis, D. G. Kelley, and C. T. Pham. 2002. Dipeptidyl peptidase I activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis. J. Clin. Invest. 109: 363-371.
40. Meyer-Hoffert, U. 2009. Neutrophil-derived serine proteases modulate innate immune responses. Front. Biosci. 14: 3409-3418.
41. Devaney, J. M., C. M. Greene, C. C. Taggart, T. P. Carroll, S. J. O'Neill, and N. G. McElvaney. 2003. Neutrophil elastase up-regulates interleukin-8 via tolllike receptor 4. FEBS Lett. 544: 129-132.
42. Ding, D., H. Mehta, W. J. McCune, and M. J. Kaplan. 2006. Aberrant phenotype and function of myeloid dendritic cells in systemic lupus erythematosus. J. Immunol. 177: 5878-5889.
43. Bals, R., and J. M. Wilson. 2003. Cathelicidins - a family of multifunctional antimicrobial peptides. Cell. Mol. Life Sci. 60: 711-720.
44. de la Rosa, G., D. Yang, P. Tewary, A. Varadhachary, and J. J. Oppenheim. 2008. Lactoferrin acts as an alarmin to promote the recruitment and activation of APCs and antigen-specific immune responses. J. Immunol. 180: 6868-6876.
45. Vordenbaumen, S., R. Fischer-Betz, D. Timm, O. Sander, G. Chehab, J. Richter, E. Bleck, and M. Schneider. 2010. Elevated levels of human beta-defensin 2 and human neutrophil peptides in systemic lupus erythematosus. Lupus 19: 1648-1653.
46. Telles, R. W., G. A. Ferreira, N. P. da Silva, and E. I. Sato. 2010. Increased plasma myeloperoxidase levels in systemic lupus erythematosus. Rheumatol. Int. 30: 779-784.
47. Tamiya, H., K. Tani, J. Miyata, K. Sato, T. Urata, B. Lkhagvaa, S. Otsuka, S. Shigekiyo, and S. Sone. 2006. Defensins- and cathepsin G-ANCA in systemic lupus erythematosus. Rheumatol. Int. 27: 147-152.
48. Froy, O., and Z. M. Sthoeger. 2009. Defensins in systemic lupus erythematosus. Ann. N. Y. Acad. Sci. 1173: 365-369.
49. Kumar, V., and A. Sharma. 2010. Neutrophils: Cinderella of innate immune system. Int. Immunopharmacol. 10: 1325-1334.
50. Viau, A., K. El Karoui, D. Laouari, M. Burtin, C. Nguyen, K. Mori, E. Pillebout, T. Berger, T. W. Mak, B. Knebelmann, et al. 2010. Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J. Clin. Invest. 120: 4065-4076.
51. Ionita, M. G., P. van den Borne, L. M. Catanzariti, F. L. Moll, J. P. de Vries, G. Pasterkamp, A. Vink, and D. P. de Kleijn. 2010. High neutrophil numbers in human carotid atherosclerotic plaques are associated with characteristics of rupture-prone lesions. Arterioscler. Thromb. Vasc. Biol. 30: 1842-1848.
52. Banchereau, J., and V. Pascual. 2006. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 25: 383-392. (Pubitemid 44354221)
53. Ruiz-Irastorza, G., M. A. Khamashta, G. Castellino, and G. R. Hughes. 2001. Systemic lupus erythematosus. Lancet 357: 1027-1032.
54. Wenzel, J., S. Zahn, and T. Tüting. 2010. Pathogenesis of cutaneous lupus erythematosus: common and different features in distinct subsets. Lupus 19: 1020-1028.
55. Farkas, L., K. Beiske, F. Lund-Johansen, P. Brandtzaeg, and F. L. Jahnsen. 2001. Plasmacytoid dendritic cells (natural interferon- alpha/beta-producing cells) accumulate in cutaneous lupus erythematosus lesions. Am. J. Pathol. 159: 237-243.
56. Guiducci, C., C. Tripodo, M. Gong, S. Sangaletti, M. P. Colombo, R. L. Coffman, and F. J. Barrat. 2010. Autoimmune skin inflammation is dependent on plasma-cytoiddendritic cell activation by nucleic acids via TLR7 and TLR9. J. Exp. Med. 207: 2931-2942.
57. Shah, K., W. W. Lee, S. H. Lee, S. H. Kim, S. W. Kang, J. Craft, and I. Kang. 2010. Dysregulated balance of Th17 and Th1 cells in systemic lupus erythematosus. Arthritis Res. Ther. 12: R53.
58. Dolff, S., D. Quandt, B. Wilde, T. Feldkamp, F. Hua, X. Cai, C. Specker, A. Kribben, C. G. Kallenberg, and O. Witzke. 2010. Increased expression of costimulatory markers CD134 and CD80 on interleukin-17 producing T cells in patients with systemic lupus erythematosus. Arthritis Res. Ther. 12: R150.
59. Zhang, Z., V. C. Kyttaris, and G. C. Tsokos. 2009. The role of IL-23/IL-17 axis in lupus nephritis. J. Immunol. 183: 3160-3169.
60. Tanasescu, C., E. Balanescu, P. Balanescu, R. Olteanu, C. Badea, C. Grancea, C. Vagu, C. Bleotu, C. Ardeleanu, and A. Georgescu. 2010. IL-17 in cutaneous lupus erythematosus. Eur. J. Intern. Med. 21: 202-207.
61. Roussel, L., F. Houle, C. Chan, Y. Yao, J. Bérubé, R. Olivenstein, J. G. Martin, J. Huot, Q. Hamid, L. Ferri, and S. Rousseau. 2010. IL-17 promotes p38 MAPK-dependent endothelial activation enhancing neutrophil recruitment to sites of inflammation. J. Immunol. 184: 4531-4537.
62. Emamian, E. S., J. M. Leon, C. J. Lessard, M. Grandits, E. C. Baechler, P. M. Gaffney, B. Segal, N. L. Rhodus, and K. L. Moser. 2009. Peripheral blood gene expression profiling in Sjogren's syndrome. Genes Immun. 10: 285-296.
63. Walsh, R. J., S. W. Kong, Y. Yao, B. Jallal, P. A. Kiener, J. L. Pinkus, A. H. Beggs, A. A. Amato, and S. A. Greenberg. 2007. Type I interferon-inducible gene expression in blood is present and reflects disease activity in dermatomyositis and polymyositis. Arthritis Rheum. 56: 3784-3792.
64. Yang, D., D. Arkfeld, and T. L. Fong. 2010. Development of anti-CCP-positive rheumatoid arthritis following pegylated interferon-alpha2a treatment for chronic hepatitis C infection. J. Rheumatol. 37: 1777.
65. Garcia-Romo, G. S., S. Caielli, B. Vega, J. Connolly, F. Allantaz, Z. Xu, M. Punaro, J. Baisch, C. Guiducci, R. L. Coffman, et al. 2010. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 3: 73ra20.
66. Lande, R., D. Ganguly, V. Facchinetti, L. Frasca, C. Conrad, J. Gregorio, S. Meller, G. Chamilos, R. Sebasigari, V. Riccieri, et al. 2011. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci. Transl. Med. 3: 73ra19.