Macrophage clearance of neutrophil extracellular traps is a silent process

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2647-2656

  Farrera, Consol ^a   Fadeel, Bengt ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; COMPLEMENT COMPONENT C1Q; CYTOCHALASIN D; DEOXYRIBONUCLEASE I; DEOXYRIBONUCLEASE II; DNA; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; CELL COMPONENT; CELL ISOLATION; CLEARANCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEGRADATION; ENDOCYTOSIS; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTERNALIZATION; LYSOSOME; MACROPHAGE; NEUTROPHIL; NEUTROPHIL EXTRACELLULAR TRAP; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; WESTERN BLOTTING;

BLOTTING, WESTERN; COMPLEMENT C1Q; DEOXYRIBONUCLEASE I; EXTRACELLULAR SPACE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MACROPHAGES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; NEUTROPHIL ACTIVATION; NEUTROPHILS; PHAGOCYTOSIS;

EID: 84883403574     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300436     Document Type: Article

References (41)

1. 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.
2. 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.
3. Yipp, B. G., B. Petri, D. Salina, C. N. Jenne, B. N. Scott, L. D. Zbytnuik, K. Pittman, M. Asaduzzaman, K. Wu, H. C. Meijndert, et al. 2012. Infectioninduced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat. Med. 18: 1386-1393.
4. Papayannopoulos, V., and A. Zychlinsky. 2009. NETs: a new strategy for using old weapons. Trends Immunol. 30: 513-521.
5. Saffarzadeh, M., and K. T. Preissner. 2013. Fighting against the dark side of neutrophil extracellular traps in disease: manoeuvres for host protection. Curr. Opin. Hematol. 20: 3-9.
6. Muñoz, L. E., K. Lauber, M. Schiller, A. A. Manfredi, and M. Herrmann. 2010. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat. Rev. Rheumatol. 6: 280-289.
7. 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.
8. Lauber, K., S. G. Blumenthal, M. Waibel, and S. Wesselborg. 2004. Clearance of apoptotic cells: getting rid of the corpses. Mol. Cell 14: 277-287.
9. Napirei, M., H. Karsunky, B. Zevnik, H. Stephan, H. G. Mannherz, and T. Möröy. 2000. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 25: 177-181.
10. 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. 2011. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 3: 73ra20.
11. 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.
12. Ricklin, D., G. Hajishengallis, K. Yang, and J. D. Lambris. 2010. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 11: 785-797.
13. Botto, M., C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, M. Loos, P. P. Pandolfi, and M. J. Walport. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19: 56-59.
14. Taylor, P. R., A. Carugati, V. A. Fadok, H. T. Cook, M. Andrews, M. C. Carroll, J. S. Savill, P. M. Henson, M. Botto, and M. J. Walport. 2000. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J. Exp. Med. 192: 359-366.
15. Leffler, J., M. Martin, B. Gullstrand, H. Tydén, C. Lood, L. Truedsson, A. A. Bengtsson, and A. M. Blom. 2012. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J. Immunol. 188: 3522-3531.
16. Fadeel, B., A. Åhlin, J. I. Henter, S. Orrenius, and M. B. Hampton. 1998. Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood 92: 4808-4818.
17. Kagan, V. E., B. Gleiss, Y. Y. Tyurina, V. A. Tyurin, C. Elenström-Magnusson, S. X. Liu, F. B. Serinkan, A. Arroyo, J. Chandra, S. Orrenius, and B. Fadeel. 2002. A role for oxidative stress in apoptosis: oxidation and externalization of phosphatidylserine is required for macrophage clearance of cells undergoing Fas-mediated apoptosis. J. Immunol. 169: 487-499.
18. Beiter, K., F. Wartha, B. Albiger, S. Normark, A. Zychlinsky, and B. Henriques-Normark. 2006. An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr. Biol. 16: 401-407.
19. Remijsen, Q., T. W. Kuijpers, E. Wirawan, S. Lippens, P. Vandenabeele, and T. Vanden Berghe. 2011. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ. 18: 581-588.
20. Thomas, G. M., C. Carbo, B. R. Curtis, K. Martinod, I. B. Mazo, D. Schatzberg, S. M. Cifuni, T. A. Fuchs, U. H. von Andrian, J. H. Hartwig, et al. 2012. Extracellular DNA traps are associated with the pathogenesis of TRALI in humans and mice. Blood 119: 6335-6343.
21. Buchanan, J. T., A. J. Simpson, R. K. Aziz, G. Y. Liu, S. A. Kristian, M. Kotb, J. Feramisco, and V. Nizet. 2006. DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr. Biol. 16: 396-400.
22. Berends, E. T., A. R. Horswill, N. M. Haste, M. Monestier, V. Nizet, and M. von Kö ckritz-Blickwede. 2010. Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J. Innate Immun. 2: 576-586.
23. Tinazzi, E., A. Puccetti, R. Gerli, A. Rigo, P. Migliorini, S. Simeoni, R. Beri, M. Dolcino, N. Martinelli, R. Corrocher, and C. Lunardi. 2009. Serum DNase I, soluble Fas/FasL levels and cell surface Fas expression in patients with SLE: a possible explanation for the lack of efficacy of hrDNase I treatment. Int. Immunol. 21: 237-243.
24. Sjöberg, A. P., L. A. Trouw, and A. M. Blom. 2009. Complement activation and inhibition: a delicate balance. Trends Immunol. 30: 83-90.
25. Okabe, Y., K. Kawane, S. Akira, T. Taniguchi, and S. Nagata. 2005. Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J. Exp. Med. 202: 1333-1339.
26. Kawane, K., H. Fukuyama, G. Kondoh, J. Takeda, Y. Ohsawa, Y. Uchiyama, and S. Nagata. 2001. Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver. Science 292: 1546-1549.
27. Kawane, K., H. Fukuyama, H. Yoshida, H. Nagase, Y. Ohsawa, Y. Uchiyama, K. Okada, T. Iida, and S. Nagata. 2003. Impaired thymic development in mouse embryos deficient in apoptotic DNA degradation. Nat. Immunol. 4: 138-144.
28. Kawane, K., M. Ohtani, K. Miwa, T. Kizawa, Y. Kanbara, Y. Yoshioka, H. Yoshikawa, and S. Nagata. 2006. Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature 443: 998-1002.
29. Yoshida, H., Y. Okabe, K. Kawane, H. Fukuyama, and S. Nagata. 2005. Lethal anemia caused by interferon-beta produced in mouse embryos carrying undigested DNA. Nat. Immunol. 6: 49-56.
30. Clark, S. R., A. C. Ma, S. A. Tavener, B. McDonald, Z. Goodarzi, M. M. Kelly, K. D. Patel, S. Chakrabarti, E. McAvoy, G. D. Sinclair, et al. 2007. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 13: 463-469.
31. 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.
32. Hakkim, A., T. A. Fuchs, N. E. Martinez, S. Hess, H. Prinz, A. Zychlinsky, and H. Waldmann. 2011. Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat. Chem. Biol. 7: 75-77.
33. Menegazzi, R., E. Decleva, and P. Dri. 2012. Killing by neutrophil extracellular traps: fact or folklore? Blood 119: 1214-1216.
34. Gaipl, U. S., T. D. Beyer, P. Heyder, S. Kuenkele, A. Böttcher, R. E. Voll, J. R. Kalden, and M. Herrmann. 2004. Cooperation between C1q and DNase I in the clearance of necrotic cell-derived chromatin. Arthritis Rheum. 50: 640-649.
35. Kawane, K., H. Tanaka, Y. Kitahara, S. Shimaoka, and S. Nagata. 2010. Cytokine-dependent but acquired immunity-independent arthritis caused by DNA escaped from degradation. Proc. Natl. Acad. Sci. USA 107: 19432-19437.
36. Bergsmedh, A., J. Ehnfors, K. Kawane, N. Motoyama, S. Nagata, and L. Holmgren. 2006. DNase II and the Chk2 DNA damage pathway form a genetic barrier blocking replication of horizontally transferred DNA. Mol. Cancer Res. 4: 187-195.
37. Keshari, R. S., A. Verma, M. K. Barthwal, and M. Dikshit. 2013. Reactive oxygen species-induced activation of ERK and p38 MAPK mediates PMA-induced NETs release from human neutrophils. J. Cell. Biochem. 114: 532-540.
38. Farley, K., J. M. Stolley, P. Zhao, J. Cooley, and E. Remold-O'Donnell. 2012. A serpinB1 regulatory mechanism is essential for restricting neutrophil extracellular trap generation. J. Immunol. 189: 4574-4581.
39. Campbell, A. M., M. Kashgarian, M. J. Shlomchik. 2012. NADPH oxidase inhibits the pathogenesis of systemic lupus erythematosus. Sci. Transl. Med. 4: 157ra141.
40. Liu, C. L., S. Tangsombatvisit, J. M. Rosenberg, G. Mandelbaum, E. C. Gillespie, O. P. Gozani, A. A. Alizadeh, and P. J. Utz. 2012. Specific posttranslational histone modifications of neutrophil extracellular traps as immunogens and potential targets of lupus autoantibodies. Arthritis Res. Ther. 14: R25.
41. Fadeel, B., D. Xue, and V. Kagan. 2010. Programmed cell clearance: molecular regulation of the elimination of apoptotic cell corpses and its role in the resolution of inflammation. Biochem. Biophys. Res. Commun. 396: 7-10.