Traps and hyper inflammation - new ways that neutrophils promote or hinder survival

British Journal of Haematology

Volumn 164, Issue 2, 2014, Pages 189-199

  Gunzer, Matthias ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

C X C motif chemokine receptor 2 (CXCR2); Chemokine ligand 1; Chemokine ligand 2; Myeloid derived suppressor cells; Neutrophil extracellular traps

Indexed keywords

INTERLEUKIN 17;

ADAPTIVE IMMUNITY; BASEMENT MEMBRANE; CELL ACTIVITY; CELL NUCLEUS; CELL POPULATION; HOST RESISTANCE; HUMAN; INFLAMMATION; LEUKOCYTE ACTIVATION; LEUKOCYTE FUNCTION; LEUKOCYTE MICROPARTICLE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL EXTRACELLULAR TRAP; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; TUMOR GROWTH;

C-X-C MOTIF-CHEMOKINE RECEPTOR 2 (CXCR2); CHEMOKINE LIGAND 1; CHEMOKINE LIGAND 2; MYELOID DERIVED SUPPRESSOR CELLS; NEUTROPHIL EXTRACELLULAR TRAPS;

ANIMALS; CELL MOVEMENT; CELL NUCLEUS; CYTOTOXICITY, IMMUNOLOGIC; EXTRACELLULAR MATRIX; HUMANS; INFLAMMATION; NEUTROPHIL ACTIVATION; NEUTROPHILS; PHAGOCYTOSIS;

EID: 84891629775     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12608     Document Type: Review

References (108)

1. Abi Abdallah, D.S., Lin, C., Ball, C.J., King, M.R., Duhamel, G.E. & Denkers, E.Y. (2012) Toxoplasma gondii triggers release of human and mouse neutrophil extracellular traps. Infection and Immunity, 80, 768-777.
2. Acharyya, S.S., Oskarsson, T., Vanharanta, S., Malladi, S., Kim, J., Morris, P.G., Manova-Todorova, K., Leversha, M., Hogg, N., Seshan, V.E., Norton, L., Brogi, E. & Massague, J. (2012) A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell, 150, 165-178.
3. Autenrieth, S.E., Warnke, P., Wabnitz, G.H., Lucero, E.C., Pasquevich, K.A., Drechsler, D., Gunter, M., Hochweller, K., Novakovic, A., Beer-Hammer, S., Samstag, Y., Hammerling, G.J., Garbi, N. & Autenrieth, I.B. (2012) Depletion of dendritic cells enhances innate anti-bacterial host defense through modulation of phagocyte homeostasis. PLoS Pathogens, 8, e1002552.
4. Behnsen, J., Narang, P., Hasenberg, M., Gunzer, F., Bilitewski, U., Klippel, N., Rohde, M., Brock, M., Brakhage, A.A. & Gunzer, M. (2007) Environmental dimensionality controls the interaction of phagocytes with the pathogenic fungi Aspergillus fumigatus and Candida albicans. PLoS Pathogens, 3, e13.
5. Beiter, K., Wartha, F., Albiger, B., Normark, S., Zychlinsky, A. & Henriques-Normark, B. (2006) An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Current Biology, 16, 401-407.
6. Bennett, C.L., Djulbegovic, B., Norris, L.B. & Armitage, J.O. (2013) Colony-stimulating factors for febrile neutropenia during cancer therapy. New England Journal of Medicine, 368, 1131-1139.
7. Bianchi, M., Hakkim, R.A., Brinkmann, V., Siler, U., Seger, R.A., Zychlinsky, A. & Reichenbach, J. (2009) Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood, 114, 2619-2622.
8. Bonnett, C.R., Cornish, E.J., Harmsen, A.G. & Burritt, J.B. (2006) Early neutrophil recruitment and aggregation in the murine lung inhibit germination of Aspergillus fumigatus conidia. Infection and Immunity, 74, 6528-6539.
9. Brandau, S., Trellakis, S., Bruderek, K., Schmaltz, D., Steller, G., Elian, M., Suttmann, H., Schenck, M., Welling, J., Zabel, P. & Lang, S. (2011) Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. Journal of Leukocyte Biology, 89, 311-317.
10. Brandau, S., Dumitru, C.A. & Lang, S. (2013) Protumor and antitumor functions of neutrophil granulocytes. Seminars in Immunopathology, 35, 163-176.
11. Brandes, M., Klauschen, F., Kuchen, S. & Germain, R.N. (2013) A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell, 154, 197-212.
12. Brinkmann, V. & Zychlinsky, A. (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? Journal of Cell Biology, 198, 773-783.
13. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D.S., Weinrauch, Y. & Zychlinsky, A. (2004) Neutrophil extracellular traps kill bacteria. Science, 303, 1532-1535.
14. von Brühl, M.L., Stark, K., Steinhart, A., Chandraratne, S., Konrad, I., Lorenz, M., Khandoga, A., Tirniceriu, A., Coletti, R., Kollnberger, M., Byrne, R.A., Laitinen, I., Walch, A., Brill, A., Pfeiler, S., Manukyan, D., Braun, S., Lange, P., Riegger, J., Ware, J., Eckart, A., Haidari, S., Rudelius, M., Schulz, C., Echtler, K., Brinkmann, V., Schwaiger, M., Preissner, K.T., Wagner, D.D., Mackman, N., Engelmann, B. & Massberg, S. (2012) Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. Journal of Experimental Medicine, 209, 819-835.
15. Bruns, S., Kniemeyer, O., Hasenberg, M., Aimanianda, V., Nietzsche, S., Thywißen, A., Jeron, A., Latge, J.P., Brakhage, A.A. & Gunzer, M. (2010) Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathogens, 6, e1000873.
16. Campbell, A.M., Kashgarian, M. & Shlomchik, M.J. (2012) NADPH oxidase inhibits the pathogenesis of systemic lupus erythematosus. Science Translational Medicine, 4, 157ra141.
17. Cashen, A., Lopez, S., Gao, F., Calandra, G., MacFarland, R., Badel, K. & DiPersio, J. (2008) A phase II study of plerixafor (AMD3100) plus G-CSF for autologous hematopoietic progenitor cell mobilization in patients with Hodgkin lymphoma. Biology of Blood and Marrow Transplantation, 14, 1253-1261.
18. Caudrillier, A., Kessenbrock, K., Gilliss, B.M., Nguyen, J.X., Marques, M.B., Monestier, M., Toy, P., Werb, Z. & Looney, M.R. (2012) Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. The Journal of Clinical Investigation, 122, 2661-2671.
19. Christin, L., Wysong, D.R., Meshulam, T., Hastey, R., Simons, E.R. & Diamond, R.D. (1998) Human platelets damage Aspergillus fumigatus hyphae and may supplement killing by neutrophils. Infection and Immunity, 66, 1181-1189.
20. Chtanova, T., Schaeffer, M., Han, S.J., van Dooren, G.G., Nollmann, M., Herzmark, P., Chan, S.W., Satija, H., Camfield, K., Aaron, H., Striepen, B. & Robey, E.A. (2008) Dynamics of neutrophil migration in lymph nodes during infection. Immunity, 29, 487-496.
21. Clark, S.R., Ma, A.C., Tavener, S.A., McDonald, B., Goodarzi, Z., Kelly, M.M., Patel, K.D., Chakrabarti, S., McAvoy, E., Sinclair, G.D., Keys, E.M., Allen-Vercoe, E., Devinney, R., Doig, C.J., Green, F.H. & Kubes, P. (2007) Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nature Medicine, 13, 463-469.
22. Conti, H.R., Shen, F., Nayyar, N., Stocum, E., Sun, J.N., Lindemann, M.J., Ho, A.W., Hai, J.H., Yu, J.J., Jung, J.W., Filler, S.G., Masso-Welch, P., Edgerton, M. & Gaffen, S.L. (2009) Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. Journal of Experimental Medicine, 206, 299-311.
23. Dancey, J.T., Deubelbeiss, K.A., Harker, L.A. & Finch, C.A. (1976) Neutrophil kinetics in man. The Journal of Clinical Investigation, 58, 705-715.
24. De Filippo, K., Dudeck, A., Hasenberg, M., Nye, E., von Rooijen, N., Hartmann, K., Gunzer, M., Roers, A. & Hogg, N. (2013) Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation. Blood, 121, 4930-4937.
25. Demers, M., Krause, D.S., Schatzberg, D., Martinod, K., Voorhees, J.R., Fuchs, T.A., Scadden, D.T. & Wagner, D.D. (2012) Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proceedings of the National Academy of Sciences of the United States of America, 109, 13076-13081.
26. Dengler, V., Downey, G.P., Tuder, R.M., Eltzschig, H.K. & Schmidt, E.P. (2013) Neutrophil intercellular communication in acute lung injury. Emerging roles of microparticles and gap junctions. American Journal of Respiratory Cell and Molecular Biology, 49, 1-5.
27. Eash, K.J., Means, J.M., White, D.W. & Link, D.C. (2009) CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood, 113, 4711-4719.
28. Essin, K., Salanova, B., Kettritz, R., Sausbier, M., Luft, F.C., Kraus, D., Bohn, E., Autenrieth, I.B., Peschel, A., Ruth, P. & Gollasch, M. (2007) Large-conductance calcium-activated potassium channel activity is absent in human and mouse neutrophils and is not required for innate immunity. American Journal of Physiology-Cell Physiology, 293, C45-C54.
29. Femling, J.K., Cherny, V.V., Morgan, D., Rada, B., Davis, A.P., Czirjak, G., Enyedi, P., England, S.K., Moreland, J.G., Ligeti, E., Nauseef, W.M. & DeCoursey, T.E. (2006) The antibacterial activity of human neutrophils and eosinophils requires proton channels but not BK channels. Journal of General Physiology, 127, 659-672.
30. Fiore, S. & Serhan, C.N. (1990) Formation of lipoxins and leukotrienes during receptor-mediated interactions of human platelets and recombinant human granulocyte/macrophage colony-stimulating factor-primed neutrophils. Journal of Experimental Medicine, 172, 1451-1457.
31. Flomenberg, N., Devine, S.M., Dipersio, J.F., Liesveld, J.L., McCarty, J.M., Rowley, S.D., Vesole, D.H., Badel, K. & Calandra, G. (2005) The use of AMD3100 plus G-CSF for autologous hematopoietic progenitor cell mobilization is superior to G-CSF alone. Blood, 106, 1867-1874.
32. Fuchs, T.A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V. & Zychlinsky, A. (2007) Novel cell death program leads to neutrophil extracellular traps. Journal of Cell Biology, 176, 231-241.
33. Fuchs, T.A., Kremer Hovinga, J.A., Schatzberg, D., Wagner, D.D. & Lammle, B. (2012) Circulating DNA and myeloperoxidase indicate disease activity in patients with thrombotic microangiopathies. Blood, 120, 1157-1164.
34. Gabrilovich, D.I. & Nagaraj, S. (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nature Reviews Immunology, 9, 162-174.
35. Garcia-Romo, G.S., Caielli, S., Vega, B., Connolly, J., Allantaz, F., Xu, Z., Punaro, M., Baisch, J., Guiducci, C., Coffman, R.L., Barrat, F.J., Banchereau, J. & Pascual, V. (2011) Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Science Translational Medicine, 3, 73ra20.
36. Gasser, O. & Schifferli, J.A. (2004) Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood, 104, 2543-2548.
37. Goodridge, H.S., Reyes, C.N., Becker, C.A., Katsumoto, T.R., Ma, J., Wolf, A.J., Bose, N., Chan, A.S., Magee, A.S., Danielson, M.E., Weiss, A., Vasilakos, J.P. & Underhill, D.M. (2011) Activation of the innate immune receptor Dectin-1 upon formation of a 'phagocytic synapse'. Nature, 472, 471-475.
38. Guimaraes-Costa, A.B., Nascimento, M.T., Froment, G.S., Soares, R.P., Morgado, F.N., Conceicao-Silva, F. & Saraiva, E.M. (2009) Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proceedings of the National Academy of Sciences of the United States of America, 106, 6748-6753.
39. Haak, S., Croxford, A.L., Kreymborg, K., Heppner, F.L., Pouly, S., Becher, B. & Waisman, A. (2009) IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. The Journal of Clinical Investigation, 119, 61-69.
40. Hakkim, A., Furnrohr, B.G., Amann, K., Laube, B., Abed, U.A., Brinkmann, V., Herrmann, M., Voll, R.E. & Zychlinsky, A. (2010) Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proceedings of the National Academy of Sciences of the United States of America, 107, 9813-9818.
41. Hasenberg, M., Köhler, A., Bonifatius, S., Borucki, K., Riek-Burchardt, M., Achilles, J., Männ, L., Baumgart, K., Schraven, B. & Gunzer, M. (2011a) Rapid immunomagnetic negative enrichment of neutrophil granulocytes from murine bone marrow for functional studies in vitro and in vivo. PLoS ONE, 6, e17314.
42. Hasenberg, M., Behnsen, J., Krappmann, S., Brakhage, A. & Gunzer, M. (2011b) Phagocyte responses towards Aspergillus fumigatus. International Journal of Medical Microbiology, 301, 436-444.
43. Hasenberg, M., Köhler, A., Bonifatius, S., Jeron, A. & Gunzer, M. (2011c) Direct observation of phagocytosis and NET-formation by neutrophils in infected lungs using 2-photon microscopy. Journal of Visualized Experiments, 52, p ii, 2659.
44. Hasenberg, M., Stegemann-Koniszewski, S. & Gunzer, M. (2013) Cellular immune reactions in the lung. Immunological Reviews, 251, 189-214.
45. Hirano, Y., Hizume, K., Kimura, H., Takeyasu, K., Haraguchi, T. & Hiraoka, Y. (2012) Lamin B receptor recognizes specific modifications of histone H4 in heterochromatin formation. Journal of Biological Chemistry, 287, 42654-42663.
46. Hirsch, J.G. (1959) Immunity to infectious diseases: review of some concepts of Metchnikoff. Bacteriological Reviews, 23, 48-60.
47. Hoffmann, K., Dreger, C.K., Olins, A.L., Olins, D.E., Shultz, L.D., Lucke, B., Karl, H., Kaps, R., Muller, D., Vaya, A., Aznar, J., Ware, R.E., Sotelo, C.N., Lindner, T.H., Herrmann, H., Reis, A. & Sperling, K. (2002) Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huet anomaly). Nature Genetics, 31, 410-414.
48. Hosseinzadeh, A., Messer, P.K. & Urban, C.F. (2012) Stable redox-cycling nitroxide Tempol inhibits NET formation. Frontiers in Immunology, 3, 391.
49. Hurst, J.K. (2012) What really happens in the neutrophil phagosome? Free Radical Biology and Medicine, 53, 508-520.
50. Jenne, C.N., Wong, C.H., Zemp, F.J., McDonald, B., Rahman, M.M., Forsyth, P.A., McFadden, G. & Kubes, P. (2013) Neutrophils recruited to sites of infection protect from virus challenge by releasing neutrophil extracellular traps. Cell Host & Microbe, 13, 169-180.
51. Kash, J.C., Tumpey, T.M., Proll, S.C., Carter, V., Perwitasari, O., Thomas, M.J., Basler, C.F., Palese, P., Taubenberger, J.K., Garcia-Sastre, A., Swayne, D.E. & Katze, M.G. (2006) Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature, 443, 578-581.
52. Khandpur, R., Carmona-Rivera, C., Vivekanandan-Giri, A., Gizinski, A., Yalavarthi, S., Knight, J.S., Friday, S., Li, S., Patel, R.M., Subramanian, V., Thompson, P., Chen, P., Fox, D.A., Pennathur, S. & Kaplan, M.J. (2013) NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Science Translational Medicine, 5, 178ra40.
53. Kim, J.V., Kang, S.S., Dustin, M.L. & McGavern, D.B. (2009) Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis. Nature, 457, 191-195.
54. Klebanoff, S.J., Kettle, A.J., Rosen, H., Winterbourn, C.C. & Nauseef, W.M. (2013) Myeloperoxidase: a front-line defender against phagocytosed microorganisms. Journal of Leukocyte Biology, 93, 185-198.
55. von Köckritz-Blickwede, M., Goldmann, O., Thulin, P., Heinemann, K., Norrby-Teglund, A., Rohde, M. & Medina, E. (2008) Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood, 111, 3070-3080.
56. Köhler, A., De Filippo, K., Hasenberg, M., van den Brandt, C., Nye, E., Hosking, M.P., Lane, T.E., Männ, L., Ransohoff, R.M., Hauser, A.E., Winter, O., Schraven, B., Geiger, H., Hogg, N. & Gunzer, M. (2011) G-CSF mediated thrombopoietin release triggers neutrophil motility and mobilization from bone marrow via induction of Cxcr2 ligands. Blood, 117, 4349-4357.
57. Kolaczkowska, E. & Kubes, P. (2013) Neutrophil recruitment and function in health and inflammation. Nature Reviews Immunology, 13, 159-175.
58. Kolls, J.K. & Linden, A. (2004) Interleukin-17 family members and inflammation. Immunity, 21, 467-476.
59. Lämmermann, T., Afonso, P.V., Angermann, B.R., Wang, J.M., Kastenmüller, W., Parent, C.A. & Germain, R.N. (2013) Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature, 498, 371-375.
60. Lande, R., Ganguly, D., Facchinetti, V., Frasca, L., Conrad, C., Gregorio, J., Meller, S., Chamilos, G., Sebasigari, R., Riccieri, V., Bassett, R., Amuro, H., Fukuhara, S., Ito, T., Liu, Y.J. & Gilliet, M. (2011) Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Science Translational Medicine, 3, 73ra19.
61. Latimer, K.S., Kircher, I.M., Lindl, P.A., Dawe, D.L. & Brown, J. (1989) Leukocyte function in Pelger-Huet anomaly of dogs. Journal of Leukocyte Biology, 45, 301-310.
62. Leonardi, C., Matheson, R., Zachariae, C., Cameron, G., Li, L., Edson-Heredia, E., Braun, D. & Banerjee, S. (2012) Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. New England Journal of Medicine, 366, 1190-1199.
63. Li, P., Li, M., Lindberg, M.R., Kennett, M.J., Xiong, N. & Wang, Y. (2010) PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. Journal of Experimental Medicine, 207, 1853-1862.
64. Li, K.W., Turner, S.M., Emson, C.L., Hellerstein, M.K. & Dale, D.C. (2011) Deuterium and neutrophil kinetics. Blood, 117, 6052-6053.
65. Manitz, M.P., Horst, B., Seeliger, S., Strey, A., Skryabin, B.V., Gunzer, M., Frings, W., Schonlau, F., Roth, J., Sorg, C. & Nacken, W. (2003) Loss of S100A9 (MRP14) results in reduced interleukin-8-induced CD11b surface expression, a polarized microfilament system, and diminished responsiveness to chemoattractants in vitro. Molecular and Cellular Biology, 23, 1034-1043.
66. Martinod, K., Demers, M., Fuchs, T.A., Wong, S.L., Brill, A., Gallant, M., Hu, J., Wang, Y. & Wagner, D.D. (2013) Neutrophil histone modification by peptidylarginine deiminase 4 is critical for deep vein thrombosis in mice. Proceedings of the National Academy of Sciences of the United States of America, 110, 8674-8679.
67. Massberg, S., Grahl, L., von Bruehl, M.L., Manukyan, D., Pfeiler, S., Goosmann, C., Brinkmann, V., Lorenz, M., Bidzhekov, K., Khandagale, A.B., Konrad, I., Kennerknecht, E., Reges, K., Holdenrieder, S., Braun, S., Reinhardt, C., Spannagl, M., Preissner, K.T. & Engelmann, B. (2010) Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nature Medicine, 16, 887-896.
68. McDonald, B., Pittman, K., Menezes, G.B., Hirota, A.A., Slaba, I., Waterhouse, C.C.M., Beck, P.L., Muruve, D.A. & Kubes, P. (2010) Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science, 330, 362-366.
69. McDonald, B., Urrutia, R., Yipp, B.G., Jenne, C.N. & Kubes, P. (2012) Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host & Microbe, 12, 324-333.
70. Menegazzi, R., Decleva, E. & Dri, P. (2012) Killing by neutrophil extracellular traps: fact or folklore? Blood, 119, 1214-1216.
71. Mocsai, A. (2013) Diverse novel functions of neutrophils in immunity, inflammation, and beyond. Journal of Experimental Medicine, 210, 1283-1299.
72. Nauseef, W.M. (2007) How human neutrophils kill and degrade microbes: an integrated view. Immunological Reviews, 219, 88-102.
73. Nauseef, W.M. (2012) Editorial: Nyet to NETs? A pause for healthy skepticism. Journal of Leukocyte Biology, 91, 353-355.
74. Niesner, R.A., Narang, P., Spiecker, H., Andresen, V., Gericke, K.H. & Gunzer, M. (2008) Selective detection of NADPH oxidase in polymorphonuclear cells by means of NAD(P)H-based fluorescence lifetime imaging. Journal of Biophysics, 2008, Article ID 602639.
75. Norris, B.A., Uebelhoer, L.S., Nakaya, H.I., Price, A.A., Grakoui, A. & Pulendran, B. (2013) Chronic but not acute virus infection induces sustained expansion of myeloid suppressor cell numbers that inhibit viral-specific T cell immunity. Immunity, 38, 309-321.
76. Nunes, P., Cornut, D., Bochet, V., Hasler, U., Oh-Hora, M., Waldburger, J.M. & Demaurex, N. (2012) STIM1 juxtaposes ER to phagosomes, generating Ca(2)(+) hotspots that boost phagocytosis. Current Biology, 22, 1990-1997.
77. Ostrand-Rosenberg, S., Sinha, P., Beury, D.W. & Clements, V.K. (2012) Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Seminars in Cancer Biology, 22, 275-281.
78. Papp, K.A., Leonardi, C., Menter, A., Ortonne, J.P., Krueger, J.G., Kricorian, G., Aras, G., Li, J., Russell, C.B., Thompson, E.H. & Baumgartner, S. (2012) Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. New England Journal of Medicine, 366, 1181-1189.
79. Patel, D.D., Lee, D.M., Kolbinger, F. & Antoni, C. (2013) Effect of IL-17A blockade with secukinumab in autoimmune diseases. Annals of the Rheumatic Diseases, 72(Suppl. 2), ii116-ii123.
80. Peters, N.C., Egen, J.G., Secundino, N., Debrabant, A., Kimblin, N., Kamhawi, S., Lawyer, P., Fay, M.P., Germain, R.N. & Sacks, D. (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science, 321, 970-974.
81. Pillay, J., den Braber I., Vrisekoop, N., Kwast, L.M., de Boer, R.J., Borghans, J.A., Tesselaar, K. & Koenderman, L. (2010) In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood, 116, 625-627.
82. Pillay, J., van, H.E., Visser, T., Tak, T., Lammers, J.W., Ulfman, L.H., Leenen, L.P., Pickkers, P. & Koenderman, L. (2012) A subset of neutrophils in human systemic inflammation inhibits T cell responses through Mac-1. The Journal of Clinical Investigation, 122, 327-336.
83. Proebstl, D., Voisin, M.B., Woodfin, A., Whiteford, J., D'Acquisto, F., Jones, G.E., Rowe, D. & Nourshargh, S. (2012) Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo. Journal of Experimental Medicine, 209, 1219-1234.
84. Puel, A., Cypowyj, S., Bustamante, J., Wright, J.F., Liu, L., Lim, H.K., Migaud, M., Israel, L., Chrabieh, M., Audry, M., Gumbleton, M., Toulon, A., Bodemer, C., El-Baghdadi, J., Whitters, M., Paradis, T., Brooks, J., Collins, M., Wolfman, N.M., Al-Muhsen, S., Galicchio, M., Abel, L., Picard, C. & Casanova, J.L. (2011) Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science, 332, 65-68.
85. Puellmann, K., Kaminski, W.E., Vogel, M., Nebe, C.T., Schroeder, J., Wolf, H. & Beham, A.W. (2006) A variable immunoreceptor in a subpopulation of human neutrophils. Proceedings of the National Academy of Sciences of the United States of America, 103, 14441-14446.
86. Reeves, E.P., Lu, H., Jacobs, H.L., Messina, C.G., Bolsover, S., Gabella, G., Potma, E.O., Warley, A., Roes, J. & Segal, A.W. (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature, 416, 291-297.
87. Remijsen, Q., Kuijpers, T.W., Wirawan, E., Lippens, S., Vandenabeele, P. & Vanden Berghe, T. (2011) Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death and Differentiation, 18, 581-588.
88. Rowat, A.C., Jaalouk, D.E., Zwerger, M., Ung, W.L., Eydelnant, I.A., Olins, D.E., Olins, A.L., Herrmann, H., Weitz, D.A. & Lammerding, J. (2013) Nuclear envelope composition determines the ability of neutrophil-type cells to passage through micron-scale constrictions. Journal of Biological Chemistry, 288, 8610-8618.
89. Sasse, C., Hasenberg, M., Weyler, M., Gunzer, M. & Morschhäuser, J. (2013) White-opaque switching of Candida albicans allows immune evasion in an environment-dependent fashion. Eukaryotic Cell, 12, 50-58.
90. Segal, A.W. (2005) How neutrophils kill microbes. Annual Review of Immunology, 23, 197-223.
91. Springer, T.A. (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell, 76, 301-314.
92. Stein, S., Scholz, S., Schwaeble, J., Sadat, M.A., Modlich, U., Schultze-Strasser, S., Diaz, M., Chen-Wichmann, L., Mueller-Kuller, U., Brendel, C., Fronza, R., Kaufmann, K.B., Naundorf, S., Pech, N.K., Travers, J.B., Matute, J.D., Presson, R.G. Jr, Sandusky, G.E., Kunkel, H., Rudolf, E., Dillmann, A., von, K.C., Kuehlcke, K., Baum, C., Schambach, A., Dinauer, M.C., Schmidt, M. & Grez, M. (2013) From bench to bedside: preclinical evaluation of a SIN gammaretroviral vector for the gene therapy of X-linked chronic granulomatous disease. Human Gene Therapy Clinical Development, 24, 86-98.
93. Steinberg, B.E. & Grinstein, S. (2007) Unconventional roles of the NADPH oxidase: signaling, ion homeostasis, and cell death. Science Signaling, 2007, e11.
94. Stewart, C.L., Roux, K.J. & Burke, B. (2007) Blurring the boundary: the nuclear envelope extends its reach. Science, 318, 1408-1412.
95. Sundd, P., Gutierrez, E., Koltsova, E.K., Kuwano, Y., Fukuda, S., Pospieszalska, M.K., Groisman, A. & Ley, K. (2012) 'Slings' enable neutrophil rolling at high shear. Nature, 488, 399-403.
96. Tak, T., Tesselaar, K., Pillay, J., Borghans, J.A. & Koenderman, L. (2013) What's your age again? Determination of human neutrophil half-lives revisited. Journal of Leukocyte Biology, 94, 595-601.
97. Tittel, A.P., Heuser, C., Ohliger, C., Llanto, C., Yona, S., Hammerling, G.J., Engel, D.R., Garbi, N. & Kurts, C. (2012) Functionally relevant neutrophilia in CD11c diphtheria toxin receptor transgenic mice. Nature Methods, 9, 385-390.
98. Tofts, P.S., Chevassut, T., Cutajar, M., Dowell, N.G. & Peters, A.M. (2011) Doubts concerning the recently reported human neutrophil lifespan of 5.4 days. Blood, 117, 6050-6052.
99. Underhill, D.M. & Goodridge, H.S. (2012) Information processing during phagocytosis. Nature Reviews Immunology, 12, 492-502.
100. Urban, C.F., Reichard, U., Brinkmann, V. & Zychlinsky, A. (2006) Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cellular Microbiology, 8, 668-676.
101. Urban, C.F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., Brinkmann, V., Jungblut, P.R. & Zychlinsky, A. (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathogens, 5, e1000639.
102. Wang, S., Voisin, M.B., Larbi, K.Y., Dangerfield, J., Scheiermann, C., Tran, M., Maxwell, P.H., Sorokin, L. & Nourshargh, S. (2006) Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. Journal of Experimental Medicine, 203, 1519-1532.
103. Wang, K., Lin, B., Lin, J. & Lan, X. (2013) A novel mutation in the myeloperoxidase gene in a Chinese female with complete myeloperoxidase deficiency: the role of nonsense-mediated mRNA decay. Gene, 515, 205-207.
104. Weaver, C.T., Hatton, R.D., Mangan, P.R. & Harrington, L.E. (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annual Review of Immunology, 25, 821-852.
105. Winterbourn, C.C. & Kettle, A.J. (2013) Redox reactions and microbial killing in the neutrophil phagosome. Antioxidants & Redox Signaling, 18, 642-660.
106. Yousefi, S., Gold, J.A., Andina, N., Lee, J.J., Kelly, A.M., Kozlowski, E., Schmid, I., Straumann, A., Reichenbach, J., Gleich, G.J. & Simon, H.U. (2008) Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nature Medicine, 14, 949-953.
107. Zhang, X., Kluger, Y., Nakayama, Y., Poddar, R., Whitney, C., DeTora, A., Weissman, S.M. & Newburger, P.E. (2004) Gene expression in mature neutrophils: early responses to inflammatory stimuli. Journal of Leukocyte Biology, 75, 358-372.
108. Zhou, S.L., Dai, Z., Zhou, Z.J., Wang, X.Y., Yang, G.H., Wang, Z., Huang, X.W., Fan, J. & Zhou, J. (2012) Overexpression of CXCL5 mediates neutrophil infiltration and indicates poor prognosis for hepatocellular carcinoma. Hepatology, 56, 2242-2254.