Table of Contents Author Guidelines Submit a Manuscript
Journal of Immunology Research
Volume 2016 (2016), Article ID 2908034, 17 pages
http://dx.doi.org/10.1155/2016/2908034
Research Article

Differential Use of Human Neutrophil Fcγ Receptors for Inducing Neutrophil Extracellular Trap Formation

1Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, 04510 México, DF, Mexico
2División de Estudios de Posgrado e Investigación, Facultad de Odontología, Universidad Nacional Autónoma de México, 04510 México, DF, Mexico

Received 15 September 2015; Revised 11 December 2015; Accepted 13 December 2015

Academic Editor: Kurt Blaser

Copyright © 2016 Omar Rafael Alemán et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Mócsai, “Diverse novel functions of neutrophils in immunity, inflammation, and beyond,” The Journal of Experimental Medicine, vol. 210, no. 7, pp. 1283–1299, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Brinkmann, U. Reichard, C. Goosmann et al., “Neutrophil extracellular traps kill bacteria,” Science, vol. 303, no. 5663, pp. 1532–1535, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. B. G. Yipp, B. Petri, D. Salina et al., “Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo,” Nature Medicine, vol. 18, no. 9, pp. 1386–1393, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. T. A. Fuchs, U. Abed, C. Goosmann et al., “Novel cell death program leads to neutrophil extracellular traps,” Journal of Cell Biology, vol. 176, no. 2, pp. 231–241, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Bianchi, A. Hakkim, V. Brinkmann et al., “Restoration of NET formation by gene therapy in CGD controls aspergillosis,” Blood, vol. 114, no. 13, pp. 2619–2622, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. Q. Remijsen, T. V. Berghe, E. Wirawan et al., “Neutrophil extracellular trap cell death requires both autophagy and superoxide generation,” Cell Research, vol. 21, no. 2, pp. 290–304, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. I. Neeli and M. Radic, “Knotting the NETs: analyzing histone modifications in neutrophil extracellular traps,” Arthritis Research and Therapy, vol. 14, article 115, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Parker, M. Dragunow, M. B. Hampton, A. J. Kettle, and C. C. Winterbourn, “Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus,” Journal of Leukocyte Biology, vol. 92, no. 4, pp. 841–849, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Branzk and V. Papayannopoulos, “Molecular mechanisms regulating NETosis in infection and disease,” Seminars in Immunopathology, vol. 35, no. 4, pp. 513–530, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. V. Papayannopoulos and A. Zychlinsky, “NETs: a new strategy for using old weapons,” Trends in Immunology, vol. 30, no. 11, pp. 513–521, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Rosales and E. Uribe-Querol, “Antibody—Fc receptor interactions in antimicrobial functions,” Current Immunology Reviews, vol. 9, no. 1, pp. 44–55, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. J. C. Unkeless, Z. Shen, C.-W. Lin, and E. DeBeus, “Function of human FcγRIIA and FcγRIIIB,” Seminars in Immunology, vol. 7, no. 1, pp. 37–44, 1995. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Rosales and E. Uribe-Querol, “Fc receptors: cell activators of antibody functions,” Advances in Bioscience and Biotechnology, vol. 4, no. 4, pp. 21–33, 2013. View at Publisher · View at Google Scholar
  14. P. Selvaraj, W. F. Rosse, R. Silber, and T. A. Springer, “The major Fc receptor in blood has a phosphatidylinositol anchor and is deficient in paroxysmal nocturnal haemoglobinuria,” Nature, vol. 333, no. 6173, pp. 565–567, 1988. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Marois, G. Paré, M. Vaillancourt, E. Rollet-Labelle, and P. H. Naccache, “FcγRIIIb triggers raft-dependent calcium influx in IgG-mediated responses in human neutrophils,” The Journal of Biological Chemistry, vol. 286, no. 5, pp. 3509–3519, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. J. E. Salmon, N. L. Browle, J. C. Edberg, and R. P. Kimberly, “Fcγ receptor III induces actin polymerization in human neutrophils and primes phagocytosis mediated by Fcγ receptor II,” The Journal of Immunology, vol. 146, no. 3, pp. 997–1004, 1991. View at Google Scholar
  17. A. Ortiz-Stern and C. Rosales, “FcγRIIIB stimulation promotes β1 integrin activation in human neutrophils,” Journal of Leukocyte Biology, vol. 77, no. 5, pp. 787–799, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. E. García-García and C. Rosales, “Nuclear factor activation by FcγR in human peripheral blood neutrophils detected by a novel flow cytometry-based method,” Journal of Immunological Methods, vol. 320, no. 1-2, pp. 104–118, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. I. Neeli, N. Dwivedi, S. Khan, and M. Radic, “Regulation of extracellular chromatin release from neutrophils,” Journal of Innate Immunity, vol. 1, no. 3, pp. 194–201, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. I. Neeli, S. N. Khan, and M. Radic, “Histone deimination as a response to inflammatory stimuli in neutrophils,” The Journal of Immunology, vol. 180, no. 3, pp. 1895–1902, 2008. View at Google Scholar · View at Scopus
  21. A. K. Gupta, M. B. Joshi, M. Philippova et al., “Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death,” FEBS Letters, vol. 584, no. 14, pp. 3193–3197, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Chen, H. Nishi, R. Travers et al., “Endocytosis of soluble immune complexes leads to their clearance by FcγRIIIB but induces neutrophil extracellular traps via FcγRIIA in vivo,” Blood, vol. 120, no. 22, pp. 4421–4431, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. K. R. Short, M. von Köckritz-Blickwede, J. D. Langereis et al., “Antibodies mediate formation of neutrophil extracellular traps in the middle ear and facilitate secondary pneumococcal otitis media,” Infection and Immunity, vol. 82, no. 1, pp. 364–370, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Behnen, C. Leschczyk, S. Möller et al., “Immobilized immune complexes induce neutrophil extracellular trap release by human neutrophil granulocytes via FcγRIIIB and Mac-1,” Journal of Immunology, vol. 193, no. 4, pp. 1954–1965, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. E. García-García, E. Uribe-Querol, and C. Rosales, “A simple and efficient method to detect nuclear factor activation in human neutrophils by flow cytometry,” Journal of Visualized Experiments, no. 74, Article ID e50410, 2013. View at Google Scholar · View at Scopus
  26. R. J. Looney, G. N. Abraham, and C. L. Anderson, “Human monocytes and U937 cells bear two distinct Fc receptors for IgG,” The Journal of Immunology, vol. 136, no. 5, pp. 1641–1647, 1986. View at Google Scholar · View at Scopus
  27. H. B. Fleit, S. D. Wright, and J. C. Unkeless, “Human neutrophil Fcγ receptor distribution and structure,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, no. 10, pp. 3275–3279, 1982. View at Publisher · View at Google Scholar · View at Scopus
  28. V. Brinkmann, B. Laube, U. A. Abed, C. Goosmann, and A. Zychlinsky, “Neutrophil extracellular traps: how to generate and visualize them,” Journal of Visualized Experiments, vol. 36, Article ID e1724, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. E. García-García, E. J. Brown, and C. Rosales, “Transmembrane mutations to FcγRIIA alter its association with lipid rafts: implications for receptor signaling,” The Journal of Immunology, vol. 178, no. 5, pp. 3048–3058, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Rivas-Fuentes, E. García-García, G. Nieto-Castañeda, and C. Rosales, “Fcγ receptors exhibit different phagocytosis potential in human neutrophils,” Cellular Immunology, vol. 263, no. 1, pp. 114–121, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Reyes-Reyes, N. Mora, A. Zentella, and C. Rosales, “Phosphatidylinositol 3-kinase mediates integrin-dependent NF-κB and MAPK activation through separate signaling pathways,” Journal of Cell Science, vol. 114, no. 8, pp. 1579–1589, 2001. View at Google Scholar · View at Scopus
  32. J. F. Sweeney, P. K. Nguyen, G. M. Omann, and D. B. Hinshaw, “Ultraviolet irradiation accelerates apoptosis in human polymorphonuclear leukocytes: protection by LPS and GM-CSF,” Journal of Leukocyte Biology, vol. 62, no. 4, pp. 517–523, 1997. View at Google Scholar · View at Scopus
  33. J. T. McClave and T. T. Sincich, Statistics, Pearson, London, UK, 2012.
  34. C. H. Homburg, M. de Haas, A. E. von dem Borne, A. J. Verhoeven, C. P. Reutelingsperger, and D. Roos, “Human neutrophils lose their surface Fc gamma RIII and acquire Annexin V binding sites during apoptosis in vitro,” Blood, vol. 85, no. 2, pp. 532–540, 1995. View at Google Scholar
  35. H. R. Luo and F. Loison, “Constitutive neutrophil apoptosis: mechanisms and regulation,” American Journal of Hematology, vol. 83, no. 4, pp. 288–295, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Akgul, D. A. Moulding, and S. W. Edwards, “Molecular control of neutrophil apoptosis,” FEBS Letters, vol. 487, no. 3, pp. 318–322, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Hakkim, T. A. Fuchs, N. E. Martinez et al., “Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation,” Nature Chemical Biology, vol. 7, no. 2, pp. 75–77, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. E. García-García, G. Nieto-Castañeda, M. Ruiz-Saldaña, N. Mora, and C. Rosales, “FcγRIIA and FcγRIIIB mediate nuclear factor activation through separate signaling pathways in human neutrophils,” The Journal of Immunology, vol. 182, no. 8, pp. 4547–4556, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Y. S. Chuang, M. Sassaroli, and J. C. Unkeless, “Convergence of Fcγ receptor IIA and Fcγ receptor IIIB signaling pathways in human neutrophils,” Journal of Immunology, vol. 164, no. 1, pp. 350–360, 2000. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Patel, S. Kumar, A. Jyoti et al., “Nitric oxide donors release extracellular traps from human neutrophils by augmenting free radical generation,” Nitric Oxide, vol. 22, no. 3, pp. 226–234, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. M. J. Lapponi, A. Carestia, V. I. Landoni et al., “Regulation of neutrophil extracellular trap formation by anti-inflammatory drugs,” Journal of Pharmacology and Experimental Therapeutics, vol. 345, no. 3, pp. 430–437, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. E. Kolaczkowska and P. Kubes, “Neutrophil recruitment and function in health and inflammation,” Nature Reviews Immunology, vol. 13, no. 3, pp. 159–175, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Futosi, S. Fodor, and A. Mócsai, “Neutrophil cell surface receptors and their intracellular signal transduction pathways,” International Immunopharmacology, vol. 17, no. 3, pp. 638–650, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. T. N. Mayadas, X. Cullere, and C. A. Lowell, “The multifaceted functions of neutrophils,” Annual Review of Pathology, vol. 9, pp. 181–218, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. C. F. Urban, D. Ermert, M. Schmid et al., “Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans,” PLoS Pathogens, vol. 5, no. 10, Article ID e1000639, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Aleyd, M. W. M. van Hout, S. H. Ganzevles et al., “IgA enhances netosis and release of neutrophil extracellular traps by polymorphonuclear cells via FCα receptor I,” The Journal of Immunology, vol. 192, no. 5, pp. 2374–2383, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. J. M. Kelley, P. A. Monach, C. Ji et al., “IgA and IgG antineutrophil cytoplasmic antibody engagement of Fc receptor genetic variants influences granulomatosis with polyangiitis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 51, pp. 20736–20741, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. F. H. Pilsczek, D. Salina, K. K. H. Poon et al., “A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus,” The Journal of Immunology, vol. 185, no. 12, pp. 7413–7425, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. I. Neeli and M. Radic, “Opposition between PKC isoforms regulates histone deimination and neutrophil extracellular chromatin release,” Frontiers in Immunology, vol. 4, article 38, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. J. A. Van Ziffle and C. A. Lowell, “Neutrophil-specific deletion of Syk kinase results in reduced host defense to bacterial infection,” Blood, vol. 114, no. 23, pp. 4871–4882, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. A. C. Newton, “Protein kinase C,” IUBMB life, vol. 60, no. 11, pp. 765–768, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. O. Popa-Nita, S. Proulx, G. Paré, E. Rollet-Labelle, and P. H. Naccache, “Crystal-induced neutrophil activation. XI. Implication and novel roles of classical protein kinase C,” Journal of Immunology, vol. 183, no. 3, pp. 2104–2114, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. V. Jancinova, T. Perecko, R. Nosal, K. Svitekova, and K. Drabikova, “The natural stilbenoid piceatannol decreases activity and accelerates apoptosis of human neutrophils: involvement of protein kinase C,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 136539, 8 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. R. S. Keshari, A. Verma, M. K. Barthwal, and M. Dikshit, “Reactive oxygen species-induced activation of ERK and p38 MAPK mediates PMA-induced NETs release from human neutrophils,” Journal of Cellular Biochemistry, vol. 114, no. 3, pp. 532–540, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. M. J. Zhou and E. J. Brown, “CR3 (Mac-1, αMβ2, CD11b/CD18) and FcγRIII cooperate in generation of a neutrophil respiratory burst: requirement for FcγRIII and tyrosine phosphorylation,” The Journal of Cell Biology, vol. 125, pp. 1407–1416, 1994. View at Google Scholar
  56. A. S. Byrd, X. M. O'Brien, C. M. Johnson, L. M. Lavigne, and J. S. Reichner, “An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans,” The Journal of Immunology, vol. 190, no. 8, pp. 4136–4148, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. E. Gillenius and C. F. Urban, “The adhesive protein invasin of Yersinia pseudotuberculosis induces neutrophil extracellular traps via β1 integrins,” Microbes and Infection, vol. 17, no. 5, pp. 327–336, 2015. View at Publisher · View at Google Scholar
  58. N. Branzk, A. Lubojemska, S. E. Hardison et al., “Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens,” Nature Immunology, vol. 15, no. 11, pp. 1017–1025, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. M. F. Tosi and M. Berger, “Functional differences between the 40 kDa and 50 to 70 kDa IgG Fc receptors on human neutrophils revealed by elastase treatment and antireceptor antibodies,” The Journal of Immunology, vol. 141, no. 6, pp. 2097–2103, 1988. View at Google Scholar · View at Scopus
  60. S. Nagarajan, K. Venkiteswaran, M. Anderson, U. Sayed, C. Zhu, and P. Selvaraj, “Cell-specific, activation-dependent regulation of neutrophil CD32A ligand-binding function,” Blood, vol. 95, no. 3, pp. 1069–1077, 2000. View at Google Scholar · View at Scopus