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Mediators of Inflammation
Volume 2016 (2016), Article ID 5898074, 13 pages
http://dx.doi.org/10.1155/2016/5898074
Review Article

Far beyond Phagocytosis: Phagocyte-Derived Extracellular Traps Act Efficiently against Protozoan Parasites In Vitro and In Vivo

1Institute of Parasitology, Justus Liebig University Giessen, 35392 Giessen, Germany
2Laboratory of Molecular Pharmacology, Institute of Pharmacology and Morphophysiology, Faculty of Veterinary Sciences, University Austral of Chile, Valdivia, Chile

Received 1 April 2016; Revised 2 June 2016; Accepted 5 June 2016

Academic Editor: Edecio Cunha-Neto

Copyright © 2016 Liliana M. R. Silva 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. W. Segal, “How neutrophils kill microbes,” Annual Review of Immunology, vol. 23, pp. 197–223, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Faurschou and N. Borregaard, “Neutrophil granules and secretory vesicles in inflammation,” Microbes and Infection, vol. 5, no. 14, pp. 1317–1327, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. D. F. Bainton, J. L. Ullyot, and M. G. Farquhar, “The development of neutrophilic polymorphonuclear leukocytes in human bone marrow,” The Journal of Experimental Medicine, vol. 134, no. 4, pp. 907–934, 1971. View at Publisher · View at Google Scholar · View at Scopus
  4. N. Borregaard and J. B. Cowland, “Granules of the human neutrophilic polymorphonuclear leukocyte,” Blood, vol. 89, no. 10, pp. 3503–3521, 1997. View at Google Scholar · View at Scopus
  5. C. Nathan, “Neutrophils and immunity: challenges and opportunities,” Nature Reviews Immunology, vol. 6, no. 3, pp. 173–182, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Hermosilla, T. M. Caro, L. M. R. Silva, A. Ruiz, and A. Taubert, “The intriguing host innate immune response: Novel anti-parasitic defence by neutrophil extracellular traps,” Parasitology, vol. 141, no. 11, pp. 1489–1498, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. D. M. Underhill and A. Ozinsky, “Phagocytosis of microbes: complexity in action,” Annual Review of Immunology, vol. 20, pp. 825–852, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. O. Soehnlein, “Direct and alternative antimicrobial mechanisms of neutrophil-derived granule proteins,” Journal of Molecular Medicine, vol. 87, no. 12, pp. 1157–1164, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. U. Gullberg, E. Andersson, D. Garwicz, A. Lindmark, and I. Olsson, “Biosynthesis, processing and sorting of neutrophil proteins: insight into neutrophil granule development,” European Journal of Haematology, vol. 58, no. 3, pp. 137–153, 1997. View at Google Scholar · View at Scopus
  10. N. Borregaard, O. E. Sørensen, and K. Theilgaard-Mönch, “Neutrophil granules: a library of innate immunity proteins,” Trends in Immunology, vol. 28, no. 8, pp. 340–345, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. S. K. Bliss, A. J. Marshall, Y. Zhang, and E. Y. Denkers, “Human polymorphonuclear leukocytes produce IL-12, TNF-α, and the chemokines macrophage-inflammatory protein-1α and -1β in response to Toxoplasma gondii antigens,” The Journal of Immunology, vol. 162, no. 12, pp. 7369–7375, 1999. View at Google Scholar · View at Scopus
  12. L. Del Rio, B. A. Butcher, S. Bennouna, S. Hieny, A. Sher, and E. Y. Denkers, “Toxoplasma gondii triggers myeloid differentiation factor 88-dependent IL-12 and chemokine ligand 2 (monocyte chemoattractant protein 1) responses using distinct parasite molecules and host receptors,” The Journal of Immunology, vol. 172, no. 11, pp. 6954–6960, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. J. H. Behrendt, C. Hermosilla, M. Hardt, K. Failing, H. Zahner, and A. Taubert, “PMN-mediated immune reactions against Eimeria bovis,” Veterinary Parasitology, vol. 151, no. 2–4, pp. 97–109, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Muñoz-Caro, M. Lendner, A. Daugschies, C. Hermosilla, and A. Taubert, “NADPH oxidase, MPO, NE, ERK1/2, p38 MAPK and Ca2+ influx are essential for Cryptosporidium parvum-induced NET formation,” Developmental and Comparative Immunology, vol. 52, no. 2, pp. 245–254, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Maksimov, C. Hermosilla, S. Kleinertz, J. Hirzmann, and A. Taubert, “Besnoitia besnoiti infections activate primary bovine endothelial cells and promote PMN adhesion and NET formation under physiological flow condition,” Parasitology Research, vol. 115, no. 5, pp. 1991–2001, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Kato and S. Kitagawa, “Regulation of neutrophil functions by proinflammatory cytokines,” International Journal of Hematology, vol. 84, no. 3, pp. 205–209, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Hachicha, P. Rathanaswami, P. H. Naccache, and S. R. McColl, “Regulation of chemokine gene expression in human peripheral blood neutrophils phagocytosing microbial pathogens,” Journal of Immunology, vol. 160, no. 1, pp. 449–454, 1998. View at Google Scholar · View at Scopus
  18. O. Soehnlein, E. Kenne, P. Rotzius, E. E. Eriksson, and L. Lindbom, “Neutrophil secretion products regulate anti-bacterial activity in monocytes and macrophages,” Clinical and Experimental Immunology, vol. 151, no. 1, pp. 139–145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. O. Soehnlein, “An elegant defense: how neutrophils shape the immune response,” Trends in Immunology, vol. 30, no. 11, pp. 511–512, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. N. Borregaard, “Neutrophils, from marrow to microbes,” Immunity, vol. 33, no. 5, pp. 657–670, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. M. A. Cassatella, S. Gasperini, F. Calzetti, A. Bertagnin, A. D. Luster, and P. P. McDonald, “Regulated production of the interferon-γ-inducible protein-l0 (IP-10) chemokine by human neutrophils,” European Journal of Immunology, vol. 27, no. 1, pp. 111–115, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Schorn, C. Janko, M. Latzko, R. Chaurio, G. Schett, and M. Herrmann, “Monosodium urate crystals induce extracellular DNA traps in neutrophils, eosinophils, and basophils but not in mononuclear cells,” Frontiers in Immunology, vol. 3, article 277, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Muñoz-Caro, S. J. Mena Huertas, I. Conejeros et al., “Eimeria bovis-triggered neutrophil extracellular trap formation is CD11b-, ERK 1/2-, p38 MAP kinase- and SOCE-dependent,” Veterinary Research, vol. 46, article 23, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. L. M. R. Silva, T. Muñoz Caro, R. Gerstberger et al., “The apicomplexan parasite Eimeria arloingi induces caprine neutrophil extracellular traps,” Parasitology Research, vol. 113, no. 8, pp. 2797–2807, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. D. S. Abi Abdallah, C. Lin, C. J. Ball, M. R. King, G. E. Duhamel, and E. Y. Denkers, “Toxoplasma gondii triggers release of human and mouse neutrophil extracellular traps,” Infection and Immunity, vol. 80, no. 2, pp. 768–777, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Reichel, T. Muñoz-Caro, G. Sanchez Contreras et al., “Harbour seal (Phoca vitulina) PMN and monocytes release extracellular traps to capture the apicomplexan parasite Toxoplasma gondii,” Developmental and Comparative Immunology, vol. 50, no. 2, pp. 106–115, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Muñoz-Caro, L. Machado Ribeiro da Silva, Z. Rentería-Solis, A. Taubert, and C. Hermosilla, “Neutrophil extracellular traps in the intestinal mucosa of Eimeria-infected animals,” Asian Pacific Journal of Tropical Biomedicine, vol. 6, no. 4, pp. 301–307, 2016. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Muñoz-Caro, L. M. R. Silva, C. Ritter, A. Taubert, and C. Hermosilla, “ Besnoitia besnoiti tachyzoites induce monocyte extracellular trap formation,” Parasitology Research, vol. 113, no. 11, pp. 4189–4197, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. N. C. Rochael, A. B. Guimarães-Costa, M. T. C. Nascimento et al., “Classical ROS-dependent and early/rapid ROS-independent release of Neutrophil extracellular traps triggered by Leishmania parasites,” Scientific Reports, vol. 5, Article ID 18302, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Sousa-Rocha, M. Thomaz-Tobias, L. F. A. Diniz, P. S. S. Souza, P. Pinge-Filho, and K. A. Toledo, “Trypanosoma cruzi and its soluble antigens induce NET release by stimulating toll-like receptors,” PLoS ONE, vol. 10, no. 10, Article ID e0139569, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. 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
  32. T. Lögters, S. Margraf, J. Altrichter et al., “The clinical value of neutrophil extracellular traps,” Medical Microbiology and Immunology, vol. 198, no. 4, pp. 211–219, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. O. Z. Cheng and N. Palaniyar, “NET balancing: a problem in inflammatory lung diseases,” Frontiers in Immunology, vol. 4, article 1, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Hahn, S. Giaglis, C. S. Chowdury, I. Hösli, and P. Hasler, “Modulation of neutrophil NETosis: interplay between infectious agents and underlying host physiology,” Seminars in Immunopathology, vol. 35, no. 4, pp. 439–453, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Hahn, S. Giaglis, I. Hoesli, and P. Hasler, “Neutrophil NETs in reproduction: from infertility to preeclampsia and the possibility of fetal loss,” Frontiers in Immunology, vol. 3, article 362, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. M. R. Rebordão, C. Carneiro, G. Alexandre-Pires et al., “Neutrophil extracellular traps formation by bacteria causing endometritis in the mare,” Journal of Reproductive Immunology, vol. 106, pp. 41–49, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Wartha, K. Beiter, S. Normark, and B. Henriques-Normark, “Neutrophil extracellular traps: casting the NET over pathogenesis,” Current Opinion in Microbiology, vol. 10, no. 1, pp. 52–56, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. 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
  39. K. Beiter, F. Wartha, B. Albiger, S. Normark, A. Zychlinsky, and B. Henriques-Normark, “An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps,” Current Biology, vol. 16, no. 4, pp. 401–407, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. S. R. Clark, A. C. Ma, S. A. Tavener et al., “Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood,” Nature Medicine, vol. 13, no. 4, pp. 463–469, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. N. A. Aulik, K. M. Hellenbrand, H. Klos, and C. J. Czuprynski, “Mannheimia haemolytica and its leukotoxin cause neutrophil extracellular trap formation by bovine neutrophils,” Infection and Immunity, vol. 78, no. 11, pp. 4454–4466, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. C. F. Urban, U. Reichard, V. Brinkmann, and A. Zychlinsky, “Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms,” Cellular Microbiology, vol. 8, no. 4, pp. 668–676, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. 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
  44. 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,” Journal of Immunology, vol. 190, no. 8, pp. 4136–4148, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. T. H. Ng, S.-H. Chang, M.-H. Wu, and H.-C. Wang, “Shrimp hemocytes release extracellular traps that kill bacteria,” Developmental and Comparative Immunology, vol. 41, no. 4, pp. 644–651, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Narasaraju, E. Yang, R. P. Samy et al., “Excessive neutrophils and neutrophil extracellular traps contribute to acute lung injury of influenza pneumonitis,” American Journal of Pathology, vol. 179, no. 1, pp. 199–210, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. C. N. Jenne and P. Kubes, “NETs tangle with HIV,” Cell Host and Microbe, vol. 12, no. 1, pp. 5–7, 2012. View at Publisher · View at Google Scholar
  48. C. N. Jenne and P. Kubes, “Virus-induced NETs—critical component of host defense or pathogenic mediator?” PLoS Pathogens, vol. 11, no. 1, Article ID e1004546, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Saitoh, J. Komano, Y. Saitoh et al., “Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1,” Cell Host & Microbe, vol. 12, no. 1, pp. 109–116, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. V. S. Baker, G. E. Imade, N. B. Molta et al., “Cytokine-associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age,” Malaria Journal, vol. 7, article 41, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. A. B. Guimarães-Costa, M. T. C. Nascimento, G. S. Froment et al., “Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 16, pp. 6748–6753, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. J. H. Behrendt, A. Ruiz, H. Zahner, A. Taubert, and C. Hermosilla, “Neutrophil extracellular trap formation as innate immune reactions against the apicomplexan parasite Eimeria bovis,” Veterinary Immunology and Immunopathology, vol. 133, no. 1, pp. 1–8, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Bonne-Année, L. A. Kerepesi, J. A. Hess et al., “Extracellular traps are associated with human and mouse neutrophil and macrophage mediated killing of larval Strongyloides stercoralis,” Microbes and Infection, vol. 16, no. 6, pp. 502–511, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. 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
  55. T. Muñoz-Caro, M. C. Rubio R, L. M. R. Silva et al., “Leucocyte-derived extracellular trap formation significantly contributes to Haemonchus contortus larval entrapment,” Parasites and Vectors, vol. 8, article 607, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Yousefi, C. Mihalache, E. Kozlowski, I. Schmid, and H. U. Simon, “Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps,” Cell Death and Differentiation, vol. 16, no. 11, pp. 1438–1444, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Martinelli, M. Urosevic, A. Baryadel et al., “Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation,” Journal of Biological Chemistry, vol. 279, no. 42, pp. 44123–44132, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Caudrillier, K. Kessenbrock, B. M. Gilliss et al., “Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury,” The Journal of Clinical Investigation, vol. 122, no. 7, pp. 2661–2671, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. T. Muñoz Caro, C. Hermosilla, L. M. R. Silva, H. Cortes, and A. Taubert, “Neutrophil extracellular traps as innate immune reaction against the emerging apicomplexan parasite Besnoitia besnoiti,” PloS ONE, vol. 9, no. 3, Article ID e91415, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Nishinaka, T. Arai, S. Adachi, A. Takaori-Kondo, and K. Yamashita, “Singlet oxygen is essential for neutrophil extracellular trap formation,” Biochemical and Biophysical Research Communications, vol. 413, no. 1, pp. 75–79, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. L. Pijanowski, M. Scheer, B. M. L. Verburg-van Kemenade, and M. Chadzinska, “Production of inflammatory mediators and extracellular traps by carp macrophages and neutrophils in response to lipopolysaccharide and/or interferon-γ2,” Fish and Shellfish Immunology, vol. 42, no. 2, pp. 473–482, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. A. K. Gupta, P. Hasler, W. Holzgreve, S. Gebhardt, and S. Hahn, “Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia,” Human Immunology, vol. 66, no. 11, pp. 1146–1154, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. 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 Publisher · View at Google Scholar · View at Scopus
  64. Y. Wang, M. Li, S. Stadler et al., “Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation,” The Journal of Cell Biology, vol. 184, no. 2, pp. 205–213, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. V. Papayannopoulos, K. D. Metzler, A. Hakkim, and A. Zychlinsky, “Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps,” The Journal of Cell Biology, vol. 191, no. 3, pp. 677–691, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. 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
  67. D. N. Douda, M. A. Khan, H. Grasemann, and N. Palaniyar, “SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx,” Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 9, pp. 2817–2822, 2015. View at Publisher · View at Google Scholar · View at Scopus
  68. 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
  69. R. S. Keshari, A. Jyoti, M. Dubey et al., “Cytokines induced neutrophil extracellular traps formation: implication for the inflammatory disease condition,” PLoS ONE, vol. 7, no. 10, Article ID e48111, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. D. Palić, J. Ostojić, C. B. Andreasen, and J. A. Roth, “Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils,” Developmental and Comparative Immunology, vol. 31, no. 8, pp. 805–816, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. R. A. Burgos, I. Conejeros, M. A. Hidalgo, D. Werling, and C. Hermosilla, “Calcium influx, a new potential therapeutic target in the control of neutrophil-dependent inflammatory diseases in bovines,” Veterinary Immunology and Immunopathology, vol. 143, no. 1-2, pp. 1–10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. A. K. Gupta, S. Giaglis, P. Hasler, and S. Hahn, “Efficient neutrophil extracellular trap induction requires mobilization of both intracellular and extracellular calcium pools and is modulated by cyclosporine A,” PLoS ONE, vol. 9, no. 5, Article ID e97088, 2014. View at Publisher · View at Google Scholar · View at Scopus
  73. P. Li, M. Li, M. R. Lindberg, M. J. Kennett, N. Xiong, and Y. Wang, “PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps,” Journal of Experimental Medicine, vol. 207, no. 9, pp. 1853–1862, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Leshner, S. Wang, C. Lewis et al., “PAD4 mediated histone hypercitrullination induces heterochromatin decondensation and chromatin unfolding to form neutrophil extracellular trap-like structures,” Frontiers in Immunology, vol. 3, article 307, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. V. Brinkmann and A. Zychlinsky, “Neutrophil extracellular traps: is immunity the second function of chromatin?” The Journal of Cell Biology, vol. 198, no. 5, pp. 773–783, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Von Köckritz-Blickwede and V. Nizet, “Innate immunity turned inside-out: antimicrobial defense by phagocyte extracellular traps,” Journal of Molecular Medicine, vol. 87, no. 8, pp. 775–783, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. Y. Arai, Y. Nishinaka, T. Arai et al., “Uric acid induces NADPH oxidase-independent neutrophil extracellular trap formation,” Biochemical and Biophysical Research Communications, vol. 443, no. 2, pp. 556–561, 2014. View at Publisher · View at Google Scholar
  78. N. Grinberg, S. Elazar, I. Rosenshine, and N. Y. Shpigel, “β-Hydroxybutyrate abrogates formation of bovine neutrophil extracellular traps and bactericidal activity against mammary pathogenic Escherichia coli,” Infection and Immunity, vol. 76, no. 6, pp. 2802–2807, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. V. Ramos-Kichik, R. Mondragón-Flores, M. Mondragón-Castelán et al., “Neutrophil extracellular traps are induced by Mycobacterium tuberculosis,” Tuberculosis, vol. 89, no. 1, pp. 29–37, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. N. A. Aulik, K. M. Hellenbrand, and C. J. Czuprynski, “Mannheimia haemolytica and its leukotoxin cause macrophage extracellular trap formation by bovine macrophages,” Infection and Immunity, vol. 80, no. 5, pp. 1923–1933, 2012. View at Publisher · View at Google Scholar · View at Scopus
  81. K. M. Hellenbrand, K. M. Forsythe, J. J. Rivera-Rivas, C. J. Czuprynski, and N. A. Aulik, “Histophilus somni causes extracellular trap formation by bovine neutrophils and macrophages,” Microbial Pathogenesis, vol. 54, no. 1, pp. 67–75, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. D. M. Boe, B. J. Curtis, M. M. Chen, J. A. Ippolito, and E. J. Kovacs, “Extracellular traps and macrophages: new roles for the versatile phagocyte,” Journal of Leukocyte Biology, vol. 97, no. 6, pp. 1023–1035, 2015. View at Publisher · View at Google Scholar · View at Scopus
  83. O. A. Chow, M. von Köckritz-Blickwede, A. T. Bright et al., “Statins enhance formation of phagocyte extracellular traps,” Cell Host and Microbe, vol. 8, no. 5, pp. 445–454, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Von Köckritz-Blickwede, O. Goldmann, P. Thulin et al., “Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation,” Blood, vol. 111, no. 6, pp. 3070–3080, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. A. M. Lin, C. J. Rubin, R. Khandpur et al., “Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis,” Journal of Immunology, vol. 187, no. 1, pp. 490–500, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Yousefi, J. A. Gold, N. Andina et al., “Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense,” Nature Medicine, vol. 14, no. 9, pp. 949–953, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. R. Dworski, H.-U. Simon, A. Hoskins, and S. Yousefi, “Eosinophil and neutrophil extracellular DNA traps in human allergic asthmatic airways,” Journal of Allergy and Clinical Immunology, vol. 127, no. 5, pp. 1260–1266, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Morshed, R. Hlushchuk, D. Simon et al., “NADPH oxidase-independent formation of extracellular DNA traps by basophils,” Journal of Immunology, vol. 192, no. 11, pp. 5314–5323, 2014. View at Publisher · View at Google Scholar · View at Scopus
  89. S. E. Malawista, G. Van Blaricom, and M. G. Breitenstein, “Cryopreservable neutrophil surrogates. Stored cytoplasts from human polymorphonuclear leukocytes retain chemotactic, phagocytic, and microbicidal function,” Journal of Clinical Investigation, vol. 83, no. 2, pp. 728–732, 1989. View at Publisher · View at Google Scholar · View at Scopus
  90. 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
  91. C. Schauer, C. Janko, L. E. Munoz et al., “Aggregated neutrophil extracellular traps limit inflammation by degrading cytokines and chemokines,” Nature Medicine, vol. 20, no. 5, pp. 511–517, 2014. View at Publisher · View at Google Scholar · View at Scopus
  92. WHO, World Malaria Report 2014, World Health Organization, Geneva, Switzerland, 2014.
  93. M. Waisberg, A. Molina-Cruz, D. M. Mizurini et al., “Plasmodium falciparum infection induces expression of a mosquito salivary protein (Agaphelin) that targets neutrophil function and inhibits thrombosis without impairing hemostasis,” PLoS Pathogens, vol. 10, no. 9, Article ID e1004338, 2014. View at Publisher · View at Google Scholar · View at Scopus
  94. H. D. Chapman, “Milestones in avian coccidiosis research: a review,” Poultry Science, vol. 93, no. 3, pp. 501–511, 2014. View at Publisher · View at Google Scholar · View at Scopus
  95. C. Hermosilla, B. Barbisch, A. Heise, S. Kowalik, and H. Zahner, “Development of Eimeria boris in vitro: suitability of several bovine, human and porcine endothelial cell lines, bovine fetal gastrointestinal, Madin-Darby bovine kidney (MDBK) and African green monkey kidney (VERO) cells,” Parasitology Research, vol. 88, no. 4, pp. 301–307, 2002. View at Publisher · View at Google Scholar · View at Scopus
  96. C. Hermosilla, H.-J. Bürger, and H. Zahner, “T cell responses in calves to a primary Eimeria bovis infection: phenotypical and functional changes,” Veterinary Parasitology, vol. 84, no. 1-2, pp. 49–64, 1999. View at Publisher · View at Google Scholar · View at Scopus
  97. A. Daugschies and M. Najdrowski, “Eimeriosis in cattle: current understanding,” Journal of Veterinary Medicine Series B: Infectious Diseases and Veterinary Public Health, vol. 52, no. 10, pp. 417–427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  98. J.-E. Faber, D. Kollmann, A. Heise et al., “Eimeria infections in cows in the periparturient phase and their calves: oocyst excretion and levels of specific serum and colostrum antibodies,” Veterinary Parasitology, vol. 104, no. 1, pp. 1–17, 2002. View at Publisher · View at Google Scholar · View at Scopus
  99. A. Ruiz, J. F. González, E. Rodríguez et al., “Influence of climatic and management factors on Eimeria infections in goats from semi-arid zones,” Journal of Veterinary Medicine Series B: Infectious Diseases and Veterinary Public Health, vol. 53, no. 8, pp. 399–402, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. A. K. Soe and W. E. Pomroy, “New species of Eimeria (Apicomplexa: Eimeriidae) from the domesticated goat Capra hircus in New Zealand,” Systematic Parasitology, vol. 23, no. 3, pp. 195–202, 1992. View at Publisher · View at Google Scholar · View at Scopus
  101. H. Mehlhorn and P. M. Armstrong, Encyclopedic Reference of Parasitology: Biology, Structure, Function, Springer, Berlin, Germany, 2001.
  102. L. M. Silva, M. J. Vila-Viçosa, T. Nunes, A. Taubert, C. Hermosilla, and H. C. Cortes, “Eimeria infections in goats in Southern Portugal,” Revista Brasileira de Parasitologia Veterinária, vol. 23, no. 2, pp. 280–286, 2014. View at Publisher · View at Google Scholar
  103. M. A. Taylor and J. Catchpole, “Review article: coccidiosis of domestic ruminants,” Applied Parasitology, vol. 35, no. 2, pp. 73–86, 1994. View at Google Scholar · View at Scopus
  104. S. C. E. Friend and P. H. G. Stockdale, “Experimental Eimeria bovis infection in calves: a histopathological study,” Canadian Journal of Comparative Medicine, vol. 44, no. 2, pp. 129–140, 1980. View at Google Scholar · View at Scopus
  105. A. Ruiz, L. Matos, M. C. Muñoz et al., “Isolation of an Eimeria ninakohlyakimovae field strain (Canary Islands) and analysis of its infection characteristics in goat kids,” Research in Veterinary Science, vol. 94, no. 2, pp. 277–284, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. G. M. Mesfin, J. E. C. Bellamy, and P. H. G. Stockdale, “The pathological changes caused by Eimeria falciformis var pragensis in mice,” Canadian Journal of Comparative Medicine, vol. 42, no. 4, pp. 496–510, 1978. View at Google Scholar · View at Scopus
  107. U. Gadde, H. D. Chapman, T. Rathinam, and G. F. Erf, “Cellular immune responses, chemokine, and cytokine profiles in Turkey poults following infection with the intestinal parasite Eimeria adenoeides,” Poultry Science, vol. 90, no. 10, pp. 2243–2250, 2011. View at Publisher · View at Google Scholar · View at Scopus
  108. R. L. Szabady and B. A. McCormick, “Control of neutrophil inflammation at mucosal surfaces by secreted epithelial products,” Frontiers in Immunology, vol. 4, article 220, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. R. Sumagin, A. Z. Robin, A. Nusrat, and C. A. Parkos, “Transmigrated neutrophils in the intestinal lumen engage ICAM-1 to regulate the epithelial barrier and neutrophil recruitment,” Mucosal Immunology, vol. 7, no. 4, pp. 905–915, 2014. View at Publisher · View at Google Scholar · View at Scopus
  110. A. Hosseinzadeh, P. K. Messer, and C. F. Urban, “Stable redox-cycling nitroxidetempol inhibits NET formation,” Frontiers in Immunology, vol. 3, article 391, 2012. View at Publisher · View at Google Scholar · View at Scopus
  111. A. Taubert, J. H. Behrendt, A. Sühwold, H. Zahner, and C. Hermosilla, “Monocyte- and macrophage-mediated immune reactions against Eimeria bovis,” Veterinary Parasitology, vol. 164, no. 2–4, pp. 141–153, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. C. Chuah, M. K. Jones, M. L. Burke, D. P. Mcmanus, H. C. Owen, and G. N. Gobert, “Defining a pro-inflammatory neutrophil phenotype in response to schistosome eggs,” Cellular Microbiology, vol. 16, no. 11, pp. 1666–1677, 2014. View at Publisher · View at Google Scholar · View at Scopus
  113. C. Chuah, M. K. Jones, M. L. Burke et al., “Spatial and temporal transcriptomics of Schistosoma japonicum-induced hepatic granuloma formation reveals novel roles for neutrophils,” Journal of Leukocyte Biology, vol. 94, no. 2, pp. 353–365, 2013. View at Publisher · View at Google Scholar · View at Scopus
  114. D. Hill and J. P. Dubey, “Toxoplasma gondii: transmission, diagnosis, and prevention,” Clinical Microbiology and Infection, vol. 8, no. 10, pp. 634–640, 2002. View at Publisher · View at Google Scholar · View at Scopus
  115. J. P. Dubey, “History of the discovery of the life cycle of Toxoplasma gondii,” International Journal for Parasitology, vol. 39, no. 8, pp. 877–882, 2009. View at Publisher · View at Google Scholar · View at Scopus
  116. A. M. Tenter, A. R. Heckeroth, and L. M. Weiss, “Toxoplasma gondii: from animals to humans,” International Journal for Parasitology, vol. 30, no. 12-13, pp. 1217–1258, 2000. View at Publisher · View at Google Scholar · View at Scopus
  117. S. K. Bliss, B. A. Butcher, and E. Y. Denkers, “Rapid recruitment of neutrophils containing prestored IL-12 during microbial infection,” Journal of Immunology, vol. 165, no. 8, pp. 4515–4521, 2000. View at Publisher · View at Google Scholar · View at Scopus
  118. A. MacLaren, M. Attias, and W. De Souza, “Aspects of the early moments of interaction between tachyzoites of Toxoplasma gondii with neutrophils,” Veterinary Parasitology, vol. 125, no. 3-4, pp. 301–312, 2004. View at Publisher · View at Google Scholar · View at Scopus
  119. A. MacLaren and W. De Souza, “Further studies on the interaction of Toxoplasma gondii with neutrophils and eosinophils,” Journal of Submicroscopic Cytology and Pathology, vol. 34, no. 1, pp. 99–104, 2002. View at Google Scholar · View at Scopus
  120. D. S. Abi Abdallah and E. Y. Denkers, “Neutrophils cast extracellular traps in response to protozoan parasites,” Frontiers in Immunology, vol. 3, article 382, 2012. View at Publisher · View at Google Scholar · View at Scopus
  121. K. S. Harker, N. Ueno, T. Wang, C. Bonhomme, W. Liu, and M. B. Lodoen, “Toxoplasma gondii modulates the dynamics of human monocyte adhesion to vascular endothelium under fluidic shear stress,” Journal of Leukocyte Biology, vol. 93, no. 5, pp. 789–800, 2013. View at Publisher · View at Google Scholar · View at Scopus
  122. N. Ueno, K. S. Harker, E. V. Clarke et al., “Real-time imaging of Toxoplasma-infected human monocytes under fluidic shear stress reveals rapid translocation of intracellular parasites across endothelial barriers,” Cellular Microbiology, vol. 16, no. 4, pp. 580–595, 2014. View at Publisher · View at Google Scholar · View at Scopus
  123. J.-H. Quan, W. Zhou, G.-H. Cha, I.-W. Choi, D.-W. Shin, and Y.-H. Lee, “Kinetics of IL-23 and IL-12 secretion in response to Toxoplasma gondii antigens from THP-1 monocytic cells,” The Korean Journal of Parasitology, vol. 51, no. 1, pp. 85–92, 2013. View at Publisher · View at Google Scholar · View at Scopus
  124. J. P. Dubey, E. van Wilpe, D. J. C. Blignaut, G. Schares, and J. H. Williams, “Development of early tissue cysts and associated pathology of Besnoitia besnoiti in a naturally infected bull (Bos taurus) from South Africa,” Journal of Parasitology, vol. 99, no. 3, pp. 459–466, 2013. View at Publisher · View at Google Scholar · View at Scopus
  125. G. Schares, W. Basso, M. Majzoub et al., “Evaluation of a commercial ELISA for the specific detection of antibodies against Besnoitia besnoiti,” Veterinary Parasitology, vol. 175, no. 1-2, pp. 52–59, 2011. View at Publisher · View at Google Scholar · View at Scopus
  126. G. Schares, M. C. Langenmayer, J. C. Scharr et al., “Novel tools for the diagnosis and differentiation of acute and chronic bovine besnoitiosis,” International Journal for Parasitology, vol. 43, no. 2, pp. 143–154, 2013. View at Publisher · View at Google Scholar · View at Scopus
  127. EFSA, “Bovine besnoitiosis: an emerging disease in Europe,” EFSA Journal, vol. 8, no. 2, article 1499, 2010. View at Publisher · View at Google Scholar
  128. G. Álvarez-García, C. F. Frey, L. M. O. Mora, and G. Schares, “A century of bovine besnoitiosis: an unknown disease re-emerging in Europe,” Trends in Parasitology, vol. 29, no. 8, pp. 407–415, 2013. View at Publisher · View at Google Scholar · View at Scopus
  129. 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
  130. M. Saffarzadeh, C. Juenemann, M. A. Queisser et al., “Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones,” PLoS ONE, vol. 7, no. 2, Article ID e32366, 2012. View at Publisher · View at Google Scholar · View at Scopus
  131. C. Carmona-Rivera, W. Zhao, S. Yalavarthi, and M. J. Kaplan, “Neutrophil extracellular traps induce endothelial dysfunction in systemic lupus erythematosus through the activation of matrix metalloproteinase-2,” Annals of the Rheumatic Diseases, vol. 74, no. 7, pp. 1417–1424, 2015. View at Publisher · View at Google Scholar · View at Scopus
  132. J. Etulain, K. Martinod, S. L. Wong, S. M. Cifuni, M. Schattner, and D. D. Wagner, “P-selectin promotes neutrophil extracellular trap formation in mice,” Blood, vol. 126, no. 2, pp. 242–246, 2015. View at Publisher · View at Google Scholar · View at Scopus
  133. M. Lendner and A. Daugschies, “Cryptosporidium infections: molecular advances,” Parasitology, vol. 141, no. 11, pp. 1511–1532, 2014. View at Publisher · View at Google Scholar · View at Scopus
  134. M. Shahiduzzaman and A. Daugschies, “Therapy and prevention of cryptosporidiosis in animals,” Veterinary Parasitology, vol. 188, no. 3-4, pp. 203–214, 2012. View at Publisher · View at Google Scholar · View at Scopus
  135. C. Kourenti, P. Karanis, and H. Smith, “Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt,” Journal of Water and Health, vol. 5, no. 1, pp. 1–38, 2007. View at Publisher · View at Google Scholar · View at Scopus
  136. D. Takeuchi, V. C. Jones, M. Kobayashi, and F. Suzuki, “Cooperative role of macrophages and neutrophils in host antiprotozoan resistance in mice acutely infected with Cryptosporidium parvum,” Infection and Immunity, vol. 76, no. 8, pp. 3657–3663, 2008. View at Publisher · View at Google Scholar · View at Scopus
  137. S. Lacroix-Lamandé, R. Mancassola, M. Naciri, and F. Laurent, “Role of gamma interferon in chemokine expression in the ileum of mice and in a murine intestinal epithelial cell line after Cryptosporidium parvum infection,” Infection and Immunity, vol. 70, no. 4, pp. 2090–2099, 2002. View at Publisher · View at Google Scholar · View at Scopus
  138. J. C. Brazil, R. Liu, R. Sumagin et al., “α3/4 fucosyltransferase 3-dependent synthesis of sialyl lewis A on CD44 variant containing exon 6 mediates polymorphonuclear leukocyte detachment from intestinal epithelium during transepithelial migration,” Journal of Immunology, vol. 191, no. 9, pp. 4804–4817, 2013. View at Publisher · View at Google Scholar · View at Scopus
  139. A. Seper, A. Hosseinzadeh, G. Gorkiewicz et al., “Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases,” PLoS Pathogens, vol. 9, no. 9, Article ID e1003614, 2013. View at Publisher · View at Google Scholar · View at Scopus
  140. C. Alfaro, A. Teijeira, C. Onate et al., “Tumor-produced interleukin-8 attracts human myeloid-derived suppressor cells and elicits extrusion of neutrophil extracellular traps (NETs),” Clinical Cancer Research, 2016. View at Publisher · View at Google Scholar
  141. R. Allam, S. V. R. Kumar, M. N. Darisipudi, and H.-J. Anders, “Extracellular histones in tissue injury and inflammation,” Journal of Molecular Medicine, vol. 92, no. 5, pp. 465–472, 2014. View at Publisher · View at Google Scholar · View at Scopus
  142. R. W. Ashford, “The leishmaniases as emerging and reemerging zoonoses,” International Journal for Parasitology, vol. 30, no. 12-13, pp. 1269–1281, 2000. View at Publisher · View at Google Scholar · View at Scopus
  143. J. Alvar, I. D. Vélez, C. Bern et al., “Leishmaniasis worldwide and global estimates of its incidence,” PLoS ONE, vol. 7, no. 5, Article ID e35671, 2012. View at Publisher · View at Google Scholar · View at Scopus
  144. M. Kolivand, M. Fallah, A. Salehzadeh et al., “An epidemiological study of cutaneous leishmaniasis using active case finding among elementary school students in Pakdasht, Southeast of Tehran, Iran 2013-2014,” Journal of Research in Health Sciences, vol. 15, no. 2, pp. 104–108, 2015. View at Google Scholar · View at Scopus
  145. A. C. Chagas, F. Oliveira, A. Debrabant, J. G. Valenzuela, J. M. C. Ribeiro, and E. Calvo, “Lundep, a sand fly salivary endonuclease increases Leishmania parasite survival in neutrophils and inhibits xiia contact activation in human plasma,” PLoS Pathogens, vol. 10, no. 2, Article ID e1003923, 2014. View at Publisher · View at Google Scholar · View at Scopus
  146. M. Charmoy, F. Auderset, C. Allenbach, and F. Tacchini-Cottier, “The prominent role of neutrophils during the initial phase of infection by Leishmania parasites,” Journal of Biomedicine and Biotechnology, vol. 2010, Article ID 719361, 8 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  147. B. P. Hurrell, S. Schuster, E. Grün et al., “Rapid sequestration of Leishmania mexicana by Neutrophils contributes to the development of chronic lesion,” PLoS Pathogens, vol. 11, no. 5, Article ID e1004929, 2015. View at Publisher · View at Google Scholar · View at Scopus
  148. N. C. Peters, J. G. Egen, N. Secundino et al., “In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies,” Science, vol. 321, no. 5891, pp. 970–974, 2008. View at Publisher · View at Google Scholar · View at Scopus
  149. C. J. Thalhofer, Y. Chen, B. Sudan, L. Love-Homan, and M. E. Wilson, “Leukocytes infiltrate the skin and draining lymph nodes in response to the protozoan Leishmania infantum chagasi,” Infection and Immunity, vol. 79, no. 1, pp. 108–117, 2011. View at Publisher · View at Google Scholar · View at Scopus
  150. C. Gabriel, W. R. McMaster, D. Girard, and A. Descoteaux, “Leishmania donovani promastigotes evade the antimicrobial activity of neutrophil extracellular traps,” Journal of Immunology, vol. 185, no. 7, pp. 4319–4327, 2010. View at Publisher · View at Google Scholar · View at Scopus
  151. F. N. Morgado, M. T. C. Nascimento, E. M. Saraiva et al., “Are neutrophil extracellular traps playing a role in the parasite control in active American tegumentary leishmaniasis lesions?” PLoS ONE, vol. 10, no. 7, Article ID e0133063, 2015. View at Publisher · View at Google Scholar · View at Scopus
  152. A. B. Guimarães-Costa, T. S. DeSouza-Vieira, R. Paletta-Silva, A. L. Freitas-Mesquita, J. R. Meyer-Fernandes, and E. M. Saraiva, “3′-nucleotidase/nuclease activity allows Leishmania parasites to escape killing by neutrophil extracellular traps,” Infection and Immunity, vol. 82, no. 4, pp. 1732–1740, 2014. View at Publisher · View at Google Scholar · View at Scopus
  153. Y. Wang, Y. Chen, L. Xin et al., “Differential microbicidal effects of human histone proteins H2A and H2B on Leishmania promastigotes and amastigotes,” Infection and Immunity, vol. 79, no. 3, pp. 1124–1133, 2011. View at Publisher · View at Google Scholar · View at Scopus
  154. “Chagas disease,” Pan American Health Organization, 2016, http://www.paho.org/hq/index.php?option=com_topics&view=article&id=10&Itemid=40743.
  155. F. Villalta and F. Kierszenbaum, “Host-cell invasion by Trypanosoma cruzi: role of cell surface galactose residues,” Biochemical and Biophysical Research Communications, vol. 119, no. 1, pp. 228–235, 1984. View at Publisher · View at Google Scholar · View at Scopus
  156. T. Luna-Gomes, A. A. Filardy, J. D. B. Rocha et al., “Neutrophils increase or reduce parasite burden in Trypanosoma cruzi-infected macrophages, depending on host strain: role of neutrophil elastase,” PLoS ONE, vol. 9, no. 3, Article ID e90582, 2014. View at Publisher · View at Google Scholar · View at Scopus