NADPH oxidase inhibits the pathogenesis of systemic lupus erythematosus

Science Translational Medicine

Volumn 4, Issue 157, 2012, Pages

  Campbell, Allison M ^a   Kashgarian, Michael ^a   Shlomchik, Mark J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; NUCLEIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; DISEASE COURSE; HETEROZYGOSITY; IN VITRO STUDY; IN VIVO STUDY; KIDNEY DISEASE; MOUSE; NEUTROPHIL; NONHUMAN; NULL ALLELE; PATHOGENESIS; PHAGOCYTE; PRIORITY JOURNAL; SPLEEN WEIGHT; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIBODY FORMATION; CELL PROLIFERATION; DNA; EXTRACELLULAR SPACE; FEMALE; HUMANS; KIDNEY DISEASES; LUPUS ERYTHEMATOSUS, SYSTEMIC; MEMBRANE GLYCOPROTEINS; MICE; MYELOID CELLS; NADPH OXIDASE; NEUTROPHILS; ORGAN SIZE; SPLEEN;

EID: 84868020491     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3004801     Document Type: Article

References (48)

1. S. R. Christensen, J. Shupe, K. Nickerson, M. Kashgarian, R. A. Flavell, M. J. Shlomchik, Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity 25, 417-428 (2006).
2. K. M. Nickerson, S. R. Christensen, J. Shupe, M. Kashgarian, D. Kim, K. Elkon, M. J. Shlomchik, TLR9 regulates TLR7- and MyD88-dependent autoantibody production and disease in a murine model of lupus. J. Immunol. 184, 1840-1848 (2010).
3. S. Nagata, R. Hanayama, K. Kawane, Autoimmunity and the clearance of dead cells. Cell 140, 619-630 (2010).
4. M. Botto, C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, M. Loos, P. P. Pandolfi, M. J.Walport, Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19, 56-59 (1998).
5. R. Hanayama, M. Tanaka, K. Miyasaka, K. Aozasa, M. Koike, Y. Uchiyama, S. Nagata, Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304, 1147-1150 (2004).
6. H. D. Shin, B. L. Park, H. S. Cheong, H. S. Lee, J. B. Jun, S. C. Bae, DNase II polymorphisms associated with risk of renal disorder among systemic lupus erythematosus patients. J. Hum. Genet. 50, 107-111 (2005).
7. M. Napirei, H. Karsunky, B. Zevnik, H. Stephan, H. G. Mannherz, T. Möröy, Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 25, 177-181 (2000).
8. Y. Ren, J. Tang, M. Y. Mok, A. W. Chan, A. Wu, C. S. Lau, Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum. 48, 2888-2897 (2003).
9. S. M. Anderton, Post-translational modifications of self antigens: Implications for autoimmunity. Curr. Opin. Immunol. 16, 753-758 (2004).
10. E. Darrah, A. Rosen, Granzyme B cleavage of autoantigens in autoimmunity. Cell Death Differ. 17, 624-632 (2010).
11. J. C. Hall, L. Casciola-Rosen, A. Rosen, Altered structure of autoantigens during apoptosis. Rheum. Dis. Clin. North Am. 30, 455-471 (2004).
12. X. Wu, C. Molinaro, N. Johnson, C. A. Casiano, Secondary necrosis is a source of proteolytically modified forms of specific intracellular autoantigens: Implications for systemic autoimmunity. Arthritis Rheum. 44, 2642-2652 (2001).
13. S. L. Fink, B. T. Cookson, Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 8, 1812-1825 (2006).
14. P. Vandenabeele, W. Declercq, F. Van Herreweghe, T. Vanden Berghe, The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci. Signal. 3, re4 (2010).
15. V. Brinkmann, U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, D. S. Weiss, Y. Weinrauch, A. Zychlinsky, Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535 (2004).
16. T. A. Fuchs, U. Abed, C. Goosmann, R. Hurwitz, I. Schulze, V. Wahn, Y.Weinrauch, V. Brinkmann, A. Zychlinsky, Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231-241 (2007).
17. M. von Köckritz-Blickwede, O. Goldmann, P. Thulin, K. Heinemann, A. Norrby-Teglund, M. Rohde, E. Medina, Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111, 3070-3080 (2008).
18. C. C. Mihalache, S. Yousefi, S. Conus, P. M. Villiger, E. M. Schneider, H. U. Simon, Inflammationassociated autophagy-related programmed necrotic death of human neutrophils characterized by organelle fusion events. J. Immunol. 186, 6532-6542 (2011).
19. J. W. Athens,O. P.Haab, S.O. Raab, A.M. Mauer, H. Ashenbrucker,G. E. Cartwright, M. M. Wintrobe, Leukokinetic studies. IV. The total blood, circulating and marginal granulocyte pools and the granulocyte turnover rate in normal subjects. J. Clin. Invest. 40, 989-995 (1961).
20. R. Lande, D. Ganguly, V. Facchinetti, L. Frasca, C. Conrad, J. Gregorio, S. Meller, G. Chamilos, R. Sebasigari, V. Riccieri, R. Bassett, H. Amuro, S. Fukuhara, T. Ito, Y. J. Liu, M. Gilliet, Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci. Transl. Med. 3, 73ra19 (2011).
21. G. S. Garcia-Romo, S. Caielli, B. Vega, J. Connolly, F. Allantaz, Z. Xu, M. Punaro, J. Baisch, C. Guiducci, R. L. Coffman, F. J. Barrat, J. Banchereau, V. Pascual, Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 3, 73ra20 (2011).
22. A. Hakkim, B. G. Fürnrohr, K. Amann, B. Laube, U. A. Abed, V. Brinkmann, M. Herrmann, R. E. Voll, A. Zychlinsky, Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc. Natl. Acad. Sci. U.S.A. 107, 9813-9818 (2010).
23. E. Villanueva, S. Yalavarthi, C. C. Berthier, J. B. Hodgin, R. Khandpur, A. M. Lin, C. J. Rubin, W. Zhao, S. H. Olsen, M. Klinker, D. Shealy, M. F. Denny, J. Plumas, L. Chaperot, M. Kretzler, A. T. Bruce, M. J. Kaplan, Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J. Immunol. 187, 538-552 (2011).
24. J. E. Craft, Dissecting the immune cell mayhem that drives lupus pathogenesis. Sci. Transl. Med. 3, 73ps9 (2011).
25. V. Papayannopoulos, A. Zychlinsky, NETs: A new strategy for using old weapons. Trends Immunol. 30, 513-521 (2009).
26. R. Menegazzi, E. Decleva, P. Dri, Killing by neutrophil extracellular traps: Fact or folklore? Blood 119, 1214-1216 (2012).
27. K. Beiter, F. Wartha, B. Albiger, S. Normark, A. Zychlinsky, B. Henriques-Normark, An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr. Biol. 16, 401-407 (2006).
28. D. Ermert, C. F. Urban, B. Laube, C. Goosmann, A. Zychlinsky, V. Brinkmann, Mouse neutrophil extracellular traps in microbial infections. J. Innate Immun. 1, 181-193 (2009).
29. H. Parker, M. Dragunow, M. B. Hampton, A. J. Kettle, C. C. Winterbourn, Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J. Leukoc. Biol. 92, 841-849 (2012).
30. M. C. Hochberg, Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40, 1725 (1997).
31. P. L. Cohen, R. A. Eisenberg, Lpr and gld: Single gene models of systemic autoimmunity and lymphoproliferative disease. Annu. Rev. Immunol. 9, 243-269 (1991).
32. D. Perry, A. Sang, Y. Yin, Y. Y. Zheng, L. Morel, Murine models of systemic lupus erythematosus. J. Biomed. Biotechnol. 2011, 271694 (2011).
33. S. Manzi, A. H. Urbach, A. B. McCune, H. A. Altman, S. S. Kaplan, T. A. Medsger Jr., R. Ramsey- Goldman, Systemic lupus erythematosus in a boy with chronic granulomatous disease: Case report and review of the literature. Arthritis Rheum. 34, 101-105 (1991).
34. J. Schaller, Illness resembling lupus erythematosus in mothers of boys with chronic granulomatous disease. Ann. Intern. Med. 76, 747-750 (1972).
35. C. M. Cale, L. Morton, D. Goldblatt, Cutaneous and other lupus-like symptoms in carriers of X-linked chronic granulomatous disease: Incidence and autoimmune serology. Clin. Exp. Immunol. 148, 79-84 (2007).
36. L. Romani, F. Fallarino, A. De Luca, C. Montagnoli, C. D'Angelo, T. Zelante, C. Vacca, F. Bistoni, M. C. Fioretti, U. Grohmann, B. H. Segal, P. Puccetti, Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451, 211-215 (2008).
37. A. L. Mellor, D. H. Munn, IDO expression by dendritic cells: Tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4, 762-774 (2004).
38. B. Jürgens, D. Fuchs, J. Reichenbach, A. Heitger, Intact indoleamine 2,3-dioxygenase activity in human chronic granulomatous disease. Clin. Immunol. 137, 1-4 (2010).
39. S. S. De Ravin, K. A. Zarember, D. Long-Priel, K. C. Chan, S. D. Fox, J. I. Gallin, D. B. Kuhns, H. L. Malech, Tryptophan/kynurenine metabolism in human leukocytes is independent of superoxide and is fully maintained in chronic granulomatous disease. Blood 116, 1755-1760 (2010).
40. R. Fernandez-Boyanapalli, K. A. McPhillips, S. C. Frasch, W. J. Janssen, M. C. Dinauer, D. W. Riches, P. M. Henson, A. Byrne, D. L. Bratton, Impaired phagocytosis of apoptotic cells by macrophages in chronic granulomatous disease is reversed by IFN-g in a nitric oxide-dependent manner. J. Immunol. 185, 4030-4041 (2010).
41. K. Lee, H. Y. Won, M. A. Bae, J. H. Hong, E. S. Hwang, Spontaneous and aging-dependent development of arthritis in NADPH oxidase 2 deficiency through altered differentiation of CD11b+ and Th/Treg cells. Proc. Natl. Acad. Sci. U.S.A. 108, 9548-9553 (2011).
42. V. Brinkmann, A. Zychlinsky, Beneficial suicide: Why neutrophils die to make NETs. Nat. Rev. Microbiol. 5, 577-582 (2007).
43. B. Fadeel, A. Ahlin, J. I. Henter, S. Orrenius, M. B. Hampton, Involvement of caspases in neutrophil apoptosis: Regulation by reactive oxygen species. Blood 92, 4808-4818 (1998).
44. R. P. Wilkie, M. C. M. Vissers, M. Dragunow, M. B. Hampton, A functional NADPH oxidase prevents caspase involvement in the clearance of phagocytic neutrophils. Infect. Immun. 75, 3256-3263 (2007).
45. F. Andrade, L. Casciola-Rosen, A. Rosen, Apoptosis in systemic lupus erythematosus. Clinical implications. Rheum. Dis. Clin. North Am. 26, 215-227 (2000).
46. M. Nagahama, S. Nomura, Y. Ozaki, C. Yoshimura, H. Kagawa, S. Fukuhara, Platelet activation markers and soluble adhesion molecules in patients with systemic lupus erythematosus. Autoimmunity 33, 85-94 (2001).
47. C. O. Jacob, M. Eisenstein, M. C. Dinauer, W. Ming, Q. Liu, S. John, F. P. Quismorio Jr., A. Reiff, B. L. Myones, K. M. Kaufman, D. McCurdy, J. B. Harley, E. Silverman, R. P. Kimberly, T. J. Vyse, P. M. Gaffney, K. L. Moser, M. Klein-Gitelman, L. Wagner-Weiner, C. D. Langefeld, D. L. Armstrong, R. Zidovetzki, Lupus-associated causal mutation in neutrophil cytosolic factor 2 (NCF2) brings unique insights to the structure and function of NADPH oxidase. Proc. Natl. Acad. Sci. U.S.A. 109, E59-E67 (2012).
48. A. Doria, M. Canova, M. Tonon, M. Zen, E. Rampudda, N. Bassi, F. Atzeni, S. Zampieri, A. Ghirardello, Infections as triggers and complications of systemic lupus erythematosus. Autoimmun. Rev. 8, 24-28 (2008).