Influence of microbes on neutrophil life and death

Frontiers in Cellular and Infection Microbiology

Volumn 7, Issue MAY, 2017, Pages

  Kobayashi, Scott D ^a   Malachowa, Natalia ^a   DeLeo, Frank R ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Apoptosis; Host defense; Necroptosis; Necrosis; Phagocytosis; Programmed cell death

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICROBICIDE; PATHOGEN RECOGNITION RECEPTOR; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANTIBIOTIC SENSITIVITY; ANTIFUNGAL SUSCEPTIBILITY; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; BACTERIAL INFECTION; BORRELIA HERMSII; CANDIDIASIS; CELL MEMBRANE; EXTRACELLULAR TRAP; FRANCISELLA TULARENSIS; HOMEOSTASIS; HUMAN; HUMAN GRANULOCYTIC ANAPLASMOSIS; HYPOXIA; INFLAMMATION; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; MICROENVIRONMENT; MYCOBACTERIUM TUBERCULOSIS; MYCOSIS; NEUTROPHIL; NONHUMAN; PARASITOSIS; PHAGOCYTE; PHAGOCYTOSIS; PROTEIN EXPRESSION; REVIEW; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; TISSUE INJURY; ANIMAL; BACTERIUM; CELL DEATH; FUNGUS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY; NECROSIS; PARASITE; PATHOGENICITY; PHYSIOLOGY; VIRUS;

ANIMALS; APOPTOSIS; BACTERIA; CELL DEATH; FUNGI; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; NECROSIS; NEUTROPHILS; PARASITES; PHAGOCYTOSIS; VIRUSES;

EID: 85027489470     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2017.00159     Document Type: Review

References (121)

1. 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. Infect. Immun. 80, 768-777. doi: 10.1128/IAI.05730-11
2. Aga, E., Katschinski, D. M., van Zandbergen, G., Laufs, H., Hansen, B., Muller, K., et al. (2002). Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J. Immunol. 169, 898-905. doi: 10.4049/jimmunol.169.2.898
3. Allen, H. L., and Deepe, G. S. Jr. (2005). Apoptosis modulates protective immunity to the pathogenic fungus Histoplasma capsulatum. J. Clin. Invest. 115, 2875-2885. doi: 10.1172/JCI25365
4. Athens, J. W., Haab, O. P., Raab, S. O., Mauer, A. M., Ashenbrucker, H., Cartwright, G. E., et al. (1961). Leukokinetic studies. IV. The total blood, circulating and marginal granulocyte pools and the granulocyte turnover rate in normal subjects. J. Clin. Invest. 40, 989-995. doi: 10.1172/JCI104338
5. Bai, F., Kong, K. F., Dai, J., Qian, F., Zhang, L., Brown, C. R., et al. (2010). A paradoxical role for neutrophils in the pathogenesis of West Nile virus. J. Infect. Dis. 202, 1804-1812. doi: 10.1086/657416
6. Baker, V. S., Imade, G. E., Molta, N. B., Tawde, P., Pam, S. D., Obadofin, M. O., et al. (2008). Cytokine-associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age. Malar. J. 7:41. doi: 10.1186/1475-2875-7-41
7. Boyles, J., and Bainton, D. F. (1981). Changes in plasma-membrane-associated filaments during endocytosis and exocytosis in polymorphonuclear leukocytes. Cell 24, 905-914
8. Branzk, N., Lubojemska, A., Hardison, S. E., Wang, Q., Gutierrez, M. G., Brown, G. D., et al. (2014). Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat. Immunol. 15, 1017-1025. doi: 10.1038/ni.2987
9. Bratton, D. L., and Henson, P. M. (2011). Neutrophil clearance: when the party is over, clean-up begins. Trends Immunol. 32, 350-357. doi: 10.1016/j.it.2011.04.009
10. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., et al. (2004). Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535. doi: 10.1126/science.1092385
11. Brummer, E., and Stevens, D. A. (1982). Opposite effects of human monocytes, macrophages, and polymorphonuclear neutrophils on replication of Blastomyces dermatitidis in vitro. Infect. Immun. 36, 297-303
12. Cartwright, G. E., Athens, J. W., and Wintrobe, M. M. (1964). The kinetics of granulopoiesis in normal man. Blood 24, 780-803
13. Casulli, S., and Elbim, C. (2014). Interactions between human immunodeficiency virus type 1 and polymorphonuclear neutrophils. J. Innate Immun. 6, 13-20. doi: 10.1159/000353588
14. Chen, A., and Seifert, H. S. (2011). Neisseria gonorrhoeae-mediated inhibition of apoptotic signalling in polymorphonuclear leukocytes. Infect. Immun. 79, 4447-4458. doi: 10.1128/IAI.01267-10
15. Christin, L., Wysong, D. R., Meshulam, T., Wang, S., and Diamond, R. D. (1997). Mechanisms and target sites of damage in killing of Candida albicans hyphae by human polymorphonuclear neutrophils. J. Infect. Dis. 176, 1567-1578
16. Chuah, C., Jones, M. K., Burke, M. L., Owen, H. C., Anthony, B. J., McManus, D. P., et al. (2013). Spatial and temporal transcriptomics of Schistosoma japonicum-induced hepatic granuloma formation reveals novel roles for neutrophils. J. Leukoc. Biol. 94, 353-365. doi: 10.1189/jlb.1212653
17. Colamussi, M. L., White, M. R., Crouch, E., and Hartshorn, K. L. (1999). Influenza A virus accelerates neutrophil apoptosis and markedly potentiates apoptotic effects of bacteria. Blood 93, 2395-2403
18. Colotta, F., Re, F., Polentarutti, N., Sozzani, S., and Mantovani, A. (1992). Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 80, 2012-2020
19. Coxon, A., Rieu, P., Barkalow, F. J., Askari, S., Sharpe, A. H., von Andrian, U. H., et al. (1996). A novel role for the β 2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity 5, 653-666
20. Cunnington, A. J., de Souza, J. B., Walther, M., and Riley, E. M. (2011). Malaria impairs resistance to Salmonella through heme-and heme oxygenase-dependent dysfunctional granulocyte mobilization. Nat. Med. 18, 120-127. doi: 10.1038/nm.2601
21. Cunnington, A. J., Njie, M., Correa, S., Takem, E. N., Riley, E. M., and Walther, M. (2012). Prolonged neutrophil dysfunction after Plasmodium falciparum malaria is related to hemolysis and heme oxygenase-1 induction. J. Immunol. 189, 5336-5346. doi: 10.4049/jimmunol.1201028
22. Dancey, J. T., Deubelbeiss, K. A., Harker, L. A., and Finch, C. A. (1976). Neutrophil kinetics in man. J. Clin. Invest. 58, 705-715. doi: 10.1172/JCI108517
23. Diep, B. A., Chan, L., Tattevin, P., Kajikawa, O., Martin, T. R., Basuino, L., et al. (2010). Polymorphonuclear leukocytes mediate Staphylococcus aureus Panton-Valentine leukocidin-induced lung inflammation and injury. Proc. Natl. Acad. Sci. U.S.A. 107, 5587-5592. doi: 10.1073/pnas.0912403107
24. Duffy, D., Perrin, H., Abadie, V., Benhabiles, N., Boissonnas, A., Liard, C., et al. (2012). Neutrophils transport antigen from the dermis to the bone marrow, initiating a source of memory CD8+ T cells. Immunity 37, 917-929. doi: 10.1016/j.immuni.2012.07.015
25. Fliedner, T. M., Cronkite, E. P., Killmann, S. A., and Bond, V. P. (1964). Granulocytopoiesis. Ii. Emergence and pattern of labeling of neutrophilic granulocytes in humans. Blood 24, 683-700
26. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., et al. (2007). Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231-241. doi: 10.1083/jcb.200606027
27. Gazendam, R. P., van Hamme, J. L., Tool, A. T., Hoogenboezem, M., van den Berg, J. M., Prins, J. M., et al. (2016). Human neutrophils use different mechanisms to kill Aspergillus fumigatus conidia and hyphae: evidence from phagocyte defects. J. Immunol. 196, 1272-1283. doi: 10.4049/jimmunol.1501811
28. Gazendam, R. P., van Hamme, J. L., Tool, A. T., van Houdt, M., Verkuijlen, P. J., Herbst, M., et al. (2014). Two independent killing mechanisms of Candida albicans by human neutrophils: evidence from innate immunity defects. Blood 124, 590-597. doi: 10.1182/blood-2014-01-551473
29. Geering, B., Stoeckle, C., Conus, S., and Simon, H. U. (2013). Living and dying for inflammation: neutrophils, eosinophils, basophils. Trends Immunol. 34, 398-409. doi: 10.1016/j.it.2013.04.002
30. Green, D. R., and Llambi, F. (2015). Cell death signaling. Cold Spring Harb. Perspect. Biol. 7:a006080. doi: 10.1101/cshperspect.a006080
31. Greenlee-Wacker, M. C., Rigby, K. M., Kobayashi, S. D., Porter, A. R., DeLeo, F. R., and Nauseef, W. M. (2014). Phagocytosis of Staphylococcus aureus by human neutrophils prevents macrophage efferocytosis and induces programmed necrosis. J. Immunol. 192, 4709-4717. doi: 10.4049/jimmunol.1302692
32. Grigg, J. M., Savill, J. S., Sarraf, C., Haslett, C., and Silverman, M. (1991). Neutrophil apoptosis and clearance from neonatal lungs. Lancet 338, 720-722
33. Grundy, J. E., Lawson, K. M., MacCormac, L. P., Fletcher, J. M., and Yong, K. L. (1998). 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 neutrophil transendothelial migration. J. Infect. Dis. 177, 1465-1474
34. Guimaraes-Costa, A. B., Nascimento, M. T., Froment, G. S., Soares, R. P., Morgado, F. N., Conceicao-Silva, F., et al. (2009). Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc. Natl. Acad. Sci. U.S.A. 106, 6748-6753. doi: 10.1073/pnas.0900226106
35. Hannah, S., Mecklenburgh, K., Rahman, I., Bellingan, G. J., Greening, A., Haslett, C., et al. (1995). Hypoxia prolongs neutrophil survival in vitro. FEBS Lett. 372, 233-237
36. Haslett, C., Lee, A., Savill, J. S., Meagher, L., and Whyte, M. K. (1991). Apoptosis (programmed cell death) and functional changes in aging neutrophils. Modulation by inflammatory mediators. Chest 99(3 Suppl.), 6S
37. Hazrati, E., Galen, B., Lu, W., Wang, W., Ouyang, Y., Keller, M. J., et al. (2006). Human a-and β-defensins block multiple steps in herpes simplex virus infection. J. Immunol. 177, 8658-8666. doi: 10.4049/jimmunol.177.12.8658
38. Hemmers, S., Teijaro, J. R., Arandjelovic, S., and Mowen, K. A. (2011). PAD4-mediated neutrophil extracellular trap formation is not required for immunity against influenza infection. PLoS ONE 6:e22043. doi: 10.1371/journal.pone.0022043
39. Henson, P. M. (1971). The immunologic release of constituents from neutrophil leukocytes. II. Mechanisms of release during phagocytosis, and adherence to nonphagocytosable surfaces. J. Immunol. 107, 1547-1557
40. Henson, P. M., and Johnston, R. B. Jr. (1987). Tissue injury in inflammation. Oxidants, proteinases, and cationic proteins. J. Clin. Invest. 79, 669-674. doi: 10.1172/JCI112869
41. Herant, M., Heinrich, V., and Dembo, M. (2006). Mechanics of neutrophil phagocytosis: experiments and quantitative models. J. Cell Sci. 119(Pt 9), 1903-1913. doi: 10.1242/jcs.02876
42. Hermosilla, C., Caro, T. M., Silva, L. M., Ruiz, A., and Taubert, A. (2014). The intriguing host innate immune response: novel anti-parasitic defence by neutrophil extracellular traps. Parasitology 141, 1489-1498. doi: 10.1017/S0031182014000316
43. Hurrell, B. P., Schuster, S., Grun, E., Coutaz, M., Williams, R. A., Held, W., et al. (2015). Rapid sequestration of Leishmania mexicana by neutrophils contributes to the development of chronic lesion. PLoS Pathog. 11:e1004929. doi: 10.1371/journal.ppat.1004929
44. Kaloriti, D., Jacobsen, M., Yin, Z., Patterson, M., Tillmann, A., Smith, D. A., et al. (2014). Mechanisms underlying the exquisite sensitivity of Candida albicans to combinatorial cationic and oxidative stress that enhances the potent fungicidal activity of phagocytes. MBio 5, e01334-e01314. doi: 10.1128/mBio.01334-14
45. Kennedy, A. D., and DeLeo, F. R. (2009). Neutrophil apoptosis and the resolution of infection. Immunol. Res. 43, 25-61. doi: 10.1007/s12026-008-8049-6
46. Kobayashi, S. D., Braughton, K. R., Whitney, A. R., Voyich, J. M., Schwan, T. G., Musser, J. M., et al. (2003). Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proc. Natl. Acad. Sci. U.S.A. 100, 10948-10953. doi: 10.1073/pnas.1833375100
47. Kobayashi, S. D., and DeLeo, F. R. (2009). Role of neutrophils in innate immunity: a systems biology-level approach. Wiley Interdiscip. Rev. Syst. Biol. Med. 1, 309-333. doi: 10.1002/wsbm.32
48. Kobayashi, S. D., Voyich, J. M., Buhl, C. L., Stahl, R. M., and DeLeo, F. R. (2002). Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: cell fate is regulated at the level of gene expression. Proc. Natl. Acad. Sci. U.S.A. 99, 6901-6906. doi: 10.1073/pnas.092148299
49. Larochelle, B., Flamand, L., Gourde, P., Beauchamp, D., and Gosselin, J. (1998). Epstein-Barr virus infects and induces apoptosis in human neutrophils. Blood 92, 291-299
50. Leal, S. M. Jr., Vareechon, C., Cowden, S., Cobb, B. A., Latge, J. P., Momany, M., et al. (2012). Fungal antioxidant pathways promote survival against neutrophils during infection. J. Clin. Invest. 122, 2482-2498. doi: 10.1172/JCI63239
51. Lee, A., Whyte, M. K., and Haslett, C. (1993). Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators. J. Leukoc. Biol. 54, 283-288
52. Lichtner, M., Mengoni, F., Mastroianni, C. M., Sauzullo, I., Rossi, R., De Nicola, M., et al. (2006). HIV protease inhibitor therapy reverses neutrophil apoptosis in AIDS patients by direct calpain inhibition. Apoptosis 11, 781-787. doi: 10.1007/s10495-006-5699-5
53. Lima-Junior, J. C., Rodrigues-da-Silva, R. N., Pereira, V. A., Storer, F. L., Perce-da-Silva, D. S., Fabrino, D. L., et al. (2012). Cells and mediators of inflammation (C-reactive protein, nitric oxide, platelets and neutrophils) in the acute and convalescent phases of uncomplicated Plasmodium vivax and Plasmodium falciparum infection. Mem. Inst. Oswaldo Cruz 107, 1035-1041. doi: 10.1590/S0074-02762012000800012
54. Lindemans, C. A., Coffer, P. J., Schellens, I. M., de Graaff, P. M., Kimpen, J. L., and Koenderman, L. (2006). Respiratory syncytial virus inhibits granulocyte apoptosis through a phosphatidylinositol 3-kinase and NF-?aB-dependent mechanism. J. Immunol. 176, 5529-5537. doi: 10.4049/jimmunol.176.9.5529
55. Lodge, K. M., Thompson, A. A., Chilvers, E. R., and Condliffe, A. M. (2017). Hypoxic regulation of neutrophil function and consequences for Staphylococcus aureus infection. Microbes Infect. 19, 166-176. doi: 10.1016/j.micinf.2016.10.005
56. Lotz, S., Aga, E., Wilde, I., van Zandbergen, G., Hartung, T., Solbach, W., et al. (2004). Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2. J. Leukoc. Biol. 75, 467-477. doi: 10.1189/jlb.0803360
57. Lu, T., Kobayashi, S. D., Quinn, M. T., and Deleo, F. R. (2012). A NET Outcome. Front. Immunol. 3:365. doi: 10.3389/fimmu.2012.00365
58. Macallan, D. C., Fullerton, C. A., Neese, R. A., Haddock, K., Park, S. S., and Hellerstein, M. K. (1998). Measurement of cell proliferation by labeling of DNA with stable isotope-labeled glucose: studies in vitro, in animals, and in humans. Proc. Natl. Acad. Sci. U.S.A. 95, 708-713
59. Maianski, N. A., Geissler, J., Srinivasula, S. M., Alnemri, E. S., Roos, D., and Kuijpers, T. W. (2004). Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death Differ. 11, 143-153. doi: 10.1038/sj.cdd.4401320
60. Malachowa, N., Kobayashi, S. D., Freedman, B., Dorward, D. W., and DeLeo, F. R. (2013). Staphylococcus aureus leukotoxin GH promotes formation of neutrophil extracellular traps. J. Immunol. 191, 6022-6029. doi: 10.4049/jimmunol.1301821
61. Malachowa, N., Kobayashi, S. D., Quinn, M. T., and DeLeo, F. R. (2016). NET Confusion. Front. Immunol. 7:259. doi: 10.3389/fimmu.2016.00259
62. Marciano, B. E., Spalding, C., Fitzgerald, A., Mann, D., Brown, T., Osgood, S., et al. (2015). Common severe infections in chronic granulomatous disease. Clin. Infect. Dis. 60, 1176-1183. doi: 10.1093/cid/ciu1154
63. McCaffrey, R. L., Schwartz, J. T., Lindemann, S. R., Moreland, J. G., Buchan, B. W., Jones, B. D., et al. (2010). Multiple mechanisms of NADPH oxidase inhibition by type A and type B Francisella tularensis. J. Leukoc. Biol. 88, 791-805. doi: 10.1189/jlb.1209811
64. McCoy, C. J., Reaves, B. J., Giguere, S., Coates, R., Rada, B., and Wolstenholme, A. J. (2017). Human leukocytes kill Brugia malayi microfilariae independently of DNA-based extracellular trap release. PLoS Negl. Trop. Dis. 11:e0005279. doi: 10.1371/journal.pntd.0005279
65. McCracken, J. M., Kinkead, L. C., McCaffrey, R. L., and Allen, L. A. (2016). Francisella tularensis modulates a distinct subset of regulatory factors and sustains mitochondrial integrity to impair human neutrophil apoptosis. J. Innate Immun. 8, 299-313. doi: 10.1159/000443882
66. McGovern, N. N., Cowburn, A. S., Porter, L., Walmsley, S. R., Summers, C., Thompson, A. A., et al. (2011). Hypoxia selectively inhibits respiratory burst activity and killing of Staphylococcus aureus in human neutrophils. J. Immunol. 186, 453-463. doi: 10.4049/jimmunol.1002213
67. Medeiros, A. I., Bonato, V. L., Malheiro, A., Dias, A. R., Silva, C. L., and Faccioli, L. H. (2002). Histoplasma capsulatum inhibits apoptosis and Mac-1 expression in leucocytes. Scand. J. Immunol. 56, 392-398. doi: 10.1046/j.1365-3083.2002.01142.x
68. Menegazzi, R., Decleva, E., and Dri, P. (2012). Killing by neutrophil extracellular traps: fact or folklore? Blood 119, 1214-1216. doi: 10.1182/blood-2011-07-364604
69. Narasaraju, T., Yang, E., Samy, R. P., Ng, H. H., Poh, W. P., Liew, A. A., et al. (2011). Excessive neutrophils and neutrophil extracellular traps contribute to acute lung injury of influenza pneumonitis. Am. J. Pathol. 179, 199-210. doi: 10.1016/j.ajpath.2011.03.013
70. Nauseef, W. M. (2007). How human neutrophils kill and degrade microbes: an integrated view. Immunol. Rev. 219, 88-102. doi: 10.1111/j.1600-065X.2007.00550.x
71. Nauseef, W. M., and Borregaard, N. (2014). Neutrophils at work. Nat. Immunol. 15, 602-611. doi: 10.1038/ni.2921
72. Nauseef, W. M., and Kubes, P. (2016). Pondering neutrophil extracellular traps with healthy skepticism. Cell. Microbiol. 18, 1349-1357. doi: 10.1111/cmi.12652
73. Newman, S. L., Gootee, L., and Gabay, J. E. (1993). Human neutrophil-mediated fungistasis against Histoplasma capsulatum. Localization of fungistatic activity to the azurophil granules. J. Clin. Invest. 92, 624-631. doi: 10.1172/JCI116630
74. Newman, S. L., Henson, J. E., and Henson, P. M. (1982). Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages. J. Exp. Med. 156, 430-442
75. O'Connell, A. E., Redding, K. M., Hess, J. A., Lok, J. B., Nolan, T. J., and Abraham, D. (2011). Soluble extract from the nematode Strongyloides stercoralis induces CXCR2 dependent/IL-17 independent neutrophil recruitment. Microbes Infect. 13, 536-544. doi: 10.1016/j.micinf.2011.01.016
76. Pillay, J., den Braber, I., Vrisekoop, N., Kwast, L. M., de Boer, R. J., Borghans, J. A., et al. (2010). In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 116, 625-627. doi: 10.1182/blood-2010-01-259028
77. Pilsczek, F. H., Salina, D., Poon, K. K., Fahey, C., Yipp, B. G., Sibley, C. D., et al. (2010). A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J. Immunol. 185, 7413-7425. doi: 10.4049/jimmunol.1000675
78. Pitrak, D. L., Tsai, H. C., Mullane, K. M., Sutton, S. H., and Stevens, P. (1996). Accelerated neutrophil apoptosis in the acquired immunodeficiency syndrome. J. Clin. Invest. 98, 2714-2719. doi: 10.1172/JCI119096
79. Porto, B. N., and Stein, R. T. (2016). Neutrophil extracellular traps in pulmonary diseases: too much of a good thing? Front. Immunol. 7:311. doi: 10.3389/fimmu.2016.00311
80. Ramirez, B. L., Howard, O. M., Dong, H. F., Edamatsu, T., Gao, P., Hartlein, M., et al. (2006). Brugia malayi asparaginyl-transfer RNA synthetase induces chemotaxis of human leukocytes and activates G-protein-coupled receptors CXCR1 and CXCR2. J. Infect. Dis. 193, 1164-1171. doi: 10.1086/501369
81. Ramos-Casals, M., Cuadrado, M. J., Alba, P., Sanna, G., Brito-Zeron, P., Bertolaccini, L., et al. (2008). Acute viral infections in patients with systemic lupus erythematosus: description of 23 cases and review of the literature. Medicine 87, 311-318. doi: 10.1097/MD.0b013e31818ec711
82. Robinet, P., Baychelier, F., Fontaine, T., Picard, C., Debre, P., Vieillard, V., et al. (2014). A polysaccharide virulence factor of a human fungal pathogen induces neutrophil apoptosis via NK cells. J. Immunol. 192, 5332-5342. doi: 10.4049/jimmunol.1303180
83. Rochael, N. C., Guimaraes-Costa, A. B., Nascimento, M. T., DeSouza-Vieira, T. S., Oliveira, M. P., Garcia e Souza, L. F., et al. (2015). Classical ROS-dependent and early/rapid ROS-independent release of neutrophil extracellular traps triggered by Leishmania parasites. Sci. Rep. 5:18302. doi: 10.1038/srep18302
84. Rotstein, D., Parodo, J., Taneja, R., and Marshall, J. C. (2000). Phagocytosis of Candida albicans induces apoptosis of human neutrophils. Shock 14, 278-283
85. Royer, D. J., Zheng, M., Conrady, C. D., and Carr, D. J. (2015). Granulocytes in ocular HSV-1 infection: opposing roles of mast cells and neutrophils. Invest. Ophthalmol. Vis. Sci. 56, 3763-3775. doi: 10.1167/iovs.15-16900
86. Sabroe, I., Prince, L. R., Jones, E. C., Horsburgh, M. J., Foster, S. J., Vogel, S. N., et al. (2003). Selective roles for Toll-like receptor (TLR)2 and TLR4 in the regulation of neutrophil activation and life span. J. Immunol. 170, 5268-5275. doi: 10.4049/jimmunol.170.10.5268
87. Saitoh, T., Komano, J., Saitoh, Y., Misawa, T., Takahama, M., Kozaki, T., et al. (2012). Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 12, 109-116. doi: 10.1016/j.chom.2012.05.015
88. Salmen, S., Montes, H., Soyano, A., Hernandez, D., and Berrueta, L. (2007). Mechanisms of neutrophil death in human immunodeficiency virus-infected patients: role of reactive oxygen species, caspases and map kinase pathways. Clin. Exp. Immunol. 150, 539-545. doi: 10.1111/j.1365-2249.2007.03524.x
89. Salmen, S., Teran, G., Borges, L., Goncalves, L., Albarran, B., Urdaneta, H., et al. (2004). Increased Fas-mediated apoptosis in polymorphonuclear cells from HIV-infected patients. Clin. Exp. Immunol. 137, 166-172. doi: 10.1111/j.1365-2249.2004.02503.x
90. Sarkar, A., Aga, E., Bussmeyer, U., Bhattacharyya, A., Moller, S., Hellberg, L., et al. (2013). Infection of neutrophil granulocytes with Leishmania major activates ERK 1/2 and modulates multiple apoptotic pathways to inhibit apoptosis. Med. Microbiol. Immunol. 202, 25-35. doi: 10.1007/s00430-012-0246-1
91. Savill, J., Dransfield, I., Hogg, N., and Haslett, C. (1990). Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343, 170-173. doi: 10.1038/343170a0
92. Savill, J. S., Wyllie, A. H., Henson, J. E., Walport, M. J., Henson, P. M., and Haslett, C. (1989). Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 83, 865-875. doi: 10.1172/JCI113970
93. Schaffner, A., Davis, C. E., Schaffner, T., Markert, M., Douglas, H., and Braude, A. I. (1986). In vitro susceptibility of fungi to killing by neutrophil granulocytes discriminates between primary pathogenicity and opportunism. J. Clin. Invest. 78, 511-524. doi: 10.1172/JCI112603
94. Schonrich, G., and Raftery, M. J. (2016). Neutrophil extracellular traps go viral. Front. Immunol. 7:366. doi: 10.3389/fimmu.2016.00366
95. Simon, H. U. (2003). Neutrophil apoptosis pathways and their modifications in inflammation. Immunol. Rev. 193, 101-110. doi: 10.1034/j.1600-065X.2003.00038.x
96. Simons, M. P., Nauseef, W. M., Griffith, T. S., and Apicella, M. A. (2006). Neisseria gonorrhoeae delays the onset of apoptosis in polymorphonuclear leukocytes. Cell. Microbiol. 8, 1780-1790. doi: 10.1111/j.1462-5822.2006.00748.x
97. Skaletskaya, A., Bartle, L. M., Chittenden, T., McCormick, A. L., Mocarski, E. S., and Goldmacher, V. S. (2001). A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc. Natl. Acad. Sci. U.S.A. 98, 7829-7834. doi: 10.1073/pnas.141108798
98. Skarman, P. J., Rahbar, A., Xie, X., and Soderberg-Naucler, C. (2006). Induction of polymorphonuclear leukocyte response by human cytomegalovirus. Microbes Infect. 8, 1592-1601. doi: 10.1016/j.micinf.2006.01.017
99. Smith, P., Fallon, R. E., Mangan, N. E., Walsh, C. M., Saraiva, M., Sayers, J. R., et al. (2005). Schistosoma mansoni secretes a chemokine binding protein with antiinflammatory activity. J. Exp. Med. 202, 1319-1325. doi: 10.1084/jem.20050955
100. Summers, C., Rankin, S. M., Condliffe, A. M., Singh, N., Peters, A. M., and Chilvers, E. R. (2010). Neutrophil kinetics in health and disease. Trends Immunol. 31, 318-324. doi: 10.1016/j.it.2010.05.006
101. Tak, T., Tesselaar, K., Pillay, J., Borghans, J. A., and Koenderman, L. (2013). What's your age again? Determination of human neutrophil half-lives revisited. J. Leukoc. Biol. 94, 595-601. doi: 10.1189/jlb.1112571
102. Ting-Beall, H. P., Needham, D., and Hochmuth, R. M. (1993). Volume and osmotic properties of human neutrophils. Blood 81, 2774-2780
103. Urban, C. F., Reichard, U., Brinkmann, V., and Zychlinsky, A. (2006). Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell. Microbiol. 8, 668-676. doi: 10.1111/j.1462-5822.2005.00659.x
104. van Zandbergen, G., Bollinger, A., Wenzel, A., Kamhawi, S., Voll, R., Klinger, M., et al. (2006). Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc. Natl. Acad. Sci. U.S.A. 103, 13837-13842. doi: 10.1073/pnas.0600843103
105. van Zandbergen, G., Gieffers, J., Kothe, H., Rupp, J., Bollinger, A., Aga, E., et al. (2004). Chlamydia pneumoniae multiply in neutrophil granulocytes and delay their spontaneous apoptosis. J. Immunol. 172, 1768-1776. doi: 10.4049/jimmunol.172.3.1768
106. Ventura-Juarez, J., Campos-Esparza, M., Pacheco-Yepez, J., Lopez-Blanco, J. A., Adabache-Ortiz, A., Silva-Briano, M., et al. (2016). Entamoeba histolytica induces human neutrophils to form NETs. Parasite Immunol. 38, 503-509. doi: 10.1111/pim.12332
107. Voll, R. E., Herrmann, M., Roth, E. A., Stach, C., Kalden, J. R., and Girkontaite, I. (1997). Immunosuppressive effects of apoptotic cells. Nature 390, 350-351. doi: 10.1038/37022
108. Wallach, D., Kang, T. B., Dillon, C. P., and Green, D. R. (2016). Programmed necrosis in inflammation: Toward identification of the effector molecules. Science 352:aaf2154. doi: 10.1126/science.aaf2154
109. Walmsley, S. R., Print, C., Farahi, N., Peyssonnaux, C., Johnson, R. S., Cramer, T., et al. (2005). Hypoxia-induced neutrophil survival is mediated by HIF-1a-dependent NF-κaB activity. J. Exp. Med. 201, 105-115. doi: 10.1084/jem.20040624
110. Wang, X., van de Veerdonk, F. L., and Netea, M. G. (2016). Basic Genetics and Immunology of Candida Infections. Infect. Dis. Clin. North Am. 30, 85-102. doi: 10.1016/j.idc.2015.10.010
111. Watson, R. W., Redmond, H. P., Wang, J. H., and Bouchier-Hayes, D. (1996a). Bacterial ingestion, tumor necrosis factor-a, and heat induce programmed cell death in activated neutrophils. Shock 5, 47-51
112. Watson, R. W., Redmond, H. P., Wang, J. H., Condron, C., and Bouchier-Hayes, D. (1996b). Neutrophils undergo apoptosis following ingestion of Escherichia coli. J. Immunol. 156, 3986-3992
113. Weiss, S. J. (1989). Tissue destruction by neutrophils. N. Engl. J. Med. 320, 365-376. doi: 10.1056/NEJM198902093200606
114. Wenzel, A., and van Zandbergen, G. (2009). Lipoxin A4 receptor dependent leishmania infection. Autoimmunity 42, 331-333. doi: 10.1080/08916930902828239
115. Whyte, M. K., Meagher, L. C., MacDermot, J., and Haslett, C. (1993). Impairment of function in aging neutrophils is associated with apoptosis. J. Immunol. 150, 5124-5134
116. Wozniok, I., Hornbach, A., Schmitt, C., Frosch, M., Einsele, H., Hube, B., et al. (2008). Induction of ERK-kinase signalling triggers morphotype-specific killing of Candida albicans filaments by human neutrophils. Cell. Microbiol. 10, 807-820. doi: 10.1111/j.1462-5822.2007.01086.x
117. Wright, D. G., and Gallin, J. I. (1979). Secretory responses of human neutrophils: exocytosis of specific (secondary) granules by human neutrophils during adherence in vitro and during exudation in vivo. J. Immunol. 123, 285-294
118. Yizengaw, E., Getahun, M., Tajebe, F., Cruz Cervera, E., Adem, E., Mesfin, G., et al. (2016). Visceral leishmaniasis patients display altered composition and maturity of neutrophils as well as impaired neutrophil effector functions. Front. Immunol. 7:517. doi: 10.3389/fimmu.2016.00517
119. Yoshiie, K., Kim, H. Y., Mott, J., and Rikihisa, Y. (2000). Intracellular infection by the human granulocytic ehrlichiosis agent inhibits human neutrophil apoptosis. Infect. Immun. 68, 1125-1133. doi: 10.1128/IAI.68.3.1125-1133.2000
120. 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 Differ. 16, 1438-1444. doi: 10.1038/cdd.2009.96
121. Yousefi, S., and Simon, H. U. (2016). NETosis-does it really represent nature's "suicide bomber"? Front. Immunol. 7:328. doi: 10.3389/fimmu.2016.00328