Sieci zewnątrzkomórkowe - powszechny w świecie zwierząt (i roślin?) mechanizm unieszkodliwiania patogenów

• Authors: Łukasz Pijanowski , Joanna Homa , Magdalena Chadzińska

Title variants

EN

Extracellular traps - general mechanisms of pathogen elimination, in animal (and plant?) kingdom

• Languages of publication: PL EN

Abstracts

PL

Zewnątrzkomórkowe sieci (ET) stanowią ewolucyjnie stary mechanizm obronny, który funkcjonuje zarówno u wyższych kręgowców ze ssakami na czele, jak i u kręgowców zmiennocieplnych np. ryb, bezkręgowców i najprawdopodobniej u roślin. Struktury ET unieruchamiają patogeny, zabezpieczając organizm przed ich rozprzestrzenianiem się i prawdopodobnie prowadzą do śmierci przynajmniej niektórych z nich. W przypadku leukocytów ssaków stwierdzono, że w powstawanie sieci zaangażowane są różne szlaki molekularne i cząsteczki sygnałowe, np. wolne rodniki tlenowe, jony Ca2+ czy kinazy białkowe. Okazuje się, że formowanie sieci przez komórki immunokompetentne w innych grupach organizmów podlega podobnym regulacjom. W większości przypadków, zarówno u kręgowców, jak i bezkręgowców, ważną rolę w tym procesie odgrywa aktywność oksydazy NADPH oraz związana z nią zdolność do przeprowadzenia wybuchu tlenowego. Strategia obronna związana z produkcją ET bazuje na aktywności poszczególnych komponentów sieci. Występują wśród nich DNA, histony, jak również białka o silnych właściwościach bakteriobójczych np. różnego typu proteazy. Dokładny skład tych struktur może być nieco odmienny u organizmów należących do różnych taksonów, jak również w zależności od rodzaju komórek immunokompetentnych wytwarzających sieci.

EN

Extracellular traps (ETs) are an evolutionary old mechanism of defense that functions both in higher vertebrates including mammals, lower vertebrates such as fish, in invertebrates and most probably in plants. ET structures immobilize pathogens, protect the body from their spread and possibly lead to the death of some of them. Traps formation in mammalian leukocytes is a complex process involving several molecular pathways and signaling molecules, such as reactive oxygen species (ROS), Ca2+, or protein kinases. Most probably ET formation in immunocompetent cells of non-mamalian species is subjected to similar regulations. In most cases, both in vertebrates and invertebrates, NADPH oxidase activity and consequently ROS production play an important role in this process. ET defense strategy is based on the activity of their specific components such as DNA, histones and bactericidal proteins e.g. different types of proteases. The exact composition of these structures may be slightly different in organisms belonging to different taxa, as well as depends on the type of immunocompetent cells producing the traps.

Keywords

PL

DNA; ET; histony; leukocyty; zewnątrzkomórkowe sieci

EN

DNA; ET; extracellular traps; histones; leukocytes

• Journal: Kosmos
• Year: 2017
• Volume: 66
• Issue: 4
• Pages: 703-719

Dates

published

2017

Contributors

author

Łukasz Pijanowski

• Zakład Immunologii Ewolucyjnej, Instytut Zoologii i Badań Biomedycznych, Uniwersytet Jagielloński, Gronostajowa 9, 30-387 Kraków, Polska
• Department of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9,, 30-387 Kraków Poland

author

Joanna Homa

• Zakład Immunologii Ewolucyjnej, Instytut Zoologii i Badań Biomedycznych, Uniwersytet Jagielloński, Gronostajowa 9, 30-387 Kraków, Polska
• Department of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9,, 30-387 Kraków Poland

author

Magdalena Chadzińska

• Zakład Immunologii Ewolucyjnej, Instytut Zoologii i Badań Biomedycznych, Uniwersytet Jagielloński, Gronostajowa 9, 30-387 Kraków, Polska
• Department of Evolutionary Immunology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9,, 30-387 Kraków Poland

References

• Alemán O. R., Mora N., Cortes-Vieyra R., Uribe-Querol E., Rosales C., 2016. Differential use of human neutrophil Fcγ receptors for inducing neutrophil extracellular trap formation. J. Immunol. Res. 2016, 2908034.
• Altincicek B., Stötzel S., Wygrecka M., Preissner K.T., Vilcinskas A., 2008. Host-derived extracellular nucleic acids enhance innate immune responses, induce coagulation, and prolong survival upon infection in insects. J. Immunol. 181, 2705-2712.
• Anand P., Cermelli S., Li Z., Kassan A., Bosch M., Sigua R., Huang L., Ouellette A. J., Pol A., Welte M. A., Gross S. P., 2012. A novel role for lipid droplets in the organismal antibacterial response. Elife 1, e00003.
• Arai Y., Nishinaka Y., Arai T., Morita M., Mizugishi K., Adachi S., Takaori-Kondo A., Watanabe T., Yamashita K., 2014. Uric acid induces NADPH oxidase-independent neutrophil extracellular trap formation. Biochem. Biophys. Res. Comm. 443, 556-561.
• Arumugam M., Romestand B., Torreilles J., Roch P., 2000. In vitro production of superoxide and nitric oxide (as nitrite and nitrate) by Mytilus galloprovincialis haemocytes upon incubation with PMA or laminarin or during yeast phagocytosis. Eur. J. Cell Biol. 79, 513-519.
• Aulik N. A., Hellenbrand K. M., Czuprynski C. J., 2012. Mannheimia haemolytica and its leukotoxin causemacrophage extracellular trap formation by bovine macrophages. Infect. Immun. 80, 1923-1933.
• Augusto L. A., Decottignies P., Synguelakis M., Nicaise M., Le Maréchal P., Chaby R., 2003. Histones: a novel class of lipopolysaccharide-binding molecules. Biochemistry 42, 3929-3938.
• Bagust T. J., Jones R. C., Guy J. S., 2000. Avian infectious laryngotracheitis. Rev. Sci. Tech. 19, 483-492.
• Behnen M., Leschczyk C., Möller S., Batel T., Klinger M., Solbach W., Laskay T., 2014. Immobilized immune complexes induce neutrophil extracellular trap release by human neutrophil granulocytes via FcγRIIIB and Mac-1. J. Immunol. 193, 1954-1965.
• Belaaouaj A., 2002. Neutrophil elastase-mediated killing of bacteria: lessons from targeted mutagenesis. Microb. Infect. 4, 1259-1264.
• Bianchi M., Niemiec M. J., Siler U., Urban C. F., Reichenbach J., 2011. Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J. Allergy Clin. Immunol. 127, 1243-1252.
• Bilej M., Procházková P., Šilerová M., Josková R., 2010. Earthworm immunity. [W:] Invertebrate immunity. Söderhäll K. (red.). Springer Science+Business Media, LLC, New York, 66-79.
• Boe D. M., Curtis B. J., Chen M. M., Ippolito J. A., Kovacs E. J., 2015. Extracellular traps and macrophages: new roles for the versatile phagocyte. J. Leukoc. Biol. 97, 1023-1035.
• Branzk N., Papayannopoulos V., 2013. Molecular mechanisms regulating NETosis in infection and disease. Semin. Immunopathol. 35, 513-530.
• Brinkmann V., Zychlinsky A., 2012. Neutrophil extracellular traps: is immunity the second function of chromatin? J. Cell Biol. 198,773-783.
• 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.
• Brogden G., Krimmling T., Adamek M., Naim H. Y., Steinhagen D., von Köckritz- Blickwede M., 2014. The effect of β-glucan on formation and functionality of neutrophil extracellular traps in carp (Cyprinus carpio L.). Dev. Comp. Immunol. 44, 280-285.
• Chagas A. C., Oliveira F., Debrabant A., Valenzuela J. G., Ribeiro J. M., Calvo E., 2014. Lundep, a sand fly salivary endonuclease increases Leishmania parasite survival in neutrophils and inhibits XIIa contact activation in human plasma. PLoS Pathog. 10, e1003923.
• Chen G., Zhuchenko O., Kuspa A., 2007. Immune-like phagocyte activity in the social amoeba. Science 317, 678-81.
• Chi H., Sun L., 2016. Neutrophils of Scophthalmus maximus produce extracellular traps that capture bacteria and inhibit bacterial infection. Dev. Comp. Immunol. 56, 7-12.
• Cho J. H., Fraser I. P., Fukase K., Kusumoto S., Fujimoto Y., Stahl G. L., Ezekowitz R. A, 2005. Human peptidoglycan recognition protein S is an effector of neutrophil-mediated innate immunity. Blood 106, 2551-2558.
• Cho J. H., Sung B. H., Kim S. C., 2009. Buforins: histone H2A-derived antimicrobial peptides from toad stomach. Biochim. Biophys. Acta 1788, 1564-1569.
• Chuammitri P., Ostojić J., Andreasen C. B., Redmond S. B., Lamont S. J., Palić D., 2009. Chicken heterophil extracellular traps (HETs): novel defense mechanism of chicken heterophils. Vet. Immunol. Immunopathol. 129, 126-131.
• Connor M. A., Jaso-Friedmann L., Leary J. H. 3rd., Evans D. L., 2009. Role of nonspecific cytotoxic cells in bacterial resistance: expression of a novel pattern recognition receptor with antimicrobial activity. Mol. Immunol. 46, 953-961.
• Curlango-Rivera G., Flores-Lara Y., Cho I., Huskey D. A., Xiong Z., Hawes M. C., 2014. Signals controlling extracellular trap formation in plant and animal immune responses. Clin. Microbiol. 3, 5.
• De Cicco M., Rahim M. S., Dames S. A., 2015. Regulation of the target of rapamycin and other phosphatidylinositol 3-kinase-related kinases by membrane targeting. Membranes 5, 553-575.
• Douda D. N., Khan M. A., Grasemann H., Palaniyar N., 2015. SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx. Proc. Natl. Acad. Sci. USA 112, 2817-2822.
• Drescher B., Bai F., 2013. Neutrophil in viral infections, friend or foe? Virus. Res. 171, 1-7.
• Driouich A., Follet-Gueye M. L., Vicré-Gibouin M., Hawes M., 2013. Root border cells and secretions as critical elements in plant host defense. Curr. Opin. Plant Biol. 16, 489-495.
• Dworski R., Simon H. U., Hoskins A., Yousefi S., 2011. Eosinophil and neutrophil extracellular DNA traps in human allergic asthmatic airways. J. Allergy Clin. Immunol. 127, 1260-1266.
• Fadeel B., Ahlin A., Henter J. I., Orrenius S., Hampton M. B., 1998. Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood 92, 4808-4818.
• 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. J. Cell Biol. 176, 231-241.
• Garcia M., Spatz S., Guy J. S., 2013. Infectious laryngotracheitis. [W:] Diseases of poultry. Swayne D. E. (red.). John Wiley & Sons, Ltd, Chichester, 161-179.
• Giambelluca M., Gende O., 2008. Hydrogen peroxide activates calcium influx in human neutrophils. Mol. Cell. Biochem. 309, 151-156.
• Gray R. D., Lucas C. D., Mackellar A., Li F., Hiersemenzel K., Haslett C., Davidson D. J., Rossi A. G., 2013. Activation of conventional protein kinase C (PKC) is critical in the generation of human neutrophil extracellular traps. J. Inflamm. 10, 12.
• Grinberg N., Elazar S., Rosenshine I., Shpigel N. Y., 2008. Beta-hydroxybutyrate abrogates formation of bovine neutrophil extracellular traps and bactericidal activity against mammary pathogenic Escherichia coli. Infect. Immun. 76, 2802-2807.
• Hakkim A., Fuchs T. A., Martinez N. E., Hess S., Prinz H., Zychlinsky A., Waldmann H., 2011. Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat. Chem. Biol. 7, 75-77.
• Halverson T. W., Wilton M., Poon K. K., Petri B., Lewenza S., 2015. DNA is an antimicrobial component of neutrophil extracellular traps. PLoS Pathog. 11,e1004593.
• Hampton M. B., Stamenkovic I., Winterbourn C. C., 2002. Interaction with substrate sensitises caspase-3 to inactivation by hydrogen peroxide. FEBS Lett. 517, 229-232.
• Hawes M. C., Bengough G., Cassab G., Ponce., 2002. Root caps and rhizosphere. J. Plant Growth Regul. 21, 352-367.
• Hawes M. C., Curlango-Rivera G., Wen F., White G. J., Vanetten H. D., Xiong Z., 2011. Extracellular DNA: the tip of root defenses? Plant Sci. 180, 741-745.
• Hazeki O., Hazeki K., Katada T., Ui M., 1996. Inhibitory effect of wortmannin on phosphatidylinositol 3-kinase-mediated cellular events. J. Lipid Mediat. Cell Signal. 14, 259-261.
• He H., Farnell M. B., Kogut M. H., 2003. Inflammatory agonist stimulation and signal pathway of oxidative burst in neonatal chicken heterophils. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 135, 177-184.
• Hellenbrand K. M., Forsythe K. M., Rivera-Rivas J. J., Czuprynski C. J., Aulik N. A., 2013. Histophilus somni causes extracellular trap formation by bovine neutrophils and macrophages. Microb. Pathog. 54, 67-75.
• Hermosilla C., Caro T. M., Silva L. M., Ruiz A., Taubert A., 2014. The intriguing host innate immune response: novel anti-parasitic defence by neutrophil extracellular traps. Parasitology 141, 1489-1498.
• Homa J., Ortmann W., Kolaczkowska E., 2016. Conservative mechanisms of extracellular trap formation by Annelida Eisenia andrei: serine protease activity requirement. PLoS One 11, e0159031.
• Hutton D. M. C., Smith V. J., 1996. Antibacterial properties of isolated amoebocytes from the sea anemone Actinia equine. Biol. Bull. 191, 441-451.
• Itakura A., McCarty O. J., 2013. Pivotal role for the mTOR pathway in the formation of neutrophil extracellular traps via regulation of autophagy. Am. J. Physiol. Cell Physiol. 305, C348-C354.
• Jaroszuk-Ściseł J., Kurek E., 2007. Komórki graniczne : strukturalny i funkcjonalny składnik systemu korzeniowego. Post. Biol. Kom. 34, 623-634.
• Kahlenberg J. M., Carmona-Rivera C., Smith C. K., Kaplan M. J., 2013. Neutrophil extracellular trap-associated protein activation of the NLRP3 inflammasome is enhanced in lupus macrophages. J. Immunol. 190, 1217-1226.
• Katkar G. D., Sundaram M. S., NaveenKumar S. K., Swethakumar B., Sharma R. D., Paul M., Vishalakshi G. J., Devaraja S., Girish K. S., Kemparaju K., 2016. NETosis and lack of DNase activity are key factors in Echis carinatus venom-induced tissue destruction. Nat. Commun. 7, 11361.
• Koiwai K., Alenton R. R., Kondo H., Hirono I., 2016. Extracellular trap formation in kuruma shrimp (Marsupenaeus japonicus) hemocytes is coupled with c-type lysozyme. Fish Shellfish Immunol. 52, 206-209.
• Kolaczkowska E., Jenne C. N., Surewaard B. G., Thanabalasuriar A., Lee W. Y., Sanz M. J., Mowen K., Opdenakker G., Kubes P., 2015. Molecular mechanisms of NET formation and degradation revealed by intravital imaging in the liver vasculature. Nat. Commun. 6, 6673.
• Krautgartner W. D., Klappacher M., Hannig M., Obermayer A., Hartl D., Marcos V., Vitkov L., 2010. Fibrin mimics neutrophil extracellular traps in SEM. Ultrastruct. Pathol. 34, 226-231.
• Lange M. K., Penagos-Tabares F., Muñoz-Caro T., Gärtner U., Mejer H., Schaper R., Hermosilla C., Taubert A., 2017. Gastropod-derived haemocyte extracellular traps entrap metastrongyloid larval stages of Angiostrongylus vasorum, Aelurostrongylus abstrusus and Troglostrongylus brevior. Parasit. Vectors 10, 50.
• Leshner M., Wang S., Lewis C., Zheng H., Chen X. A., Santy L., Wang Y., 2012. PAD4 mediated histone hypercitrullination in- duces heterochromatin decondensation and chromatin unfolding to form neutrophil extracellular trap-like structures. Front. Immunol. 3, 307.
• Letunic I., Bork P., 2016. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242-W245.
• 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. J. Exp. Med. 207, 1853-1862.
• Lin A. M., Rubin C. J., Khandpur R., Wang J. Y., Riblett M., Yalavarthi S., Villanueva E. C., Shah P., Kaplan M. J., Bruce A. T., 2011. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J. Immunol. 187, 490-500.
• Mamikonyan G., Kiyatkin A., Movsesyan N., Mkrtichyan M., Ghochikyan A., Petrushina I., Hwang J., Ichim T. E., Keledjian H., Agadjanyan M. G., 2008. Detection of the active components of calf thymus nuclear proteins (TNP), histones that are binding with high affinity to HIV-1 envelope proteins and CD4 molecules. Curr. HIV Res. 6, 318-326.
• McInturff A. M., Cody M. J., Elliott E. A., Glenn J. W., Rowley J. W., Rondina M. T., Yost C. C., 2012. Mammalian target of rapamycin regulates neutrophil extracellular trap formation via induction of hypoxia-inducible factor 1 α. Blood 120, 3118-3125.
• Méndez-Samperio P., 2010. The human cathelicidin hCAP18/LL-37: a multifunctional pep- tide involved in mycobacterial infections. Peptides 31, 1791-1798.
• Merza M., Hartman H., Rahman M., Hwaiz R., Zhang E., Renström E., Luo L., Mörgelin M., Regner S., Thorlacius H., 2015. Neutrophil extracellular traps induce trypsin activation, inflammation, and tissue damage in mice with severe acute pancreatitis. Gastroenterology 149, 1920-1931.
• Metzler K. D., Fuchs T. A., Nauseef W. M., Reumaux D., Roesler J., Schulze I., Wahn V., Papayannopoulos V., Zychlinsky A., 2011. Myeloperoxidase is required for neutrophil extracellular trap formation: implications for innate immunity. Blood 117, 953-959.
• Morshed M., Hlushchuk R., Simon D., Walls A.F., Obata-Ninomiya K., Karasuyama H., Djonov V., Eggel A., Kaufmann T., Simon H. U., Yousefi S., 2014. NADPH oxidase-independent formation of extracellular DNA traps by basophils. J. Immunol. 192, 5314-5323.
• Muñoz-Caro T., Silva L. M., Ritter C., Taubert A., Hermosilla C., 2014. Besnoitia besnoiti tachyzoites induce monocyte extracellular trap formation. Parasitol. Res. 113, 4189-4197.
• Muñoz-Caro T., Rubio R. M. C., Silva L. M., Magdowski G., Gärtner U., McNeilly T. N., Taubert A., Hermosilla C., 2015. Leucocyte-derived extracellular trap formation significantly contributes to Haemonchus contortus larval entrapment. Parasit. Vectors 8, 607.
• Neeli I., Radic M., 2013. Opposition between PKC isoforms regulates histone deimination and neutrophil extracellular chromatin release. Front. Immunol. 4, 38.
• Neeli I., Khan S. N., Radic M., 2008. Histone deimination as a response to inflammatory stimuli in neutrophils. J. Immunol. 180, 1895-1902.
• Neeli I., Dwivedi N., Khan S., Radic M., 2009. Regulation of extracellular chromatin release from neutrophils. J. Innate Immun. 1, 194-201.
• Nel J. G., Theron A. J., Pool R., Durandt C., Tintinger G. R., Anderson R., 2016. Neutrophil extracellular traps and their role in health and disease. S. Afr. J. Sci. 112, 36-44.
• Ng T. H., Chang S. H., Wu M. H., Wang H. C., 2013. Shrimp hemocytes release extracellular traps that kill bacteria. Dev. Comp. Immunol. 41, 644-651.
• Ng T. H., Wu M. H., Chang S. H., Aoki T., Wang H. C., 2015. The DNA fibers of shrimp hemocyte extracellular traps are essential for the clearance of Escherichia coli. Dev. Comp. Immunol. 48, 229-233.
• Obermayer A., Stoiber W., Krautgartner W. D., Klappacher M., Kofler B., Steinbacher P., Vitkov L., Grabcanovic-Musija F., Studnicka M., 2014. New aspects on the structure of neutrophil extracellular traps from chronic obstructive pulmonary disease and in vitro generation. PLoS One 9, 1-9.
• O'Donoghue A. J., Jin Y., Knudsen G. M., Perera N. C., Jenne D. E., Murphy J. E., Craik C. S., Hermiston T. W., 2013. Global substrate profiling of proteases in human neutrophil extracellular traps reveals consensus motif predominantly contributed by elastase. PLoS One 8, e75141.
• Palić D., Andreasen C, B., Ostojić J., Tell R. M., Roth J. A., 2007a. Zebrafish (Danio rerio) whole kidney assays to measure neutrophil extracellular trap release and degranulation of primary granules. J. Immunol. Meth. 319,87-97.
• Palić D., Ostojić J., Andreasen C. B., Roth J. A., 2007b. Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils. Dev. Comp. Immunol. 31, 805-816.
• Papayannopoulos V., Metzler K. D., Hakkim A., Zychlinsky A., 2010b. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 191,677-691.
• Parker H., Dragunow M., Hampton M. B., Kettle A. J., Winterbourn C. C., 2012. Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J. Leukoc. Biol. 92, 841-849.
• Pijanowski L., Golbach L., Kolaczkowska E., Scheer M., Verburg-van Kemenade B. M., Chadzinska M., 2013. Carp neutrophilic granulocytes form extracellular traps via ROS-dependent and independent pathways. Fish Shellfish Immunol. 34, 1244-1252.
• Pijanowski L., Scheer M., Verburg-van Kemenade B. M., Chadzinska M., 2015a. Production of inflammatory mediators and extracellular traps by carp macrophages and neutrophils in response to lipopolysaccharide and/or interferon-γ2. Fish Shellfish Immunol. 42, 473-482.
• Pijanowski L., Verburg-van Kemenade B. M., Irnazarow I., Chadzinska M., 2015b. Stress- induced adaptation of neutrophilic granulocyte activity in K and R3 carp lines. Fish Shellfish Immunol. 47, 886-892.
• Reddy V. R., Trus I., Nauwynck H. J., 2017. Presence of DNA extracellular traps but not MUC5AC and MUC5B mucin in mucoid plugs/casts of infectious laryngotracheitis virus (ILTV) infected tracheas of chickens. Virus Res. 227,135-142.
• Reichel M., Muñoz-Caro T., Sanchez Contreras G., Rubio García A., Magdowski G., Gärtner U., Taubert A., Hermosilla C., 2015. Harbour seal (Phoca vitulina)PMN and monocytes release extracellular traps to capture the apicomplexan parasite Toxoplasma gonidii. Dev. Comp. Immunol. 50, 106-115.
• Remijsen Q., Kuijpers T. W., Wirawan E., Lippens S., Vandenabeele P., Vanden Berghe T., 2011a. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ. 18, 581-588.
• Remijsen Q., Vanden Berghe T., Wirawan E., Asselbergh B., Parthoens E., De Rycke R., Noppen S., Delforge M., Willems J., Vandenabeele P., 2011b. Neutrophil extracellular traps cell death requires both autophagy and superoxide generation. Cell. Res. 21, 290-304.
• Robb C. T., Dyrynda E. A., Gray R. D., Rossi A. G., Smith V. J., 2014. Invertebrate extracellular phagocyte traps show that chromatin is an ancient defence weapon. Nat. Comm. 5, 4627.
• Rogers D. F., 2007. Mucoactive agents for airway mucus hypersecretory diseases. Respir. Care 52, 11761193.
• Rohrbach A. S., Slade D. J., Thompson P. R., Mowen K. A., 2012. Activation of PAD4 in NET formation. Front Immunol. 3, 360.
• Sadikot R. T., Zeng H., Yull F. E., Li B., Cheng D. S., Kernodle D. S., Jansen E. D., Contag C. H., Segal B. H., Holland S. M., Blackwell T. S., Christman J. W., 2004. p47phox deficiency impairs NF-kappa B activation and host defense in Pseudomonas pneumonia. J. Immunol. 172, 1801-1808.
• Saffarzadeh M., Preissner K. T., 2013. Fighting against the dark side of neutrophil extracellular traps in disease: manoeuvres for host protection. Curr. Opin. Hematol. 20, 3-9.
• Saitoh T., Komano J., Saitoh Y., Misawa T., Takahama M., Kozaki T., Uehata T., Iwasaki H., Omori H., Yamaoka S., Yamamoto N., Akira S., 2012. Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 12, 109-116.
• Schauer C., Janko C., Munoz L. E., Zhao Y., Kienhöfer D., Frey B., Lell M., Manger B., Rech J., Naschberger E., Holmdahl R., Krenn V., Harrer T., Jeremic I., Bilyy R., Schett G., Hoffmann M., Herrmann M., 2014. Aggregated neutrophil extracellular traps limit inflammation by degrading cytokines and chemokines. Nat. Med. 20, 511-517.
• Schmidt O., Söderhäll K., Theopold U., Faye I., 2010. Role of adhesion in arthropod immune recognition. Annu. Rev. Entomol. 55, 485-504.
• Söderhäll K., 2010. Invertebrate immunity. Advances in experimental medicine and biology. Springer Science+Business Media, LLC, New York.
• Silva L. M., Muñoz-Caro T., Burgos R. A., Hidalgo M. A., Taubert A., Hermosilla C., 2016. Far beyond phagocytosis: phagocyte-derived extracellular traps act efficiently against protozoan parasites in vitro and in vivo. Mediators Inflamm. 2016, 5898074.
• Tran T. M., MacIntyre A., Hawes M., Allen C., 2016. Escaping underground NETs: extracellular DNases degrade plant extracellular traps and contribute to virulence of the plant pathogenic bacterium Ralstonia solanacearum. PLoS Pathog. 12, e1005686.
• 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 Pathog. 5,e1000639.
• Verschure P. J., van der Kraan I., de Leeuw W., van der Vlag J., Carpenter A. E., Belmont A. S., van Driel R., 2005. In vivo HP1 targeting causes large-scale chromatin condensation and enhanced histone lysine methylation. Mol. Cell Biol. 25, 4552-4564.
• 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.
• Wang Y., Wysocka J., Sayegh J., Lee Y. H., Perlin J. R., Leonelli L., Sonbuchner L. S., McDonald C. H., Cook R. G., Dou Y., Roeder R. G., Clarke S., Stallcup M. R., Allis C. D., Coonrod S. A., 2004. Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306, 279-283.
• Wang Y., Li M., Stadler S., Correll S., Li P., Wang D., Hayama R., Leonelli L., Han H., Grigoryev S. A., Allis C. D., Coonrod S. A., 2009. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J. Cell Biol. 184, 205-213.
• Wartha F., Beiter K., Normark S., Henriques-Normark B., 2007. Neutrophil extracellular traps: casting the NET over pathogenesis. Curr. Opin. Microbiol. 10, 52-56.
• Wen F., White G. J., VanEtten H. D., Xiong Z., Hawes M. C., 2009. Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol. 151, 820-829.
• Wilkie R. P., Vissers M. C., Dragunow M., Hampton M. B., 2007. A functional NADPH oxidase prevents caspase involvement in the clearance of phagocytic neutrophils. Infect. Immun. 75, 3256-3263.
• Yousefi S., Gold J. A., Andinaetal N., 2008. Catapult-like release of mitochondria DNA by eosinophils contributes to antibacterial defense. Nat. Med. 14, 949-953.
• Yousefi S., Mihalache C., Kozlowski E., Schmid I., Simon H. U., 2009. Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ. 16,1438-1444.
• Zhang X., Soldati T., 2016. Of amoebae and men: extracellular DNA traps as an ancient cell-intrinsic defense mechanism. Front. Immunol. 7, 269.
• Zhang X., Zhuchenko O., Kuspa A., Soldati T., 2016. Social amoebae trap and kill bacteria by casting DNA nets. Nat. Comm. 7, 10938.