Neutrophil in viral infections, Friend or foe?

Virus Research

Volumn 171, Issue 1, 2013, Pages 1-7

  Drescher, Brandon ^a   Bai, Fengwei ^a  

^a The University of Southern Mississippi   (United States)

Author keywords

Neutrophil; Viral pathogenesis

Indexed keywords

ADAPTIVE IMMUNITY; IMMUNE SYSTEM; INNATE IMMUNITY; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS INFECTION; VIRUS PATHOGENESIS; VIRUS TRANSCRIPTION; VIRUS TRANSMISSION;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; NEUTROPHILS; VIRUS DISEASES;

BACTERIA (MICROORGANISMS);

EID: 84872804890     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2012.11.002     Document Type: Review

References (106)

1. Antachopoulos C., Roilides E. Cytokines and fungal infections. British Journal of Haematology 2005, 129:583-596.
2. Bai F., Kong K.-F., Dai J., Qian F., Zhang L., Brown C., Fikrig E., Montgomery R. A paradoxical role for neutrophils in the pathogenesis of West Nile virus. Journal of Infectious Diseases 2010, 202:1804-1812.
3. Bai F., Town T., Qian F., Wang P., Kamanaka M., Connolly T., Gate D., Montgomery R., Flavell R., Fikrig E. IL-10 signaling blockade controls murine West Nile virus infection. PLoS Pathogens 2009, 5:e1000610.
4. Boucher R. New concepts of the pathogenesis of cystic fibrosis lung disease. European Respiratory Journal 2004, 23:146-158.
5. Bréhin A., Mouriès J., Frenkiel M., Dadaglio G., Desprès P., Lafon M., Couderc T. Dynamics of immune cell recruitment during West Nile encephalitis and identificaiton of a new CD19+ B220-BST-2+ leukocyte population. Journal of Immunology 2008, 180:6760-6767.
6. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D., Weinrauch Y., Zychlinksy A. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535.
7. Brinkmann V., Zychlinksy A. Beneficial suicide: why neutrophils die to make NETs. Nature Reviews Microbiology 2007, 5:577-582.
8. Brinkmann V., Zychlinsky A. Neutrophil extracellular traps: is immunity the second function of chromatin?. Journal of Cell Biology 2012, 198:773-783.
9. Choi K.-S., Dumler J. Early induction and late abrogation of respiratory burst in A. phagocytophilum-infected neutrophils. Annals of the New York Academy of Sciences 2003, 990:488-493.
10. Chtanova T., Schaeffer M., Han S.-J., van Dooren G., Nollmann M., Herzmark P., Chan S., Satija H., Camfield K., Aaron H., Striepen B., Robey E. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 2008, 29:487-496.
11. Clark S., Ma A., Tavener S., McDonald B., Goodarzi Z., Kelly M., Patel K., Chakrabarti S., McAvoy E., Sinclair G., Keys E., Allen-Vercor E., Devinney R., Doig C., Green F., Kubes P. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nature Medicine 2007, 13:463-469.
12. Colamussi M., White M., Crouch E., Hartshorn K. Influenza A virus accelerates neutrophil apoptosis and markedly potentiates apoptotic effects of bacteria. Blood 1999, 93:2395-2403.
13. Colotta F., Re F., Polentarutti N., Sozzani S., Mantovani A. Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 1992, 80:2012-2020.
14. Crameri R., Blaser K. Allergy and immunity to fungal infections and colonization. European Respiratory Journal 2002, 19:151-157.
15. Croker B., Roberts A., Nicola N. Towards a four-dimensional view of neutrophils. Leukocytes: Methods and Protocols, Methods in Molecular Biology. 2012, vol. 844:87-99. Springer, Brisbane, QLD, Australia.
16. Daffis S., Samuel M., Keller B., Gale M., Diamond M. Cell-specific IRF-3 responses protect against West Nile virus infection by interferon-depenednt and -independent mechanisms. PLoS Pathogens 2007, 3:e106.
17. Deshpande S., Banerjee K., Biswas P., Rouse B. Herpetic eye disease: immunopathogenesis and therapeutic measures. Expert Reviews in Molecular Medicine 2004, 6:1-14.
18. Djeu J., Liu J., Wei S., Rui H., Pearson C., Leonard W., Blanchard D. Function associated with IL-2 receptor-β on human neutrophils. Journal of Immunology 1993, 150:960-970.
19. Douglas R., Alford R., Cate T., Couch R. The leukocyte response during viral respiratory illness in man. Annals of Internal Medicine 1966, 64:521-530.
20. Elbim C., Katsikis P., Estaquier J. Neutrophil apoptosis during viral infections. Open Virology Journal 2009, 3:52-59.
21. Engelich G., White M., Hartshorn K. Role of the respiratory burst in co-operative reduction in neutrophil survival by influenza A virus and Escherichia coli. Journal of Medical Microbiology 2002, 51:484-490.
22. Fang M., Wan M., Guo S., Sun R., Yang M., Zhao T., Yan Y., Zhang Y., Huang W., Wu X., Yu Y., Wang L., Hua S. An oligodeoxynucleotide capable of lessening acute lung inflammatory injury in mice infected by influenza virus. Biochemical and Biophysical Research Communications 2011, 415:342-347.
23. Ferrante A. Tumor necrosis factor alpha potentiates neutrophil antimicrobial activity: increased fungicidal activity against Torulopsis glabrata and Candida albicans and associated increases in oxygen radical production and lysosomal enzyme release. Infection and Immunity 1989, 57:2115-2122.
24. Ferretti S., Bonneau O., Dubois G., Jones C., Trifilieff A. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. Journal of Immunology 2003, 170:2106-2112.
25. Fuchs T., Abed U., Goosmann C., Hurwitz R., Schulze I., Wahn V., Weinrauch Y., Brinkmann V., Zychlinksy A. Novel cell death program leads to neutrophil extracellular traps. Journal of Cell Biology 2007, 176:231-241.
26. Fujie K., Shinguh T., Inamura N., Yasumitsu R., Okamoto M., Okuhara M. Release of neutrophil elastase and its role in tissue injury in acute inflammation: effect of the elastase inhibitor. FR 134043. European Journal of Pharmacology 1999, 374:117-125.
27. Garcia-Romo G., Caielli S., Vega B., Connolly J., Allantaz F., Xu Z., Punaro M., Baisch J., Guiducci C., Coffman R., Barrat F., Banchereau J., Pascual V. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Science Translational Medicine 2011, 3:73ra20.
28. Gaviria J., van Burik J., Dale D., Root R., Liles W. Comparison of interferon-gamma, granulocyte colony-stimulating factor, and granulocyte-macrophage colony-stimulating factor for priming leukocyte-mediated hyphal damage of opportunistic fungal pathogens. Journal of Infectious Diseases 1999, 179:1038-1041.
29. Gonzalez-Dosal R., Horan K., Rahbek S., Ichijo H., Chen Z., Mieyal J., Hartmann R., Paludan S. HSV infection induces production of ROS, which potentiates signaling from pattern recognition receptors: role for S-glutathione of TRAF3 and 6. PLoS Pathogens 2011, 7:e1002250.
30. Gosselin J., Savard M., Tardif M., Flamand L., Borgeat P. Epstein-Barr virus primes human polymorphonuclear leucocytes for the biosynthesis of leukotriene B4. Clinical and Experimental Immunology 2001, 126:494-502.
31. Gray K., Worthy M., Juelich T., Agar S., Poussard A., Ragland D., Freiberg A., Holbrook M. Chemotactic and inflammatory responses in the liver and brain are associated with pathogenesis of rift valley fever virus infection in the mouse. PLoS Neglected Tropical Diseases 2011, 6:e1529.
32. Gresham H., Lowrance J., Caver T., Wilson B., Cheung A., Lindberg F. Survival of Staphylococcus aureus inside neutrophils contributes to infection. Journal of Immunology 2000, 164:3713-3722.
33. Grundy J., Lawson K., MacCormac L., Fletcher J., Young K. Cytomegalovirus-infected endothelial cells recruit neutrophils by the secretion of C-X-C chemokines and transmit virus by direct neutrophil-endothelial cell contact and during neutrophils transendothelial migration. Journal of Infectious Diseases 1998, 177:1465-1474.
34. Gu J., Xie Z., Gao Z., Liu J., Korteweg C., Ye J., Lau L., Lu J., Gao Z., Zhang B., McNutt M., Lu M., Anderson V., Gong E., Yu A., Lipkin W. H5N1 infection of the respiratory tract and beyond: a molecular pathology study. Lancet 2007, 370:1137-1145.
35. Guimarães-Costa A., Nascimento M., Wardini A., Pinto-da-Silva L., Saraiva E. ETosis: a microbicidal mechanism beyond cell death. Journal of Parasitology Research 2012, 2012. 10.1155/2012/929743.
36. Hachicha M., Rathanaswami P., Naccache P., McColl S. Regulation of chemokine gene expression in human peripheral blood neutrophils phagocytosing microbial pathogens. Journal of Immunology 1998, 160:449-454.
37. Hemmers S., Teijaro J., Arandjelovic S., Mowen K. PAD4-mediated neutrophil extracellular trap formation is not required for immunity against influenza infection. PLoS ONE 2011, 6:e22043.
38. Hoshino A., Nagao T., Nagi-Miura N., Ohno N., Yasuhara M., Yamamoto K., Nakayama T., Suzuki K. MPO-ANCA induces IL-17 production by activated neutrophils in vitro via classical complement pathway-dependent manner. Journal of Autoimmunity 2008, 31:79-89.
39. Hu S., Sheng W., Schachtele S., Lokensgard J. Reactive oxygen species drive herpes simplex virus (HSV)-1-induced proinflammatory cytokine production by murine microglia. Journal of Neuroinflammation 2011, 8. 10.1186/1742-2094-1188-1123.
40. Hufford M., Richardson G., Zhou H., Manicassamy B., CGarcia-Sastre A., Enelow R., Braciale T. Influenza-infected neutrophils within the infected lungs act as antigen presenting cells for anti-viral CD8(+) T cells. PLoS ONE 2012, 7:e46581.
41. Knickelbein J., Hendricks R., Charukamnoetkanok P. Management of herpest simplex virus stromal keratitis: and evidence-based review. Survey of Ophthalmology 2009, 54:226-234.
42. Kobasa D., Jones S., Shinya K., Kash J., Copps J., Ebihara H., Hatta Y., Kim J., Halfmann P., Hatta M., Feldmann F., Alimonti J., Fernando L., Li Y., Katze M., Feldmann H., Kawaoka Y. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 2007, 445:319-323.
43. Kobayashi S., Voyich J., Burlak C., DeLeo F. Neutrophils in the innate immune response. Archivum Immunologiae et Therapiae Experimentalis 2005, 53:505-517.
44. Kobayashi S., Voyich J., Somerville G., Braughton K., Malech H., Musser J., DeLeo F. An apoptosis-differentiation program in human polymorphonuclear leukocytes facilitates resolution of inflammation. Journal of Leukocyte Biology 2003, 73:315-322.
45. Kohyama S., Ohno S., Isoda A., Osamu M., Belladonna M., Hayashi H., Iwakura Y., Yoshimoto T., Akatsuka T., Matsui M. IL-23 enhances host defense against vaccinia virus infection via a mechanism partly involving IL-17. Journal of Immunology 2007, 179:3917-3925.
46. Lande R., Ganguly D., Facchinetti V., Frasca L., Conrad C., Gregorio J., Meller S., Chamilos G., Sebasigari R., Riccieri V., Bassett R., Amuro H., Fukuhara S., Ito T., Liu Y., Gilliet M. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Science Translational Medicine 2011, 3:73ra19.
47. Le Goffic R., Leymarie O., Chevalier C., Rebours E., Da Costa B., Vidic J., Descamps D., Sallenave J.-M., Rauch M., Samson M., Delmas B. Transcriptomic analysis of host immune and cell death responses associated with the influenza A virus PB1-F2 protein. PLoS ONE 2011, 7:e1002202.
48. Lekstrom-Himes J., Gallin J. Immunodeficiency diseases caused by defects in phagocytes. New England Journal of Medicine 2000, 343:1703-1714.
49. Li R., Lim A., Phoon M., Narasaraju T., Ng J., Poh W., Sim M., Chow V., Locht C., Alonso S. Attenuated Bordetella pertussis protects against highly pathogenic influenza A viruses by dampening the cytokine storm. Journal of Virology 2010, 84:7105-7113.
50. Lindemans C., Coffer P., Shcellens I., de Graaff P., Kimpen J., Koenderman L. Respiratory syncytial virus inhibits granulocyte apoptosis through a phosphatidylinositol 3-kinase and NF-κB-dependent mechanism. Journal of Immunology 2006, 176:5529-5537.
51. Lusitani D., Malawista S., Montgomery R. Calprotectin, an abundant cytosolic protein from human polymorphonuclear leukocytes, inhibits the growth of Borrelia burgdorferi. Infection and Immunity 2003, 71:4711-4716.
52. Marcos V., Zhou Z., Yildirim A., Bohla A., Hector A., Vitkov L., Wiedenbauer E., Krautgartner W., Stoiber W., Belohradsky B., Rieber N., Kormann M., Koller B., Roscher A., Roos D., Griese M., Eickelberg O., Döring G., Mall M., Hartl D. CXCR2 mediates NADPH oxidase-independent neutrophil extracellular trap formaiton in cystic fibrosis airway inflammation. Nature Medicine 2010, 16:1018-1023.
53. McNamara P., Selby A., Hart C., Smyth R. Bronchoalveolar cellularity in infants with severe RSV bronchiolitis. Archives of Disease in Childhood 2003, 99:922-926.
54. Munir S., Hillyer P., Le Nouën C., Buchholz U., Rabin R., Collins P., Bukreyev A. Respiratory syncytial virus interferon antagonist NS1 protein suppresses and skews the human T lymphocyte response. PLoS ONE 2011, 7:e29386.
55. Nagarkar D., Wang Q., Shim J., ZHao Y., Tsai W., Lukacs N., Sajjan U., Hershenson M. CXCR2 is required for neutrophilic airway inflammation and hyperresponsiveness in a mouse model of human rhinovirus infection. Journal of Immunology 2009, 183:6698-6707.
56. Nathan C. Neutrophils and immunity: challenges and opportunities. Nature Reviews Immunology 2006, 6:173-182.
57. Navarini A., Lang K., Verschoor A., Recher M., Zinkernagel A., Nizet V., Odermatt B., Hengartner H., Zinkernagel R. Innate immune-induce depletion of bone marrow neutrophils aggravates systemic bacterial infections. Proceedings of the National Academy of Science United States of America 2009, 106:7107-7112.
58. Papayannopoulos V., Zychlinsky A. NETs: a new strategy for using old weapons. Trends in Immunology 2009, 30:513-521.
59. Peters N., Egen J., Secundino N., Debrabant A., Kimblin N., Kamhawi S., Lawyer P., Fay M., Germain R., Sacks D. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 2008, 321:970-974.
60. 2O reveals a human neutrophil lifespan of 5.4 days. Blood 2010, 116:625-627.
61. Rada B., Leto T. Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contributions to Microbiology 2008, 15:164-187.
62. Rajasagi N., Reddy P., Suryawanshi A., Mulik S., Gjorstrup P., Rouse B. Controlling herpes simple virus-induced ocular inflammatory lesions with the lipid-derived mediator resolvin E1. Journal of Immunology 2012, 186:1735-1746.
63. Rawal A., Gavin P., Sturgis C. Cerebrospinal fluid cytology in seasonal epidemic West Nile virus meningo-encephalitis. Diagnostic Cytopathology 2006, 34:127-129.
64. Roilides E., Uhlig K., Venzon D., Pizzo P., Walsh T. Enhancement of oxidative response and damage caused by human neutrophils to Asperigullus fumigatus hyphae by granulocyte colony-stimulating factor and gamma interferon. Infection and Immunity 1993, 61:1185-1193.
65. Rosenthal L., Amineva S., Szakaly R., Lemanske R., Gern J., Sorkness R. A rat model of picornavirus-induced airway infection and inflammation. Virology Journal 2009, 6. 10.1186/1743-1422X-1186-1122.
66. Rosenthal L., Szakaly R., Amineva S., Xing Y., Hill M., Palmenberg A., Gern J., Sorkness R. Lower respiratory tract infection induced by a genetically modified picornavirus in its natural murine host. PLoS ONE 2011, 7:e32061.
67. Ruthe R., Andersen B., Cunningham B., Epstein R. Effect of granulocyte transfusion in the control of systemic candidiasis in the leukopenic host. Blood 1978, 52:493.
68. Saez-Lopez C., Ngambe-Tourere E., Rosenzwajg M., Petit J.-C., Nicolas J.-C., Gozlan J. Immediate-early antigen expression and modulation of apoptosis after in vitro infection of polymorphonuclear leukocytes by human cytomegalovirus. Microbes and Infection 2005, 7:1139-1149.
69. Saitoh T., Komano J., Saitoh Y., Misawa T., Takahama M., Kozaki T., Uehata T., Iwasaki H., Omori H., Yamaoka S., Yamamoto K., Akira S. Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host and Microbe 2012, 12:109-116.
70. Savard M., Gosselin J. Epstein-Barr virus immunossuppression of innate immunity mediated by phagocytosis. Virus Research 2006, 119:134-145.
71. Savill J., Dransfield I., Gregory C., Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nature Reviews Immunology 2002, 2:965-975.
72. Savill J., Wyllie A., Henson J., Walport M., Henson P., Haslett C. Macrophage phagocytosis of aging neutrophils in inflammation. Journal of Clinical Investigation 1989, 83:865-875.
73. Segal A. How neutrophils kill microbes. Annual Review of Immunology 2005, 23:197-223.
74. Segovia J., Sabbah A., Mgbemena V., Tsai S.-Y., Chang T.-H., Berton M., Morris I., Allen I., Ting J.-Y., Bose S. TLR2/MyD88/NF-κB pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PLoS ONE 2012, 7:e29695.
75. Seki M., Kohno S., Newstead M., Zeng X., Bhan U., Lukacs N., Kunkel S., Standiford T. Critical role of IL-1 receptor-associated kinase-M in regulating chemokine-dependent deleterious inflammation in murine influenza pneumonia. Journal of Immunology 2010, 184:1410-1418.
76. hi monocytes and neutrophils during acute viral pneumonia in mice. PLoS Pathogens 2011, 7:e1001304.
77. Serhan C., Chiang N., Van Dyke T. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nature Reviews Immunology 2008, 8:349-361.
78. Soehnlein O. Direct and alternative antimicrobial mechanisms of neutrophil-derive granule proteins. Journal of Molecular Medicine 2009, 87:1157-1164.
79. Soehnlein O. An elegant defense: how neutrophils shape the immune response. Trends in Immunology 2009, 30:511-512.
80. Soehnlein O., Zernecke A., Eriksson E., Rothfucks A., Pham C., Herwald H., Bidzhekov K., Rottenberg M., Weber C., Lindbom L. Neutrophil secretion products pave the way for inflammatory response. Blood 2008, 112:1461-1471.
81. Sohnle P., Hunter M., Hahn B., Chazin W. Zinc-reversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). Journal of Infectious Diseases 2000, 182:1272-1275.
82. Speir E., Shibutani T., Yu Z., Ferrans V., Epstein S. Role of reactive oxygen intermediates in cytomegalovirus gene expression and in the response of human smooth muscle cells to viral infection. Circulation Research 1996, 79:1143-1152.
83. Stark M., Huo Y., Burcin T., Morris M., Olson T., Ley K. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 2005, 22:285-294.
84. Stout-Delgado H., Du W., Shirali A., Booth C., Goldstein D. Aging promotes neutrophil-induced mortality by augmenting IL-17 production during viral infection. Cell Host and Microbe 2009, 19:446-456.
85. Tate M., Brooks A., Reading P. The role of neutrophils in the upper and lower respiratory tract during influenza virus infection of mice. Respiratory Research 2008, 9:57.
86. Tate M., Deng Y.-M., Jones J., Anderson G., Brooks A., Reading P. Neutrophils ameliorate lung injury and the development of severe disease during influenza infection. Journal of Immunology 2009, 183:7441-7450.
87. Tkalcevic J., Novelli M., Phylactides M., Iredale J., Segal A., Roes J. Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity 2000, 12:201-210.
88. Town T., Bai F., Wang T., Kaplan A., Qian F., Montgomery R., Anderson J., Flavell R., Fikrig E. TLR7 mitigates lethal West Nile encephalitis by affecting interleukin 23-dependent immune cell infiltration and homing. Immunity 2009, 30:242-253.
89. Tumpey T., Garcia-Sastre A., Taubenberger J., Palese P., Swayne D., Pantin-Jackwood M., Schultz-Cherry S., Solórzano A., van Rooijen N., Katz J., Basler C. Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. Journal of Virology 2005, 79:14933-14944.
90. Tyler K., Pape J., Goody R., Corkill M., Kleinschmidt-DeMasters B. CSF findings in 250 patients with serologically confirmed West Nile virus meningitis and encephalitis. Neurology 2006, 66:361-365.
91. Ulrich M., Worlitzsch D., Viglio S., Siegmann N., Iadarola P., Shute J., Geiser M., Pier G., Friedel G., Barr M., Schuster A., Meyer K., Ratjen F., Bjarnsholt T., Gulbins E., Döring G. Alveolar inflammation in cystic fibrosis. Journal of Cystic Fibrosis 2010, 9:217-227.
92. Urban C., Ermert D., Schmid M., Abu-Adeb U., Goosmann C., Nacken W., Brinkmann V., Jungblut P., Zychlinksy A. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathogens 2009, 5:e1000639.
93. Urban C., Reichard U., Brinkmann V., Zychlinksy A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cellular Microbiology 2006, 8:668-676.
94. Voyich J., Braughton K., Sturdevant D., Whitney A., Said-Salim B., Porcella S., Long R., Dorward D., Gardner D., Kreiswirth B., Musser J., DeLeo F. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. Journal of Immunology 2005, 175:3907-3919.
95. Waldorf A. Pulmonary defense mechanisms against opportunistic fungal pathogens. Immunology Series 1989, 47:243-271.
96. Wang J., Bowen G., Padden C., Cemy A., Finberg R., Newburger P., Kurt-Jones E. Toll-like receptor-mediated activation of neutrophils by influenza A virus. Blood 2008, 112:2028-2034.
97. Wang T., Town T., Alexopoulon L., Anderson J., Fikrig E., Flavell R. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nature Medicine 2004, 10:1366-1373.
98. Wang Y., Li M.-R., Stadler S., Correll S., Li P., Danchen W., Hayama R., Lauriebeth L., Han H., Grigoryev S., Allis C., Coonrod S. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. Journal of Cell Biology 2009, 184:205-213.
99. Wardini A., Guimarañes-Costa A., Nascimento M., Nadaes N., Danelli M., Mazur C., Benjamin C., Saraiva E., Pinto-da-Silva L. Characterization of neutrophil extracellular traps in cats naturally infected with feline leukemia virus. Journal of General Virology 2010, 91:259-264.
100. Wartha F., Beiter K., Normark S., Henriques-Normark B. Neutrophil extracellular traps: casting the NET over pathogenesis. Current Opinion in Microbiology 2007, 10:52-56.
101. Worlitzsch D., Tarran R., Ulrich M., Schwab U., Cekici A., Meyer K., Birrer P., Bellon G., Berger J., Weiβ T., Botzenhart K., Yankaskas J., Randell S., Boucher R., Döring G. Reduced oxygen concentrations in airway mucus contribute to the early and late pathogenesis of Pseudomonas aeruginosa cystic fibrosis airways infection. Journal of Clinical Investigation 2002, 109:295-309.
102. Yang D., de la Rosa G., Tewary P., Oppenheim J. Alarmins link neutrophils and dendritic cells. Trends in Immunology 2009, 30:531-537.
103. Yousefi S., Gold J., Andina N., Lee J., Kelly A., Kozlowski E., Schmid I., Straumann A., Reichenbach J., Gleich G., Simon H. Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nature Medicine 2008, 14:949-953.
104. Yousefi S., Mihalache C., Kozlowski E., Simon H. Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death and Differentiation 2009, 16:1438-1444.
105. + monocytes correlate with the severity of liver injury and fibrosis in patients with chronic hepatitis B. PLoS ONE 2011, 6:e17484.
106. Zhao Y., Lu M., Lau L., Lu J., Gao Z., Liu J., Yu A., Cao Q., Ye J., McNutt M., Gu J. Neutrophils may be a vehicle for viral replication and dissemination in human H5N1 avian influenza. Clinical Infectious Diseases 2008, 47:1575-1578.