Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-18T18:15:01.079Z Has data issue: false hasContentIssue false
  • English
  • Français

The intriguing host innate immune response: novel anti-parasitic defence by neutrophil extracellular traps

Published online by Cambridge University Press:  10 April 2014

CARLOS HERMOSILLA ,
TAMARA MUÑOZ CARO ,
LILIANA M. R. SILVA ,
ANTONIO RUIZ  and
ANJA TAUBERT
CARLOS HERMOSILLA*
Affiliation:
Institute of Parasitology, Justus Liebig University Giessen, Giessen, Germany
TAMARA MUÑOZ CARO
Affiliation:
Institute of Parasitology, Justus Liebig University Giessen, Giessen, Germany
LILIANA M. R. SILVA
Affiliation:
ICAAM – Instituto Ciências Agrárias e Ambientais Mediterrânicas, IIFA/Universidade de Évora, Portugal
ANTONIO RUIZ
Affiliation:
Department of Animal Pathology, Parasitology Unit, University of Las Palmas de Gran Canaria, Spain
ANJA TAUBERT
Affiliation:
Institute of Parasitology, Justus Liebig University Giessen, Giessen, Germany
*
* Corresponding author: Institute of Parasitology, Justus Liebig University Giessen, Giessen, Germany. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The capacity of polymorphonuclear neutrophils (PMN) and other leucocytes of the innate immune system to expel their DNA in a controlled process into the extracellular environment to trap and kill pathogenic microorganisms led to a paradigm shift in our comprehension of host leucocyte-pathogen interactions. Formation of neutrophil extracellular traps (NETs) has recently been recognized as a novel effector mechanism of the host innate immune response against microbial infections. Meanwhile evidence has arisen that NET formation is a widely spread mechanism in vertebrates and invertebrates and extends not only to the entrapment of microbes, fungi and viruses but also to the capture of protozoan and metazoan parasites. PMN produce NETs after stimulation with mitogens, cytokines or pathogens in a controlled process which depends on reactive oxygen species (ROS) and the induction of the Raf-MEK-ERK-mediated signalling pathway cascade. NETs consist of nuclear DNA as a backbone decorated with histones, antimicrobial peptides, and PMN-specific granular enzymes thereby providing an extracellular matrix capable of entrapping and killing invasive pathogens. This review is intended to summarize parasite-related data on NETs. Special attention will be given to NET-associated mechanisms by which parasites, in particular apicomplexa, might be hampered in their ability to reproduce within the host cell and complete the life cycle.

Keywords

Neutrophilneutrophil extracellular trapsinnate immunityparasite infectionDNAhistones
Type
Special Issue Article
Information
Parasitology , Volume 141 , Special Issue 11: ApiCOWplexa 2013 – 2nd International Meeting on Apicomplexan Parasites in Farm Animals , September 2014 , pp. 1489 - 1498
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abi Abdallah, D. S. and Denkers, E. Y. (2012). Neutrophils cast extracellular traps in response to protozoan parasites. Frontiers in Immunology 3, 382. doi: 10.3389/fimmu.2012.00382.Google Scholar
Abi Abdallah, D. S., Lin, C., Ball, C. J., King, M. R., Duhamel, G. E. and Denkers, E. Y. (2012). Toxoplasma gondii triggers release of human and mouse neutrophil extracellular traps. Infection and Immunity 80, 768–777. doi: 10.1128/IAI.05730-11.CrossRefGoogle ScholarPubMed
Alghamdi, A. S. and Foster, D. N. (2005). Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps. Biology of Reproduction 73, 1174–1181. doi: 10.1095/biolreprod.105.045666.Google Scholar
Altincicek, B., Stotzel, S., Wygrecka, M., Preissner, K. T. and Vilcinskas, A. (2008). Host-derived extracellular nucleic acids enhance innate immune responses, induce coagulation, and prolong survival upon infection in insects. Journal of Immunology 181, 2705–2712.Google Scholar
Alvar, J., Vélez, I. D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J. and den Boer, M. (2012). Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7, e35671.CrossRefGoogle ScholarPubMed
Ashford, R. W. (2000). The leishmaniases as emerging and reemerging zoonoses. International Journal for Parasitology 30, 1269–1281.CrossRefGoogle ScholarPubMed
Aulik, N. A., Hellenbrand, K. M., Klos, H. and Czuprynski, C. J. (2010). Mannheimia haemolytica and its leukotoxin cause neutrophil extracellular trap formation by bovine neutrophils. Infection and Immunity 78, 4454–4466. doi: 10.1128/IAI.00840-10.Google Scholar
Aulik, N. A., Hellenbrand, K. M. and Czuprynski, C. J. (2012). Mannheimia haemolytica and its leukotoxin cause macrophage extracellular trap formation by bovine macrophages. Infection and Immunity 80, 1923–1933. doi: 10.1128/IAI.06120-11.Google Scholar
Bainton, D. F., Ullyot, J. L. and Farquhar, M. G. (1971). The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. Journal of Experimental Medicine 134, 907–934.Google Scholar
Baker, V. S., Imade, G. E., Molta, N. B., Tawde, P., Pam, S. D., Obadofin, M. O., Sagay, S. A., Egah, D. Z., Iya, D., Afolabi, B. B., Baker, M., Ford, K., Ford, R., Roux, K. H. and Keller, T. C. III (2008). Cytokine-associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age. Malaria Journal 7, 41. doi: 10.1186/1475-2875-7-41.Google Scholar
Behrendt, J. H., Clauss, W., Zahner, H. and Hermosilla, C. (2004). Alternative mechanism of Eimeria bovis sporozoites to invade cells in vitro by breaching the plasma membrane. Journal of Parasitology 90, 1163–1165. doi: 10.1645/GE-3285RN.CrossRefGoogle ScholarPubMed
Behrendt, J. H., Hermosilla, C., Hardt, M., Failing, K., Zahner, H. and Taubert, A. (2008). PMN-mediated immune reactions against Eimeria bovis . Veterinary Parasitology 151, 97–109. doi: 10.1016/j.vetpar.2007.11.013.Google Scholar
Behrendt, J. H., Ruiz, A., Zahner, H., Taubert, A. and Hermosilla, C. (2010). Neutrophil extracellular trap formation as innate immune reactions against the apicomplexan parasite Eimeria bovis . Veterinary Immunology and Immunopathology 133, 1–8. doi: 10.1016/j.vetimm.2009.06.012.CrossRefGoogle ScholarPubMed
Beiter, K., Wartha, F., Albiger, B., Normark, S., Zychlinsky, A. and Henriques-Normark, B. (2006). An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Current Biology 16, 401–407. doi: 10.1016/j.cub.2006.01.056.Google Scholar
Bianchi, M., Hakkim, A., Brinkmann, V., Siler, U., Seger, R. A., Zychlinsky, A. and Reichenbach, J. (2009). Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 114, 2619–2622. doi: 10.1182/blood-2009-05-221606.CrossRefGoogle ScholarPubMed
Bliss, S. K., Marshall, A. J., Zhang, Y. and Denkers, E. Y. (1999). Human polymorphonuclear leukocytes produce IL-12, TNF-alpha, and the chemokines macrophage-inflammatory protein-1 alpha and -1 beta in response to Toxoplasma gondii antigens. Journal of Immunology 162, 7369–7375.Google Scholar
Bliss, S. K., Butcher, B. A. and Denkers, E. Y. (2000). Rapid recruitment of neutrophils containing prestored IL-12 during microbial infection. Journal of Immunology 165, 4515–4521.Google Scholar
Borregaard, N. and Cowland, J. B. (1997). Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89, 3503–3521.Google Scholar
Breman, J. G. and Brandling-Bennett, A. D. (2011). The challenge of malaria eradication in the twenty-first century: research linked to operations is the key. Vaccine 29 (Suppl. 4), D97–D103. doi: 10.1016/j.vaccine.2011.12.003.Google Scholar
Brinkmann, V. and Zychlinsky, A. (2007). Beneficial suicide: why neutrophils die to make NETs. Nature Reviews Microbiology 5, 577–582. doi: 10.1038/nrmicro1710.CrossRefGoogle ScholarPubMed
Brinkmann, V. and Zychlinsky, A. (2012). Neutrophil extracellular traps: is immunity the second function of chromatin? Journal of Cell Biology 198, 773–783. doi: 10.1083/jcb.201203170.Google Scholar
Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y. and Zychlinsky, A. (2004). Neutrophil extracellular traps kill bacteria. Science 303, 1532–1535. doi: 10.1126/science.1092385.Google Scholar
Bruns, S., Kniemeyer, O., Hasenberg, M., Aimanianda, V., Nietzsche, S., Thywissen, A., Jeron, A., Latge, J. P., Brakhage, A. A. and 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 Pathogen 6, e1000873. doi: 10.1371/journal.ppat.1000873.CrossRefGoogle ScholarPubMed
Buchanan, J. T., Simpson, A. J., Aziz, R. K., Liu, G. Y., Kristian, S. A., Kotb, M., Feramisco, J. and Nizet, V. (2006). DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Current Biology 16, 396–400. doi: 10.1016/j.cub.2005.12.039.Google Scholar
Burke, M. L., McManus, D. P., Ramm, G. A., Duke, M., Li, Y., Jones, M. K. and Gobert, G. N. (2010). Temporal expression of chemokines dictates the hepatic inflammatory infiltrate in a murine model of schistosomiasis. PLoS Neglected Tropical Diseases 4, e598. doi: 10.1371/journal.pntd.0000598.CrossRefGoogle Scholar
Chuah, C., Jones, M. K., Burke, M. L., Owen, H. C., Anthony, B. J., Mcmanus, D. P., Ramm, G. A. and Gobert, G. N. (2013). Spatial and temporal transcriptomics of Schistosoma japonicum-induced hepatic granuloma formation reveals novel roles for neutrophils. Journal of Leukocyte Biology 94, 353–365. doi: 10.1189/jlb.1212653.Google Scholar
Chuammitri, P., Ostojic, J., Andreasen, C. B., Redmond, S. B., Lamont, S. J. and Palic, D. (2009). Chicken heterophil extracellular traps (HETs): novel defense mechanism of chicken heterophils. Veterinary Immunology and Immunopathology 129, 126–131. doi: 10.1016/j.vetimm.2008.12.013.Google Scholar
Cogen, A. L., Yamasaki, J., Muto, J., Sanchez, K. M., Alexander, L. C., Tanios, J., Lai, Y., Kim, J. E., Nizet, V. and Gallo, R. (2010). Staphylococcus epidermidis antimicrobial δ-toxin (phenol-soluble modulin-γ) cooperates with host antimicrobial peptides to kill group A Streptococcus . PLoS ONE 5, e8557.Google Scholar
Dabritz, H. A. and Conrad, P. A. (2010). Cats and Toxoplasma: implications for public health. Zoonoses and Public Health 57, 34–52. doi: 10.1111/j.1863-2378.2009.01273.x.Google Scholar
Daugschies, A. and Najdrowski, M. (2005). Eimeriosis in cattle: current understanding. Journal of Veterinary Medicine – Series B – Infectious Diseases and Veterinary Public Health 52, 417–427. doi: 10.1111/j.1439-0450.2005.00894.x.Google Scholar
Dubey, J. P. (2009). History of the discovery of the life cycle of Toxoplasma gondii . International Journal for Parasitology 39, 877–882.Google Scholar
Ermert, D., Urban, C. F., Laube, B., Goosmann, C., Zychlinsky, A. and Brinkmann, V. (2009). Mouse neutrophil extracellular traps in microbial infections. Journal of Innate Immunity 1, 181–193. doi: 10.1159/000205281. CrossRefGoogle ScholarPubMed
Faber, J. E., Kollmann, D., Heise, A., Bauer, C., Failing, K., Burger, H. J. and Zahner, H. (2002). Eimeria infections in cows in the periparturient phase and their calves: oocyst excretion and levels of specific serum and colostrum antibodies. Veterinary Parasitology 104, 1–17.Google Scholar
Friend, S. C. and Stockdale, P. H. (1980). Experimental Eimeria bovis infection in calves: a histopathological study. Canadian Journal of Comparative Medicine 44, 129–140.Google Scholar
Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V. and Zychlinsky, A. (2007). Novel cell death program leads to neutrophil extracellular traps. Journal of Cell Biology 176, 231–241. doi: 10.1083/jcb.200606027.Google Scholar
Gabriel, C., Mcmaster, W. R., Girard, D. and Descoteaux, A. (2010). Leishmania donovani promastigotes evade the antimicrobial activity of neutrophil extracellular traps. Journal of Immunology 185, 4319–4327. doi: 10.4049/jimmunol.1000893.Google Scholar
Grinberg, N., Elazar, S., Rosenshine, I. and Shpigel, N. Y. (2008). Beta-hydroxybutyrate abrogates formation of bovine neutrophil extracellular traps and bactericidal activity against mammary pathogenic Escherichia coli . Infection and Immunity 76, 2802–2807. doi: 10.1128/IAI.00051-08.CrossRefGoogle ScholarPubMed
Guimarães-Costa, A. B., Nascimento, M. T., Froment, G. S., Soares, R. P., Morgado, F. N., Conceicao-Silva, F. and Saraiva, E. M. (2009). Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proceedings of the National Academy of Sciences USA 106, 6748–6753. doi: 10.1073/pnas.0900226106.Google Scholar
Guimarães-Costa, A. B., Nascimento, M. T. C., Wardini, A. B., Pinto-da-Silva, L. H. and Saraiva, E. M. (2011). ETosis: a microbicidal mechanism beyond cell death. Journal of Parasitology Research 2012, 1–11. doi: 10.1155/2012/929743.Google Scholar
Gupta, A. K., Hasler, P., Holzgreve, W., Gebhardt, S. and Hahn, S. (2005). Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Human Immunology 66, 1146–1154. doi: 10.1016/j.humimm.2005.11.003.Google Scholar
Hahn, S., Giaglis, S., Chowdhury, C. S., Hosli, I. and Hasler, P. (2013). Modulation of neutrophil NETosis: interplay between infectious agents and underlying host physiology. Seminars in Immunopathology 35, 439–453. doi: 10.1007/s00281-013-0380-x.Google Scholar
Hakkim, A., Fuchs, T. A., Martinez, N. E., Hess, S., Prinz, H., Zychlinsky, A. and Waldmann, H. (2011). Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Natural Chemical Biology 7, 75–77. doi: 10.1038/nchembio.496.Google Scholar
Hellenbrand, K. M., Forsythe, K. M., Rivera-Rivas, J. J., Czuprynski, C. J. and Aulik, N. A. (2013). Histophilus somni causes extracellular trap formation by bovine neutrophils and macrophages. Microbial Pathogenesis 54, 67–75. doi: 10.1016/j.micpath.2012.09.007.Google Scholar
Hermosilla, C., Zahner, H. and Taubert, A. (2006). Eimeria bovis modulates adhesion molecule gene transcription in and PMN adhesion to infected bovine endothelial cells. International Journal for Parasitology 36, 423–431. doi: 10.1016/j.ijpara.2006.01.001.Google Scholar
Hermosilla, C., Ruiz, A. and Taubert, A. (2012). Eimeria bovis: an update on parasite-host cell interactions. International Journal of Medical Microbiology 302, 210–215. doi: 10.1016/j.ijmm.2012.07.002.CrossRefGoogle ScholarPubMed
Hsu, S. Y., Hsu, H. F., Davis, J. R. and Lust, G. L. (1972). Comparative studies on the lesions caused by eggs of Schistosoma japonicum and Schistosoma mansoni in livers of albino mice and rhesus monkeys. Annals of Tropical Medicine and Parasitology 66, 89–97.Google Scholar
Lippolis, J. D., Reinhardt, T. A., Goff, J. P. and Horst, R. L. (2006). Neutrophil extracellular trap formation by bovine neutrophils is not inhibited by milk. Veterinary Immunology and Immunopathology 113, 248–255. doi: 10.1016/j.vetimm.2006.05.004.Google Scholar
Logters, T., Margraf, S., Altrichter, J., Cinatl, J., Mitzner, S., Windolf, J. and Scholz, M. (2009). The clinical value of neutrophil extracellular traps. Medical Microbiology and Immunology 198, 211–219. doi: 10.1007/s00430-009-0121-x.CrossRefGoogle ScholarPubMed
MacLaren, A. and De Souza, W. (2002). Further studies on the interaction of Toxoplasma gondii with neutrophils and eosinophils. Journal of Submicroscopic Cytology and Pathology 34, 99–104.Google Scholar
Maclaren, A., Attias, M. and De Souza, W. (2004). Aspects of the early moments of interaction between tachyzoites of Toxoplasma gondii with neutrophils. Veterinary Parasitology 125, 301–312. doi: 10.1016/j.vetpar.2004.07.006.Google Scholar
Muñoz Caro, T., Hermosilla, C., Silva, L. M. R., Cortes, H. and Taubert, A. (2014). Neutrophil extracellular traps as innate immune reaction against the emerging apicomplexan parasite Besnoitia besnoiti . PLoS One 9, e91415. doi: 10.1371/journal.pone.0091415.Google Scholar
Mota, M. M., Pradel, G., Vanderberg, J. P., Hafalla, J. C., Frevert, U., Nussenzweig, R. S., Nussenzweig, V. and Rodriguez, A. (2001). Migration of Plasmodium sporozoites through cells before infection. Science 291, 141–144. doi: 10.1126/science.291.5501.141.Google Scholar
Nathan, C. (2006). Neutrophils and immunity: challenges and opportunities. Nature Reviews Immunology 6, 173–182. doi: 10.1038/nri1785.Google Scholar
Palic, D., Ostojic, J., Andreasen, C. B. and Roth, J. A. (2007). Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils. Development and Comparative Immunology 31, 805–816. doi: 10.1016/j.dci.2006.11.010.CrossRefGoogle ScholarPubMed
Ramos-Kichik, V., Mondragon-Flores, R., Mondragon-Castelan, M., Gonzalez-Pozos, S., Muniz-Hernandez, S., Rojas-Espinosa, O., Chacon-Salinas, R., Estrada-Parra, S. and Estrada-Garcia, I. (2009). Neutrophil extracellular traps are induced by Mycobacterium tuberculosis . Tuberculosis (Edinburgh) 89, 29–37. doi: 10.1016/j.tube.2008.09.009.Google Scholar
Ross, A. G., Bartley, P. B., Sleigh, A. C., Olds, G. R., Li, Y., Williams, G. M. and McManus, D. P. (2002). Schistosomiasis. New England Journal of Medicine 346, 1212–1220. doi: 10.1056/NEJMra012396.Google Scholar
Szabady, R. L. and McCormick, B. A. (2013). Control of neutrophil inflammation at mucosal surfaces by secreted epithelial products. Frontiers in Immunology 4, 220. doi: 10.3389/fimmu.2013.00220.Google Scholar
Taubert, A. (2011). Untersuchungen zur zellulären Immunantwort sowie zu wirtszellgebundenen Reaktionen gegen Eimeria bovis-infektionen. VVB Laufersweiler Verlag, 40.Google Scholar
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217–1258.Google Scholar
Urban, C. F., Reichard, U., Brinkmann, V. and Zychlinsky, A. (2006). Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiology 8, 668–676. doi: 10.1111/j.1462-5822.2005.00659.x.Google Scholar
Urban, C. F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., Brinkmann, V., Jungblut, P. R. and Zychlinsky, A. (2009). Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans . PLoS Pathogens 5, Article ID, e1000693.Google Scholar
Von Kockritz-Blickwede, M. and Nizet, V. (2009). Innate immunity turned inside-out: antimicrobial defense by phagocyte extracellular traps. Journal of Molecular Medicine (Berlin, Germany) 87, 775–783. doi: 10.1007/s00109-009-0481-0.Google Scholar
Von Kockritz-Blickwede, M., Goldmann, O., Thulin, P., Heinemann, K., Norrby-Teglund, A., Rohde, M. and Medina, E. (2008). Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111, 3070–3080. doi: 10.1182/blood-2007-07-104018.Google Scholar
Von Lichtenberg, F., Erickson, D. G. and Sadun, E. H. (1973). Comparative histopathology of schistosome granulomas in the hamster. American Journal of Pathology 72, 149–178.Google ScholarPubMed
Wang, Y., Li, M., Stadler, S., Correll, S., Li, P., Wang, D., Hayama, R., Leonelli, L., Han, H., Grigoryev, S. A., Allis, C. D. and Coonrod, S. A. (2009). Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. Journal of Cell Biology 184, 205–213. doi: 10.1083/jcb.200806072.Google Scholar
Wang, Y., Chen, Y., Xin, L., Beverley, S. M., Carlsen, E. D., Popov, V., Chang, K. P., Wang, M. and Soong, L. (2011). Differential microbicidal effects of human histone proteins H2A and H2B on Leishmania promastigotes and amastigotes. Infection and Immunity 79, 1124–1133. doi: 10.1128/IAI.00658-10.Google Scholar
Wardini, A. B., Guimaraes-Costa, A. B., Nascimento, M. T., Nadaes, N. R., Danelli, M. G., Mazur, C., Benjamim, C. F., Saraiva, E. M. and Pinto-Da-Silva, L. H. (2010). Characterization of neutrophil extracellular traps in cats naturally infected with feline leukemia virus. Journal of General Virology 91, 259–264. doi: 10.1099/vir.0.014613-0.Google Scholar
Wartha, F., Beiter, K., Albiger, B., Fernebro, J., Zychlinsky, A., Normark, S. and Henriques-Normark, B. (2007). Capsule and D-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell Microbiology 9, 1162–1171. doi: 10.1111/j.1462-5822.2006.00857.x.Google Scholar
Wilson, C. B. and Remington, J. S. (1979). Activity of human blood leukocytes against Toxoplasma gondii . Journal of Infectious Diseases 140, 890–895.Google Scholar
Yipp, B. G., Petri, B., Salina, D., Jenne, C. N., Scott, B. N., Zbytnuik, L. D., Pittman, K., Asaduzzaman, M., Wu, K., Meijndert, H. C., Malawista, S. E., De Boisfleury Chevance, A., Zhang, K., Conly, J. and Kubes, P. (2012). Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo . Nature Medicine 18, 1386–1393. doi: 10.1038/nm.2847.Google Scholar
Yousefi, S., Gold, J. A., Andina, N., Lee, J. J., Kelly, A. M., Kozlowski, E., Schmid, I., Straumann, A., Reichenbach, J., Gleich, G. J. and Simon, H. U. (2008). Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nature Medicine 14, 949–953. doi: 10.1038/nm.1855.Google Scholar
Yousefi, S., Mihalache, C., Kozlowski, E., Schmid, I. and Simon, H. U. (2009). Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death and Differentiation 16, 1438–1444. doi: 10.1038/cdd.2009.96.Google Scholar