IgA enhances netosis and release of neutrophil extracellular traps by polymorphonuclear cells via FCA receptor I

Journal of Immunology

Volumn 192, Issue 5, 2014, Pages 2374-2383

  Aleyd, Esil ^a   Van Hout, Miel W M ^a   Ganzevles, Sonja H ^a   Hoeben, Kees A ^b   Everts, Vincent ^b   Bakema, Jantine E ^a   Van Egmond, Marjolein ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

7 AMINODACTINOMYCIN; FC ALPHA RECEPTOR I; FC RECEPTOR; IMMUNOGLOBULIN A; LIPOCORTIN 5; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEUKOCYTE FUNCTION; NEUTROPHIL EXTRACELLULAR TRAP; PHAGOCYTOSIS; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BLOCKING;

ANNEXIN A5; ANTIGENS, CD; BACTERIA; CELL DEATH; DACTINOMYCIN; FEMALE; FLUORESCENT DYES; HUMANS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; INFLAMMATION; MALE; NEUTROPHILS; PHAGOCYTOSIS; RECEPTORS, FC;

EID: 84896502411     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300261     Document Type: Article

References (56)

1. Fagarasan, S., and T. Honjo. 2003. Intestinal IgA synthesis: regulation of frontline body defences. Nat. Rev. Immunol. 3: 63-72.
2. Woof, J. M., and M. A. Kerr. 2006. The function of immunoglobulin A in immunity. J. Pathol. 208: 270-282.
3. Herr, A. B., E. R. Ballister, and P. J. Bjorkman. 2003. Insights into IgA-mediated immune responses from the crystal structures of human FcalphaRI and its complex with IgA1-Fc. Nature 423: 614-620.
4. Bakema, J. E., and M. Van Egmond. 2011. The human immunoglobulin A Fc receptor FcaRI: a multifaceted regulator of mucosal immunity. Mucosal Immunol. 4: 612-624.
5. Monteiro, R. C., R. W. Hostoffer, M. D. Cooper, J. R. Bonner, G. L. Gartland, and H. Kubagawa. 1993. Definition of immunoglobulin A receptors on eosinophils and their enhanced expression in allergic individuals. J. Clin. Invest. 92: 1681-1685.
6. Monteiro, R. C., H. Kubagawa, and M. D. Cooper. 1990. Cellular distribution, regulation, and biochemical nature of an Fc alpha receptor in humans. J. Exp. Med. 171: 597-613.
7. van Egmond, M., E. Van Garderen, A. B. Van Spriel, C. A. Damen, E. S. Van Amersfoort, G. Van Zandbergen, J. Van Hattum, J. Kuiper, and J. G. Van De Winkel. 2000. FcalphaRI-positive liver Kupffer cells: reappraisal of the function of immunoglobulin A in immunity. Nat. Med. 6: 680-685.
8. Monteiro, R. C., and J. G. Van De Winkel. 2003. IgA Fc receptors. Annu. Rev. Immunol. 21: 177-204.
9. van der Steen, L., C. W. Tuk, J. E. Bakema, G. Kooij, A. Reijerkerk, G. Vidarsson, G. Bouma, G. Kraal, H. E. De Vries, R. H. Beelen, and M. Van Egmond. 2009. Immunoglobulin A: Fc(alpha)RI interactions induce neutrophil migration through release of leukotriene B4. Gastroenterology 137: 2018-2029. e1-3.
10. Vidarsson, G., W. L. Van Der Pol, J. M. Van Den Elsen, H. Vilé, M. Jansen, J. Duijs, H. C. Morton, E. Boel, M. R. Daha, B. Corthésy, and J. G. Van De Winkel. 2001. Activity of human IgG and IgA subclasses in immune defense against Neisseria meningitidis serogroup B. J. Immunol. 166: 6250-6256.
11. van der Steen, L. P., J. E. Bakema, A. Sesarman, F. Florea, C. W. Tuk, G. Kirtschig, J. J. Hage, C. Sitaru, and M. Van Egmond. 2012. Blocking Fca receptor I on granulocytes prevents tissue damage induced by IgA autoantibodies. J. Immunol. 189: 1594-1601.
12. Amulic, B., C. Cazalet, G. L. Hayes, K. D. Metzler, and A. Zychlinsky. 2012. Neutrophil function: from mechanisms to disease. Annu. Rev. Immunol. 30: 459-489.
13. Borregaard, N. 2010. Neutrophils, from marrow to microbes. Immunity 33: 657-670.
14. 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.
15. Urban, C. F., D. Ermert, M. Schmid, U. Abu-Abed, C. Goosmann, W. Nacken, V. Brinkmann, P. R. Jungblut, and A. Zychlinsky. 2009. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5: e1000639.
16. Pilsczek, F. H., D. Salina, K. K. Poon, C. Fahey, B. G. Yipp, C. D. Sibley, S. M. Robbins, F. H. Green, M. G. Surette, M. Sugai, et al. 2010. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J. Immunol. 185: 7413-7425.
17. 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.
18. Metzler, K. D., T. A. Fuchs, W. M. Nauseef, D. Reumaux, J. Roesler, I. Schulze, V. Wahn, V. Papayannopoulos, and A. Zychlinsky. 2011. Myeloperoxidase is required for neutrophil extracellular trap formation: implications for innate immunity. Blood 117: 953-959.
19. 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.
20. 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.
21. Luo, H. R., and F. Loison. 2008. Constitutive neutrophil apoptosis: mechanisms and regulation. Am. J. Hematol. 83: 288-295.
22. von Köckritz-Blickwede, M., O. A. Chow, and V. Nizet. 2009. Fetal calf serum contains heat-stable nucleases that degrade neutrophil extracellular traps. Blood 114: 5245-5246.
23. Gorter, A., P. S. Hiemstra, P. C. Leijh, M. E. Van der Sluys, M. T. Van den Barselaar, L. A. Van Es, and M. R. Daha. 1987. IgA-And secretory IgAopsonized S. aureus induce a respiratory burst and phagocytosis by polymorphonuclear leucocytes. Immunology 61: 303-309.
24. Brinkmann, V., B. Laube, U. Abu Abed, C. Goosmann, and A. Zychlinsky. 2010. Neutrophil extracellular traps: how to generate and visualize them. J. Vis. Exp. 24: pii: 1724.
25. Pamer, E. G. 2007. Immune responses to commensal and environmental microbes. Nat. Immunol. 8: 1173-1178.
26. Hellwig, S. M., A. B. Van Spriel, J. F. Schellekens, F. R. Mooi, and J. G. Van De Winkel. 2001. Immunoglobulin A-mediated protection against Bordetella pertussis infection. Infect. Immun. 69: 4846-4850.
27. van der Pol, W., G. Vidarsson, H. A. Vilé, J. G. Van De Winkel, and M. E. Rodriguez. 2000. Pneumococcal capsular polysaccharide-specific IgA triggers efficient neutrophil effector functions via FcalphaRI (CD89). J. Infect. Dis. 182: 1139-1145.
28. Chang, A., A. Khemlani, H. Kang, and T. Proft. 2011. Functional analysis of Streptococcus pyogenes nuclease A (SpnA), a novel group A streptococcal virulence factor. Mol. Microbiol. 79: 1629-1642.
29. Midon, M., P. Schäfer, A. Pingoud, M. Ghosh, A. F. Moon, M. J. Cuneo, R. E. London, and G. Meiss. 2011. Mutational and biochemical analysis of the DNA-entry nuclease EndA from Streptococcus pneumoniae. Nucleic Acids Res. 39: 623-634.
30. Uchiyama, S., F. Andreoni, R. A. Schuepbach, V. Nizet, and A. S. Zinkernagel. 2012. DNase Sda1 allows invasive M1T1 group A Streptococcus to prevent TLR9-dependent recognition. PLoS Pathog. 8: e1002736.
31. 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.
32. McDonald, B., R. Urrutia, B. G. Yipp, C. N. Jenne, and P. Kubes. 2012. Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe 12: 324-333.
33. Meng, W., A. Paunel-Görgülü, S. Flohé, A. Hoffmann, I. Witte, C. Mackenzie, S. E. Baldus, J. Windolf, and T. T. Lögters. 2012. Depletion of neutrophil extracellular traps in vivo results in hypersusceptibility to polymicrobial sepsis in mice. Crit. Care 16: R137.
34. Jenne, C. N., C. H. Wong, F. J. Zemp, B. McDonald, M. M. Rahman, P. A. Forsyth, G. McFadden, and P. Kubes. 2013. Neutrophils recruited to sites of infection protect from virus challenge by releasing neutrophil extracellular traps. Cell Host Microbe 13: 169-180.
35. Saitoh, T., J. Komano, Y. Saitoh, T. Misawa, M. Takahama, T. Kozaki, T. Uehata, H. Iwasaki, H. Omori, S. Yamaoka, et al. 2012. Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 12: 109-116.
36. Skrzeczynska-Moncznik, J., A. Wlodarczyk, K. Zabieglo, M. Kapinska-Mrowiecka, E. Marewicz, A. Dubin, J. Potempa, and J. Cichy. 2012. Secretory leukocyte proteinase inhibitor-competent DNA deposits are potent stimulators of plasmacytoid dendritic cells: implication for psoriasis. J. Immunol. 189: 1611-1617.
37. Tillack, K., P. Breiden, R. Martin, and M. Sospedra. 2012. T lymphocyte priming by neutrophil extracellular traps links innate and adaptive immune responses. J. Immunol. 188: 3150-3159.
38. Cooper, P. R., L. J. Palmer, and I. L. Chapple. 2013. Neutrophil extracellular traps as a new paradigm in innate immunity: friend or foe? Periodontol. 2000 63: 165-197.
39. Parker, H., A. M. Albrett, A. J. Kettle, and C. C. Winterbourn. 2012. Myeloperoxidase associated with neutrophil extracellular traps is active and mediates bacterial killing in the presence of hydrogen peroxide. J. Leukoc. Biol. 91: 369-376.
40. Sémiramoth, N., A. Gleizes, I. Turbica, C. Sandré, V. Marin-Esteban, R. Gorges, A. Servin, and S. Chollet-Martin. 2010. Afa/Dr-expressing, diffusely adhering Escherichia coli strain C1845 triggers F1845 fimbria-dependent phosphatidylserine externalization on neutrophil-like differentiated PLB-985 cells through an apoptosis-independent mechanism. Infect. Immun. 78: 2974-2983.
41. Menegazzi, R., E. Decleva, and P. Dri. 2012. Killing by neutrophil extracellular traps: fact or folklore? Blood 119: 1214-1216.
42. Farrera, C., and B. Fadeel. 2013. Macrophage clearance of neutrophil extracellular traps is a silent process. J. Immunol. 191: 2647-2656.
43. Harding, M., and P. Kubes. 2012. Innate immunity in the vasculature: interactions with pathogenic bacteria. Curr. Opin. Microbiol. 15: 85-91.
44. Friggeri, A., S. Banerjee, N. Xie, H. Cui, A. De Freitas, M. Zerfaoui, H. Dupont, E. Abraham, and G. Liu. 2012. Extracellular histones inhibit efferocytosis. Mol. Med. 18: 825-833.
45. Cools-Lartigue, J., J. Spicer, B. McDonald, S. Gowing, S. Chow, B. Giannias, F. Bourdeau, P. Kubes, and L. Ferri. 2013. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J. Clin. Invest. 123: 3446-3458.
46. Caudrillier, A., K. Kessenbrock, B. M. Gilliss, J. X. Nguyen, M. B. Marques, M. Monestier, P. Toy, Z. Werb, and M. R. Looney. 2012. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J. Clin. Invest. 122: 2661-2671.
47. Allen, C., P. Thornton, A. Denes, B. W. McColl, A. Pierozynski, M. Monestier, E. Pinteaux, N. J. Rothwell, and S. M. Allan. 2012. Neutrophil cerebrovascular transmigration triggers rapid neurotoxicity through release of proteases associated with decondensed DNA. J. Immunol. 189: 381-392.
48. von Brühl, M. L., K. Stark, A. Steinhart, S. Chandraratne, I. Konrad, M. Lorenz, A. Khandoga, A. Tirniceriu, R. Coletti, M. Köllnberger, et al. 2012. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J. Exp. Med. 209: 819-835.
49. Saffarzadeh, M., C. Juenemann, M. A. Queisser, G. Lochnit, G. Barreto, S. P. Galuska, J. Lohmeyer, and K. T. Preissner. 2012. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One 7: e32366.
50. Thammavongsa, V., D. M. Missiakas, and O. Schneewind. 2013. Staphylococcus aureus degrades neutrophil extracellular traps to promote immune cell death. Science 342: 863-866.
51. Knight, J. S., and M. J. Kaplan. 2012. Lupus neutrophils: 'NET' gain in understanding lupus pathogenesis. Curr. Opin. Rheumatol. 24: 441-450.
52. 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.
53. Kessenbrock, K., M. Krumbholz, U. Schönermarck, W. Back, W. L. Gross, Z. Werb, H. J. Gröne, V. Brinkmann, and D. E. Jenne. 2009. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 15: 623-625.
54. 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.
55. Chen, K., H. Nishi, R. Travers, N. Tsuboi, K. Martinod, D. D. Wagner, R. Stan, K. Croce, and T. N. Mayadas. 2012. Endocytosis of soluble immune complexes leads to their clearance by FcgRIIIB but induces neutrophil extracellular traps via FcgRIIA in vivo. Blood 120: 4421-4431.
56. Short, K. R., M. von Kockritz-Blickwede, J. D. Langereis, K. Y. Chew, E. R. Job, C. W. Armitage, B. Hatcher, K. Fujihashi, P. C. Reading, P. W. Hermans, et al. 2014. Antibodies mediate the formation of neutrophil extracellular traps (NETs) in the middle ear and facilitate secondary pneumococcal otitis media. Infect. Immun. 82: 364-370.