Neutrophils in innate immunity and systems biology‐level approaches

UPDATE

Viktoria Rungelrath, Scott D. Kobayashi, Frank R. DeLeo

Published Online: Jun 20 2019

DOI: 10.1002/wsbm.1458

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Abstract The innate immune system is the first line of host defense against invading microorganisms. Polymorphonuclear leukocytes (PMNs or neutrophils) are the most abundant leukocyte in humans and essential to the innate immune response against invading pathogens. Compared to the acquired immune response, which requires time to develop and is dependent on previous interaction with specific microbes, the ability of neutrophils to kill microorganisms is immediate, nonspecific, and not dependent on previous exposure to microorganisms. Historically, studies of PMN‐pathogen interaction focused on the events leading to killing of microorganisms, such as recruitment/chemotaxis, transmigration, phagocytosis, and activation, whereas postphagocytosis sequelae were infrequently considered. In addition, it was widely accepted that human neutrophils possessed limited capacity for new gene transcription and thus, relatively little biosynthetic capacity. This notion has changed dramatically within the past 20 years. Further, there is now more effort directed to understand the events occurring in PMNs after killing of microbes. Herein, we give an updated review of the systems biology‐level approaches that have been used to gain an enhanced view of the role of neutrophils during host‐pathogen interaction and neutrophil‐mediated diseases. We anticipate that these and future systems‐level studies will continue to provide information important for understanding, treatment, and control of diseases caused by pathogenic microorganisms. This article is categorized under: Physiology > Organismal Responses to Environment Physiology > Mammalian Physiology in Health and Disease Biological Mechanisms > Cell Fates

Overview of neutrophil functions / processes that have been investigated using proteomics, transcriptomics, genomics and lipidomics. PICD, phagocytosis‐induced cell death. See text for details

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A schematic that illustrates possible outcomes of microbe‐neutrophil interaction. See text for details

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Neutrophil apoptosis. Human neutrophils were isolated from venous blood and then processed for transmission electron microscopy or stained with Wright‐Giemsa (inset) after purification (0 hr) or 24 hr in culture

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Neutrophil phagocytosis and microbicidal process. Panel (a) illustrates binding and phagocytosis of a microbe opsonized with antibody or serum complement. Phagocytosis triggers production of superoxide (O₂^•–) from which other secondarily derived ROS are formed, including hydrogen peroxide (H₂O₂) and hypochlorous acid (HOCl). Panel (b) is a transmission electron micrograph of a human neutrophil that has phagocytosed numerous Staphylococcus aureus (Microbe)

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References

Ackerman,, A. L., Kyritsis,, C., Tampe,, R., & Cresswell,, P. (2003). Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proceedings of the National Academy of Sciences of the United States of America, 100(22), 12889–12894. https://doi.org/10.1073/pnas.1735556100
Aglietta,, M., Piacibello,, W., Sanavio,, F., Stacchini,, A., Apra,, F., Schena,, M., … Gavosto,, F. (1989). Kinetics of human hemopoietic cells after in vivo administration of granulocyte‐macrophage colony‐stimulating factor. The Journal of Clinical Investigation, 83(2), 551–557. https://doi.org/10.1172/JCI113917
Albrechtsen,, M., Yeaman,, G. R., & Kerr,, M. A. (1988). Characterization of the IgA receptor from human polymorphonuclear leucocytes. Immunology, 64(2), 201–205.
Alvarado‐Kristensson,, M., Melander,, F., Leandersson,, K., Ronnstrand,, L., Wernstedt,, C., & Andersson,, T. (2004). p38‐MAPK signals survival by phosphorylation of caspase‐8 and caspase‐3 in human neutrophils. The Journal of Experimental Medicine, 199(4), 449–458. https://doi.org/10.1084/jem.20031771
Athens,, J. W., Haab,, O. P., Raab,, S. O., Mauer,, A. M., Ashenbrucker,, H., Cartwright,, G. E., & Wintrobe,, M. M. (1961). Leukokinetic studies. IV. The total blood, circulating and marginal granulocyte pools and the granulocyte turnover rate in normal subjects. The Journal of Clinical Investigation, 40, 989–995. https://doi.org/10.1172/JCI104338
Avdi,, N. J., Nick,, J. A., Whitlock,, B. B., Billstrom,, M. A., Henson,, P. M., Johnson,, G. L., & Worthen,, G. S. (2001). Tumor necrosis factor‐alpha activation of the c‐Jun N‐terminal kinase pathway in human neutrophils. Integrin involvement in a pathway leading from cytoplasmic tyrosine kinases apoptosis. The Journal of Biological Chemistry, 276(3), 2189–2199. https://doi.org/10.1074/jbc.M007527200
Avraham,, R., Haseley,, N., Brown,, D., Penaranda,, C., Jijon,, H. B., Trombetta,, J. J., … Hung,, D. T. (2015). Pathogen cell‐to‐cell variability drives heterogeneity in host immune responses. Cell, 162(6), 1309–1321. https://doi.org/10.1016/j.cell.2015.08.027
Bainton,, D. F., Ullyot,, J. L., & Farquhar,, M. G. (1971). The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. The Journal of Experimental Medicine, 134(4), 907–934.
Banerjee,, R., Anguita,, J., Roos,, D., & Fikrig,, E. (2000). Cutting edge: Infection by the agent of human granulocytic ehrlichiosis prevents the respiratory burst by down‐regulating gp91phox. Journal of Immunology, 164(8), 3946–3949.
Bauernfeind,, F., Rieger,, A., Schildberg,, F. A., Knolle,, P. A., Schmid‐Burgk,, J. L., & Hornung,, V. (2012). NLRP3 inflammasome activity is negatively controlled by miR‐223. Journal of Immunology, 189(8), 4175–4181. https://doi.org/10.4049/jimmunol.1201516
Baumann,, R., Casaulta,, C., Simon,, D., Conus,, S., Yousefi,, S., & Simon,, H. U. (2003). Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria‐dependent death pathway. The FASEB Journal, 17(15), 2221–2230. https://doi.org/10.1096/fj.03-0110com
Bellocchio,, S., Moretti,, S., Perruccio,, K., Fallarino,, F., Bozza,, S., Montagnoli,, C., … Romani,, L. (2004). TLRs govern neutrophil activity in aspergillosis. Journal of Immunology, 173(12), 7406–7415.
Biffl,, W. L., Moore,, E. E., Moore,, F. A., & Barnett,, C. C., Jr. (1995). Interleukin‐6 suppression of neutrophil apoptosis is neutrophil concentration dependent. Journal of Leukocyte Biology, 58(5), 582–584.
Boldt,, K., Rist,, W., Weiss,, S. M., Weith,, A., & Lenter,, M. C. (2006). FPRL‐1 induces modifications of migration‐associated proteins in human neutrophils. Proteomics, 6(17), 4790–4799. https://doi.org/10.1002/pmic.200600121
Borjesson,, D. L., Kobayashi,, S. D., Whitney,, A. R., Voyich,, J. M., Argue,, C. M., & DeLeo,, F. R. (2005). Insights into pathogen immune evasion mechanisms: Anaplasma phagocytophilum fails to induce an apoptosis differentiation program in human neutrophils. Journal of Immunology, 174(10), 6364–6372.
Bours,, M. J., Swennen,, E. L., Di Virgilio,, F., Cronstein,, B. N., & Dagnelie,, P. C. (2006). Adenosine 5′‐triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacology %26 Therapeutics, 112(2), 358–404. https://doi.org/10.1016/j.pharmthera.2005.04.013
Boxer,, L. A., Axtell,, R., & Suchard,, S. (1990). The role of the neutrophil in inflammatory diseases of the lung. Blood Cells, 16(1), 25–40 discussion 41‐22.
Brigotti,, M., Carnicelli,, D., Ravanelli,, E., Barbieri,, S., Ricci,, F., Bontadini,, A., … Tazzari,, P. L. (2008). Interactions between Shiga toxins and human polymorphonuclear leukocytes. Journal of Leukocyte Biology, 84(4), 1019–1027. https://doi.org/10.1189/jlb.0308157
Brown,, G. E., Stewart,, M. Q., Bissonnette,, S. A., Elia,, A. E., Wilker,, E., & Yaffe,, M. B. (2004). Distinct ligand‐dependent roles for p38 MAPK in priming and activation of the neutrophil NADPH oxidase. The Journal of Biological Chemistry, 279(26), 27059–27068. https://doi.org/10.1074/jbc.M314258200
Brown,, S. B., & Savill,, J. (1999). Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. Journal of Immunology, 162(1), 480–485.
Burlak,, C., Whitney,, A. R., Mead,, D. J., Hackstadt,, T., & DeLeo,, F. R. (2006). Maturation of human neutrophil phagosomes includes incorporation of molecular chaperones and endoplasmic reticulum quality control machinery. Molecular %26 Cellular Proteomics, 5(4), 620–634. https://doi.org/10.1074/mcp.M500336-MCP200
Carlyon,, J. A., Abdel‐Latif,, D., Pypaert,, M., Lacy,, P., & Fikrig,, E. (2004). Anaplasma phagocytophilum utilizes multiple host evasion mechanisms to thwart NADPH oxidase‐mediated killing during neutrophil infection. Infection and Immunity, 72(8), 4772–4783. https://doi.org/10.1128/IAI.72.8.4772-4783.2004
Carlyon,, J. A., Chan,, W. T., Galan,, J., Roos,, D., & Fikrig,, E. (2002). Repression of rac2 mRNA expression by Anaplasma phagocytophila is essential to the inhibition of superoxide production and bacterial proliferation. Journal of Immunology, 169(12), 7009–7018.
Chen,, H., Ye,, F., & Guo,, G. (2019). Revolutionizing immunology with single‐cell RNA sequencing. Cellular %26 Molecular Immunology, 16(3), 242–249. https://doi.org/10.1038/s41423-019-0214-4
Chu,, L. F., Leng,, N., Zhang,, J., Hou,, Z., Mamott,, D., Vereide,, D. T., … Thomson,, J. A. (2016). Single‐cell RNA‐seq reveals novel regulators of human embryonic stem cell differentiation to definitive endoderm. Genome Biology, 17(1), 173. https://doi.org/10.1186/s13059-016-1033-x
Cline,, M. J. (1966a). Phagocytosis and synthesis of ribonucleic acid in human granulocytes. Nature, 212(5069), 1431–1433.
Cline,, M. J. (1966b). Ribonucleic acid biosynthesis in human leukocytes: The fate of rapidly labeled RNA in normal and abnormal leukocytes. Blood, 28(5), 650–664.
Cline,, M. J. (1975). Production and distribution of neutrophils. In M. J. Cline, (Ed.), The white cell (pp. 22–38). Cambridge, MA: Harvard University Press.
Cohn,, Z. A., & Morse,, S. I. (1960). Functional and metabolic properties of polymorphonuclear leucocytes. II. The influence of a lipopolysaccharide endotoxin. The Journal of Experimental Medicine, 111, 689–704.
Coldren,, C. D., Nick,, J. A., Poch,, K. R., Woolum,, M. D., Fouty,, B. W., O`Brien,, J. M., … Geraci,, M. W. (2006). Functional and genomic changes induced by alveolar transmigration in human neutrophils. American Journal of Physiology Lung Cellular and Molecular Physiology, 291(6), L1267–L1276. https://doi.org/10.1152/ajplung.00097.2006
Colotta,, F., Re,, F., Polentarutti,, N., Sozzani,, S., & Mantovani,, A. (1992). Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood, 80(8), 2012–2020.
Conus,, S., Perozzo,, R., Reinheckel,, T., Peters,, C., Scapozza,, L., Yousefi,, S., & Simon,, H. U. (2008). Caspase‐8 is activated by cathepsin D initiating neutrophil apoptosis during the resolution of inflammation. The Journal of Experimental Medicine, 205(3), 685–698. https://doi.org/10.1084/jem.20072152
Cooper,, D., Lindberg,, F. P., Gamble,, J. R., Brown,, E. J., & Vadas,, M. A. (1995). Transendothelial migration of neutrophils involves integrin‐associated protein (CD47). Proceedings of the National Academy of Sciences of the United States of America, 92(9), 3978–3982.
Cowland,, J. B., & Borregaard,, N. (2016). Granulopoiesis and granules of human neutrophils. Immunological Reviews, 273(1), 11–28. https://doi.org/10.1111/imr.12440
Coxon,, A., Rieu,, P., Barkalow,, F. J., Askari,, S., Sharpe,, A. H., von Andrian,, U. H., … Mayadas,, T. N. (1996). A novel role for the beta 2 integrin CD11b/CD18 in neutrophil apoptosis: A homeostatic mechanism in inflammation. Immunity, 5(6), 653–666.
Cronkite,, E. P., & Fliedner,, T. M. (1964). Granulocytopoiesis. The New England Journal of Medicine, 270, 1403–1408 CONCL. https://doi.org/10.1056/NEJM196406252702608
Curnutte,, J. T., Scott,, P. J., & Mayo,, L. A. (1989). Cytosolic components of the respiratory burst oxidase: Resolution of four components, two of which are missing in complementing types of chronic granulomatous disease. Proceedings of the National Academy of Sciences of the United States of America, 86(3), 825–829.
Dahinden,, C., Galanos,, C., & Fehr,, J. (1983). Granulocyte activation by endotoxin. I. Correlation between adherence and other granulocyte functions, and role of endotoxin structure on biologic activity. Journal of Immunology, 130(2), 857–862.
Dale,, D. C., Liles,, W. C., Llewellyn,, C., & Price,, T. H. (1998). Effects of granulocyte‐macrophage colony‐stimulating factor (GM‐CSF) on neutrophil kinetics and function in normal human volunteers. American Journal of Hematology, 57(1), 7–15.
Dalli,, J., & Serhan,, C. N. (2012). Specific lipid mediator signatures of human phagocytes: Microparticles stimulate macrophage efferocytosis and pro‐resolving mediators. Blood, 120(15), e60–e72. https://doi.org/10.1182/blood-2012-04-423525
Dana,, N., Todd,, R. F., 3rd, Pitt,, J., Springer,, T. A., & Arnaout,, M. A. (1984). Deficiency of a surface membrane glycoprotein (Mo1) in man. The Journal of Clinical Investigation, 73(1), 153–159. https://doi.org/10.1172/JCI111186
Dancey,, J. T., Deubelbeiss,, K. A., Harker,, L. A., & Finch,, C. A. (1976). Neutrophil kinetics in man. The Journal of Clinical Investigation, 58(3), 705–715. https://doi.org/10.1172/JCI108517
Dang,, P. M., Dewas,, C., Gaudry,, M., Fay,, M., Pedruzzi,, E., Gougerot‐Pocidalo,, M. A., & El Benna,, J. (1999). Priming of human neutrophil respiratory burst by granulocyte/macrophage colony‐stimulating factor (GM‐CSF) involves partial phosphorylation of p47(phox). The Journal of Biological Chemistry, 274(29), 20704–20708.
Davis,, M. M., Tato,, C. M., & Furman,, D. (2017). Systems immunology: just getting started. Nature Immunology, 18(7), 725–732. https://doi.org/10.1038/ni.3768
Davis,, S. D., Schaller,, J., & Wedgwood,, R. J. (1966). Job`s syndrome. Recurrent, "cold", staphylococcal abscesses. Lancet, 1(7445), 1013–1015.
DeLeo,, F. R. (2004). Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis, 9(4), 399–413. https://doi.org/10.1023/B:APPT.0000031448.64969.fa
DeLeo,, F. R., & Nauseef,, W. M. (2014). Granulocytic phagocytes. In J. E. Bennett,, R. Dolin,, & M. J. Blaser, (Eds.), Mandell, douglas, and bennett`s principles and practice of infectious diseases (Vol. 1, 8th ed., pp. 78–92). Philadelphia, PA: Elsevier Saunders.
DeLeo,, F. R., Renee,, J., McCormick,, S., Nakamura,, M., Apicella,, M., Weiss,, J. P., & Nauseef,, W. M. (1998). Neutrophils exposed to bacterial lipopolysaccharide upregulate NADPH oxidase assembly. The Journal of Clinical Investigation, 101(2), 455–463. https://doi.org/10.1172/JCI949
Diamond,, M. S., Staunton,, D. E., de Fougerolles,, A. R., Stacker,, S. A., Garcia‐Aguilar,, J., Hibbs,, M. L., & Springer,, T. A. (1990). ICAM‐1 (CD54): A counter‐receptor for mac‐1 (CD11b/CD18). The Journal of Cell Biology, 111(6 Pt 2), 3129–3139.
Dorhoi,, A., Iannaccone,, M., Farinacci,, M., Fae,, K. C., Schreiber,, J., Moura‐Alves,, P., … Kaufmann,, S. H. (2013). MicroRNA‐223 controls susceptibility to tuberculosis by regulating lung neutrophil recruitment. The Journal of Clinical Investigation, 123(11), 4836–4848. https://doi.org/10.1172/JCI67604
Dunican,, A. L., Leuenroth,, S. J., Ayala,, A., & Simms,, H. H. (2000). CXC chemokine suppression of polymorphonuclear leukocytes apoptosis and preservation of function is oxidative stress independent. Shock, 13(3), 244–250.
Ecker,, S., Chen,, L., Pancaldi,, V., Bagger,, F. O., Fernandez,, J. M., Carrillo de Santa Pau,, E., … Paul,, D. S. (2017). Genome‐wide analysis of differential transcriptional and epigenetic variability across human immune cell types. Genome Biology, 18(1), 18. https://doi.org/10.1186/s13059-017-1156-8
Edwards,, S. W., & Hallett,, M. B. (1997). Seeing the wood for the trees: The forgotten role of neutrophils in rheumatoid arthritis. Immunology Today, 18(7), 320–324.
Eggleton,, P., Ghebrehiwet,, B., Sastry,, K. N., Coburn,, J. P., Zaner,, K. S., Reid,, K. B., & Tauber,, A. I. (1995). Identification of a gC1q‐binding protein (gC1q‐R) on the surface of human neutrophils. Subcellular localization and binding properties in comparison with the cC1q‐R. The Journal of Clinical Investigation, 95(4), 1569–1578. https://doi.org/10.1172/JCI117830
Ehrengruber,, M. U., Geiser,, T., & Deranleau,, D. A. (1994). Activation of human neutrophils by C3a and C5A. Comparison of the effects on shape changes, chemotaxis, secretion, and respiratory burst. FEBS Letters, 346(2–3), 181–184.
El Kebir,, D., Jozsef,, L., Khreiss,, T., & Filep,, J. G. (2006). Inhibition of K+ efflux prevents mitochondrial dysfunction, and suppresses caspase‐3‐, apoptosis‐inducing factor‐, and endonuclease G‐mediated constitutive apoptosis in human neutrophils. Cellular Signalling, 18(12), 2302–2313. https://doi.org/10.1016/j.cellsig.2006.05.013
Ellison,, M. A., Gearheart,, C. M., Porter,, C. C., & Ambruso,, D. R. (2017). IFN‐gamma alters the expression of diverse immunity related genes in a cell culture model designed to represent maturing neutrophils. PLoS One, 12(10), e0185956. https://doi.org/10.1371/journal.pone.0185956
Engelich,, G., White,, M., & Hartshorn,, K. L. (2001). Neutrophil survival is markedly reduced by incubation with influenza virus and Streptococcus pneumoniae: Role of respiratory burst. Journal of Leukocyte Biology, 69(1), 50–56.
Fadok,, V. A., Savill,, J. S., Haslett,, C., Bratton,, D. L., Doherty,, D. E., Campbell,, P. A., & Henson,, P. M. (1992). Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. Journal of Immunology, 149(12), 4029–4035.
Fazi,, F., Rosa,, A., Fatica,, A., Gelmetti,, V., De Marchis,, M. L., Nervi,, C., & Bozzoni,, I. (2005). A minicircuitry comprised of microRNA‐223 and transcription factors NFI‐A and C/EBPalpha regulates human granulopoiesis. Cell, 123(5), 819–831. https://doi.org/10.1016/j.cell.2005.09.023
Fessler,, M. B., Malcolm,, K. C., Duncan,, M. W., & Worthen,, G. S. (2002). A genomic and proteomic analysis of activation of the human neutrophil by lipopolysaccharide and its mediation by p38 mitogen‐activated protein kinase. The Journal of Biological Chemistry, 277(35), 31291–31302. https://doi.org/10.1074/jbc.M200755200
Fleit,, H. B., Wright,, S. D., & Unkeless,, J. C. (1982). Human neutrophil Fc gamma receptor distribution and structure. Proceedings of the National Academy of Sciences of the United States of America, 79(10), 3275–3279.
Fliedner,, T. M., Cronkite,, E. P., Killmann,, S. A., & Bond,, V. P. (1964). Granulocytopoiesis. Ii. Emergence and pattern of labeling of Neutrophilic granulocytes in humans. Blood, 24, 683–700.
Fliedner,, T. M., Cronkite,, E. P., & Robertson,, J. S. (1964). Granulocytopoiesis. I. Senescence and random loss of Neutrophilic granulocytes in human beings. Blood, 24, 402–414.
Fossati,, G., Moulding,, D. A., Spiller,, D. G., Moots,, R. J., White,, M. R., & Edwards,, S. W. (2003). The mitochondrial network of human neutrophils: Role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis. Journal of Immunology, 170(4), 1964–1972.
Fradin,, C., Mavor,, A. L., Weindl,, G., Schaller,, M., Hanke,, K., Kaufmann,, S. H., … Hube,, B. (2007). The early transcriptional response of human granulocytes to infection with Candida albicans is not essential for killing but reflects cellular communications. Infection and Immunity, 75(3), 1493–1501. https://doi.org/10.1128/IAI.01651-06
Francois,, S., El Benna,, J., Dang,, P. M., Pedruzzi,, E., Gougerot‐Pocidalo,, M. A., & Elbim,, C. (2005). Inhibition of neutrophil apoptosis by TLR agonists in whole blood: Involvement of the phosphoinositide 3‐kinase/Akt and NF‐kappaB signaling pathways, leading to increased levels of Mcl‐1, A1, and phosphorylated Bad. Journal of Immunology, 174(6), 3633–3642.
Friedman,, A. D. (2002). Transcriptional regulation of granulocyte and monocyte development. Oncogene, 21(21), 3377–3390. https://doi.org/10.1038/sj.onc.1205324
Gagnon,, E., Bergeron,, J. J., & Desjardins,, M. (2005). ER‐mediated phagocytosis: Myth or reality? Journal of Leukocyte Biology, 77(6), 843–845. https://doi.org/10.1189/jlb.0305129
Gagnon,, E., Duclos,, S., Rondeau,, C., Chevet,, E., Cameron,, P. H., Steele‐Mortimer,, O., … Desjardins,, M. (2002). Endoplasmic reticulum‐mediated phagocytosis is a mechanism of entry into macrophages. Cell, 110(1), 119–131.
Gamberale,, R., Giordano,, M., Trevani,, A. S., Andonegui,, G., & Geffner,, J. R. (1998). Modulation of human neutrophil apoptosis by immune complexes. Journal of Immunology, 161(7), 3666–3674.
Gantier,, M. P. (2013). The not‐so‐neutral role of microRNAs in neutrophil biology. Journal of Leukocyte Biology, 94(4), 575–583. https://doi.org/10.1189/jlb.1012539
Gardai,, S., Whitlock,, B. B., Helgason,, C., Ambruso,, D., Fadok,, V., Bratton,, D., & Henson,, P. M. (2002). Activation of SHIP by NADPH oxidase‐stimulated Lyn leads to enhanced apoptosis in neutrophils. The Journal of Biological Chemistry, 277(7), 5236–5246. https://doi.org/10.1074/jbc.M110005200
Garin,, J., Diez,, R., Kieffer,, S., Dermine,, J. F., Duclos,, S., Gagnon,, E., … Desjardins,, M. (2001). The phagosome proteome: Insight into phagosome functions. The Journal of Cell Biology, 152(1), 165–180.
Gaublomme,, J. T., Yosef,, N., Lee,, Y., Gertner,, R. S., Yang,, L. V., Wu,, C., … Regev,, A. (2015). Single‐cell genomics unveils critical regulators of Th17 cell pathogenicity. Cell, 163(6), 1400–1412. https://doi.org/10.1016/j.cell.2015.11.009
Genestier,, A. L., Michallet,, M. C., Prevost,, G., Bellot,, G., Chalabreysse,, L., Peyrol,, S., … Genestier,, L. (2005). Staphylococcus aureus Panton‐valentine leukocidin directly targets mitochondria and induces Bax‐independent apoptosis of human neutrophils. The Journal of Clinical Investigation, 115(11), 3117–3127. https://doi.org/10.1172/JCI22684
Gombart,, A. F., Krug,, U., O`Kelly,, J., An,, E., Vegesna,, V., & Koeffler,, H. P. (2005). Aberrant expression of neutrophil and macrophage‐related genes in a murine model for human neutrophil‐specific granule deficiency. Journal of Leukocyte Biology, 78(5), 1153–1165. https://doi.org/10.1189/jlb.0504286
Gombart,, A. F., Shiohara,, M., Kwok,, S. H., Agematsu,, K., Komiyama,, A., & Koeffler,, H. P. (2001). Neutrophil‐specific granule deficiency: Homozygous recessive inheritance of a frameshift mutation in the gene encoding transcription factor CCAAT/enhancer binding protein—epsilon. Blood, 97(9), 2561–2567.
Gounni,, A. S., Lamkhioued,, B., Koussih,, L., Ra,, C., Renzi,, P. M., & Hamid,, Q. (2001). Human neutrophils express the high‐affinity receptor for immunoglobulin E (Fc epsilon RI): Role in asthma. The FASEB Journal, 15(6), 940–949.
Grabowski,, P., Hesse,, S., Hollizeck,, S., Rohlfs,, M., Behrends,, U., Sherkat,, R., … Rappsilber,, J. (2019). Proteome analysis of human neutrophil granulocytes from patients with monogenic disease using data‐independent acquisition. Molecular %26 Cellular Proteomics, 18, 760–772. https://doi.org/10.1074/mcp.RA118.001141
Guermonprez,, P., Saveanu,, L., Kleijmeer,, M., Davoust,, J., Van Endert,, P., & Amigorena,, S. (2003). ER‐phagosome fusion defines an MHC class I cross‐presentation compartment in dendritic cells. Nature, 425(6956), 397–402. https://doi.org/10.1038/nature01911
Guichard,, C., Pedruzzi,, E., Dewas,, C., Fay,, M., Pouzet,, C., Bens,, M., … Elbim,, C. (2005). Interleukin‐8‐induced priming of neutrophil oxidative burst requires sequential recruitment of NADPH oxidase components into lipid rafts. The Journal of Biological Chemistry, 280(44), 37021–37032. https://doi.org/10.1074/jbc.M506594200
Gurol,, T., Zhou,, W., & Deng,, Q. (2016). MicroRNAs in neutrophils: Potential next generation therapeutics for inflammatory ailments. Immunological Reviews, 273(1), 29–47. https://doi.org/10.1111/imr.12450
Guthrie,, L. A., McPhail,, L. C., Henson,, P. M., & Johnston,, R. B., Jr. (1984). Priming of neutrophils for enhanced release of oxygen metabolites by bacterial lipopolysaccharide. Evidence for increased activity of the superoxide‐producing enzyme. The Journal of Experimental Medicine, 160(6), 1656–1671.
Hamers,, M. N., de Boer,, M., Meerhof,, L. J., Weening,, R. S., & Roos,, D. (1984). Complementation in monocyte hybrids revealing genetic heterogeneity in chronic granulomatous disease. Nature, 307(5951), 553–555.
Hannah,, S., Mecklenburgh,, K., Rahman,, I., Bellingan,, G. J., Greening,, A., Haslett,, C., & Chilvers,, E. R. (1995). Hypoxia prolongs neutrophil survival in vitro. FEBS Letters, 372(2–3), 233–237.
Hart,, S. P., Ross,, J. A., Ross,, K., Haslett,, C., & Dransfield,, I. (2000). Molecular characterization of the surface of apoptotic neutrophils: Implications for functional downregulation and recognition by phagocytes. Cell Death and Differentiation, 7(5), 493–503. https://doi.org/10.1038/sj.cdd.4400680
Hayashi,, F., Means,, T. K., & Luster,, A. D. (2003). Toll‐like receptors stimulate human neutrophil function. Blood, 102(7), 2660–2669. https://doi.org/10.1182/blood-2003-04-1078
Henson,, P. M. (2017). Cell Removal: Efferocytosis. Annual Review of Cell and Developmental Biology, 33, 127–144. https://doi.org/10.1146/annurev-cellbio-111315-125315
Hickstein,, D. D., Ozols,, J., Williams,, S. A., Baenziger,, J. U., Locksley,, R. M., & Roth,, G. J. (1987). Isolation and characterization of the receptor on human neutrophils that mediates cellular adherence. The Journal of Biological Chemistry, 262(12), 5576–5580.
Hill,, J. M., Vaidyanathan,, H., Ramos,, J. W., Ginsberg,, M. H., & Werner,, M. H. (2002). Recognition of ERK MAP kinase by PEA‐15 reveals a common docking site within the death domain and death effector domain. The EMBO Journal, 21(23), 6494–6504.
Holland,, S. M., DeLeo,, F. R., Elloumi,, H. Z., Hsu,, A. P., Uzel,, G., Brodsky,, N., … Grimbacher,, B. (2007). STAT3 mutations in the hyper‐IgE syndrome. The New England Journal of Medicine, 357(16), 1608–1619. https://doi.org/10.1056/NEJMoa073687
Homburg,, C. H., de Haas,, M., von dem Borne,, A. E., Verhoeven,, A. J., Reutelingsperger,, C. P., & Roos,, D. (1995). Human neutrophils lose their surface Fc gamma RIII and acquire Annexin V binding sites during apoptosis in vitro. Blood, 85(2), 532–540.
Hong,, S., Porter,, T. F., Lu,, Y., Oh,, S. F., Pillai,, P. S., & Serhan,, C. N. (2008). Resolvin E1 metabolome in local inactivation during inflammation‐resolution. Journal of Immunology, 180(5), 3512–3519.
Houde,, M., Bertholet,, S., Gagnon,, E., Brunet,, S., Goyette,, G., Laplante,, A., … Desjardins,, M. (2003). Phagosomes are competent organelles for antigen cross‐presentation. Nature, 425(6956), 402–406. https://doi.org/10.1038/nature01912
Iida,, S., Kohro,, T., Kodama,, T., Nagata,, S., & Fukunaga,, R. (2005). Identification of CCR2, flotillin, and gp49B genes as new G‐CSF targets during neutrophilic differentiation. Journal of Leukocyte Biology, 78(2), 481–490. https://doi.org/10.1189/jlb.0904515
Jethwaney,, D., Islam,, M. R., Leidal,, K. G., de Bernabe,, D. B., Campbell,, K. P., Nauseef,, W. M., & Gibson,, B. W. (2007). Proteomic analysis of plasma membrane and secretory vesicles from human neutrophils. Proteome Science, 5, 12. https://doi.org/10.1186/1477-5956-5-12
Johnnidis,, J. B., Harris,, M. H., Wheeler,, R. T., Stehling‐Sun,, S., Lam,, M. H., Kirak,, O., … Camargo,, F. D. (2008). Regulation of progenitor cell proliferation and granulocyte function by microRNA‐223. Nature, 451(7182), 1125–1129. https://doi.org/10.1038/nature06607
Jonsson,, H., Allen,, P., & Peng,, S. L. (2005). Inflammatory arthritis requires Foxo3a to prevent Fas ligand‐induced neutrophil apoptosis. Nature Medicine, 11(6), 666–671. https://doi.org/10.1038/nm1248
Juss,, J., Herre,, J., Begg,, M., Bradley,, G., Lennon,, M., Amour,, A., … Chilvers,, E. R. (2015). Genome‐wide transcription profiling in neutrophils in acute respiratory distress syndrome. Lancet, 385 Suppl 1, S55. https://doi.org/10.1016/S0140-6736(15)60370-1
Juss,, J. K., House,, D., Amour,, A., Begg,, M., Herre,, J., Storisteanu,, D. M., … Chilvers,, E. R. (2016). Acute respiratory distress syndrome neutrophils have a distinct phenotype and are resistant to phosphoinositide 3‐kinase inhibition. American Journal of Respiratory and Critical Care Medicine, 194(8), 961–973. https://doi.org/10.1164/rccm.201509-1818OC
Kasprisin,, D. O., & Harris,, M. B. (1977). The role of RNA metabolism in polymorphonuclear leukocyte phagocytosis. The Journal of Laboratory and Clinical Medicine, 90(1), 118–124.
Kasprisin,, D. O., & Harris,, M. B. (1978). The role of protein synthesis in polymorphonuclear leukocyte phagocytosis II. Experimental Hematology, 6(7), 585–589.
Kettritz,, R., Gaido,, M. L., Haller,, H., Luft,, F. C., Jennette,, C. J., & Falk,, R. J. (1998). Interleukin‐8 delays spontaneous and tumor necrosis factor‐alpha‐mediated apoptosis of human neutrophils. Kidney International, 53(1), 84–91. https://doi.org/10.1046/j.1523-1755.1998.00741.x
Khan,, A. I., Kerfoot,, S. M., Heit,, B., Liu,, L., Andonegui,, G., Ruffell,, B., … Kubes,, P. (2004). Role of CD44 and hyaluronan in neutrophil recruitment. Journal of Immunology, 173(12), 7594–7601.
Khwaja,, A., & Tatton,, L. (1999). Caspase‐mediated proteolysis and activation of protein kinase Cdelta plays a central role in neutrophil apoptosis. Blood, 94(1), 291–301.
Kinkead,, L. C., Fayram,, D. C., & Allen,, L. H. (2017). Francisella novicida inhibits spontaneous apoptosis and extends human neutrophil lifespan. Journal of Leukocyte Biology, 102(3), 815–828. https://doi.org/10.1189/jlb.4MA0117-014R
Kippner,, L. E., Kim,, J., Gibson,, G., & Kemp,, M. L. (2014). Single cell transcriptional analysis reveals novel innate immune cell types. PeerJ, 2, e452. https://doi.org/10.7717/peerj.452
Klebanoff,, S. J. (1968). Myeloperoxidase‐halide‐hydrogen peroxide antibacterial system. Journal of Bacteriology, 95(6), 2131–2138.
Klebanoff,, S. J. (1974). Role of the superoxide anion in the myeloperoxidase‐mediated antimicrobial system. The Journal of Biological Chemistry, 249(12), 3724–3728.
Kluger,, Y., Tuck,, D. P., Chang,, J. T., Nakayama,, Y., Poddar,, R., Kohya,, N., … Weissman,, S. M. (2004). Lineage specificity of gene expression patterns. Proceedings of the National Academy of Sciences of the United States of America, 101(17), 6508–6513. https://doi.org/10.1073/pnas.0401136101
Kobayashi,, S. D., Braughton,, K. R., Palazzolo‐Ballance,, A. M., Kennedy,, A. D., Sampaio,, E., Kristosturyan,, E., … DeLeo,, F. R. (2010). Rapid neutrophil destruction following phagocytosis of Staphylococcus aureus. Journal of Innate Immunity, 2(6), 560–575. https://doi.org/10.1159/000317134
Kobayashi,, S. D., Braughton,, K. R., Whitney,, A. R., Voyich,, J. M., Schwan,, T. G., Musser,, J. M., & DeLeo,, F. R. (2003). Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proceedings of the National Academy of Sciences of the United States of America, 100(19), 10948–10953. https://doi.org/10.1073/pnas.1833375100
Kobayashi,, S. D., & Deleo,, F. R. (2004). An apoptosis differentiation programme in human polymorphonuclear leucocytes. Biochemical Society Transactions, 32(Pt3), 474–476. https://doi.org/10.1042/BST0320474
Kobayashi,, S. D., Voyich,, J. M., Braughton,, K. R., & DeLeo,, F. R. (2003). Down‐regulation of proinflammatory capacity during apoptosis in human polymorphonuclear leukocytes. Journal of Immunology, 170(6), 3357–3368.
Kobayashi,, S. D., Voyich,, J. M., Braughton,, K. R., Whitney,, A. R., Nauseef,, W. M., Malech,, H. L., & DeLeo,, F. R. (2004). Gene expression profiling provides insight into the pathophysiology of chronic granulomatous disease. Journal of Immunology, 172(1), 636–643.
Kobayashi,, S. D., Voyich,, J. M., Buhl,, C. L., Stahl,, R. M., & 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. Proceedings of the National Academy of Sciences of the United States of America, 99(10), 6901–6906. https://doi.org/10.1073/pnas.092148299
Kobayashi,, S. D., Voyich,, J. M., Burlak,, C., & DeLeo,, F. R. (2005). Neutrophils in the innate immune response. Archivum Immunologiae et Therapiae Experimentalis (Warsz), 53(6), 505–517.
Kobayashi,, S. D., Voyich,, J. M., Somerville,, G. A., Braughton,, K. R., Malech,, H. L., Musser,, J. M., & DeLeo,, F. R. (2003). An apoptosis‐differentiation program in human polymorphonuclear leukocytes facilitates resolution of inflammation. Journal of Leukocyte Biology, 73(2), 315–322.
Kobayashi,, S. D., Voyich,, J. M., Whitney,, A. R., & DeLeo,, F. R. (2005). Spontaneous neutrophil apoptosis and regulation of cell survival by granulocyte macrophage‐colony stimulating factor. Journal of Leukocyte Biology, 78(6), 1408–1418. https://doi.org/10.1189/jlb.0605289
Kosak,, S. T., Scalzo,, D., Alworth,, S. V., Li,, F., Palmer,, S., Enver,, T., … Groudine,, M. (2007). Coordinate gene regulation during hematopoiesis is related to genomic organization. PLoS Biology, 5(11), e309. https://doi.org/10.1371/journal.pbio.0050309
Kurt‐Jones,, E. A., Mandell,, L., Whitney,, C., Padgett,, A., Gosselin,, K., Newburger,, P. E., & Finberg,, R. W. (2002). Role of toll‐like receptor 2 (TLR2) in neutrophil activation: GM‐CSF enhances TLR2 expression and TLR2‐mediated interleukin 8 responses in neutrophils. Blood, 100(5), 1860–1868.
Lane,, T. A., & Lamkin,, G. E. (1984). A reassessment of the energy requirements for neutrophil migration: Adenosine triphosphate depletion enhances chemotaxis. Blood, 64(5), 986–993.
Larsen,, M. T., Hother,, C., Hager,, M., Pedersen,, C. C., Theilgaard‐Monch,, K., Borregaard,, N., & Cowland,, J. B. (2013). MicroRNA profiling in human neutrophils during bone marrow granulopoiesis and in vivo exudation. PLoS One, 8(3), e58454. https://doi.org/10.1371/journal.pone.0058454
Laterveer,, L., Lindley,, I. J., Heemskerk,, D. P., Camps,, J. A., Pauwels,, E. K., Willemze,, R., & Fibbe,, W. E. (1996). Rapid mobilization of hematopoietic progenitor cells in rhesus monkeys by a single intravenous injection of interleukin‐8. Blood, 87(2), 781–788.
Lawrence,, M. B., & Springer,, T. A. (1991). Leukocytes roll on a selectin at physiologic flow rates: Distinction from and prerequisite for adhesion through integrins. Cell, 65(5), 859–873.
Le Cabec,, V., Cowland,, J. B., Calafat,, J., & Borregaard,, N. (1996). Targeting of proteins to granule subsets is determined by timing and not by sorting: The specific granule protein NGAL is localized to azurophil granules when expressed in HL‐60 cells. Proceedings of the National Academy of Sciences of the United States of America, 93(13), 6454–6457.
Lee,, A., Whyte,, M. K., & Haslett,, C. (1993). Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators. Journal of Leukocyte Biology, 54(4), 283–288.
Lee,, H. C., & Goodman,, J. L. (2006). Anaplasma phagocytophilum causes global induction of antiapoptosis in human neutrophils. Genomics, 88(4), 496–503. https://doi.org/10.1016/j.ygeno.2006.06.002
Lee,, H. C., Kioi,, M., Han,, J., Puri,, R. K., & Goodman,, J. L. (2008). Anaplasma phagocytophilum‐induced gene expression in both human neutrophils and HL‐60 cells. Genomics, 92(3), 144–151. https://doi.org/10.1016/j.ygeno.2008.05.005
Lekstrom‐Himes,, J. A., Dorman,, S. E., Kopar,, P., Holland,, S. M., & Gallin,, J. I. (1999). Neutrophil‐specific granule deficiency results from a novel mutation with loss of function of the transcription factor CCAAT/enhancer binding protein epsilon. The Journal of Experimental Medicine, 189(11), 1847–1852.
Lekstrom‐Himes,, J. A., & Gallin,, J. I. (2000). Immunodeficiency diseases caused by defects in phagocytes. The New England Journal of Medicine, 343(23), 1703–1714. https://doi.org/10.1056/NEJM200012073432307
Lekstrom‐Himes,, J. A., Kuhns,, D. B., Alvord,, W. G., & Gallin,, J. I. (2005). Inhibition of human neutrophil IL‐8 production by hydrogen peroxide and dysregulation in chronic granulomatous disease. Journal of Immunology, 174(1), 411–417.
Ley,, T. J., Mardis,, E. R., Ding,, L., Fulton,, B., McLellan,, M. D., Chen,, K., … Wilson,, R. K. (2008). DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature, 456(7218), 66–72. https://doi.org/10.1038/nature07485
Lian,, Z., Kluger,, Y., Greenbaum,, D. S., Tuck,, D., Gerstein,, M., Berliner,, N., … Newburger,, P. E. (2002). Genomic and proteomic analysis of the myeloid differentiation program: Global analysis of gene expression during induced differentiation in the MPRO cell line. Blood, 100(9), 3209–3220. https://doi.org/10.1182/blood-2002-03-0850
Lian,, Z., Wang,, L., Yamaga,, S., Bonds,, W., Beazer‐Barclay,, Y., Kluger,, Y., … Weissman,, S. M. (2001). Genomic and proteomic analysis of the myeloid differentiation program. Blood, 98(3), 513–524.
Liles,, W. C., Kiener,, P. A., Ledbetter,, J. A., Aruffo,, A., & Klebanoff,, S. J. (1996). Differential expression of Fas (CD95) and Fas ligand on normal human phagocytes: Implications for the regulation of apoptosis in neutrophils. The Journal of Experimental Medicine, 184(2), 429–440.
Liles,, W. C., Thomsen,, A. R., O`Mahony,, D. S., & Klebanoff,, S. J. (2001). Stimulation of human neutrophils and monocytes by staphylococcal phenol‐soluble modulin. Journal of Leukocyte Biology, 70(1), 96–102.
Lin,, A., & Lore,, K. (2017). Granulocytes: New members of the antigen‐presenting cell family. Frontiers in Immunology, 8, 1781. https://doi.org/10.3389/fimmu.2017.01781
Lindemann,, S. W., Yost,, C. C., Denis,, M. M., McIntyre,, T. M., Weyrich,, A. S., & Zimmerman,, G. A. (2004). Neutrophils alter the inflammatory milieu by signal‐dependent translation of constitutive messenger RNAs. Proceedings of the National Academy of Sciences of the United States of America, 101(18), 7076–7081. https://doi.org/10.1073/pnas.0401901101
Liu,, J., Akahoshi,, T., Sasahana,, T., Kitasato,, H., Namai,, R., Sasaki,, T., … Kondo,, H. (1999). Inhibition of neutrophil apoptosis by verotoxin 2 derived from Escherichia coli O157:H7. Infection and Immunity, 67(11), 6203–6205.
Lominadze,, G., Powell,, D. W., Luerman,, G. C., Link,, A. J., Ward,, R. A., & McLeish,, K. R. (2005). Proteomic analysis of human neutrophil granules. Molecular %26 Cellular Proteomics, 4(10), 1503–1521. https://doi.org/10.1074/mcp.M500143-MCP200
Lotz,, S., Aga,, E., Wilde,, I., van Zandbergen,, G., Hartung,, T., Solbach,, W., & Laskay,, T. (2004). Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2. Journal of Leukocyte Biology, 75(3), 467–477. https://doi.org/10.1189/jlb.0803360
Maianski,, N. A., Geissler,, J., Srinivasula,, S. M., Alnemri,, E. S., Roos,, D., & Kuijpers,, T. W. (2004). Functional characterization of mitochondria in neutrophils: A role restricted to apoptosis. Cell Death and Differentiation, 11(2), 143–153. https://doi.org/10.1038/sj.cdd.4401320
Maianski,, N. A., Mul,, F. P., van Buul,, J. D., Roos,, D., & Kuijpers,, T. W. (2002). Granulocyte colony‐stimulating factor inhibits the mitochondria‐dependent activation of caspase‐3 in neutrophils. Blood, 99(2), 672–679.
Malcolm,, K. C., Arndt,, P. G., Manos,, E. J., Jones,, D. A., & Worthen,, G. S. (2003). Microarray analysis of lipopolysaccharide‐treated human neutrophils. American Journal of Physiology. Lung Cellular and Molecular Physiology, 284(4), L663–L670. https://doi.org/10.1152/ajplung.00094.2002
Mantovani,, B. (1975). Different roles of IgG and complement receptors in phagocytosis by polymorphonuclear leukocytes. Journal of Immunology, 115(1), 15–17.
Martinelli,, S., Urosevic,, M., Daryadel,, A., Oberholzer,, P. A., Baumann,, C., Fey,, M. F., … Yousefi,, S. (2004). Induction of genes mediating interferon‐dependent extracellular trap formation during neutrophil differentiation. The Journal of Biological Chemistry, 279(42), 44123–44132. https://doi.org/10.1074/jbc.M405883200
McCaffrey,, R. L., & Allen,, L. A. (2006). Francisella tularensis LVS evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape. Journal of Leukocyte Biology, 80(6), 1224–1230. https://doi.org/10.1189/jlb.0406287
McDonald,, P. P. (2004). Transcriptional regulation in neutrophils: Teaching old cells new tricks. Advances in Immunology, 82, 1–48. https://doi.org/10.1016/S0065-2776(04)82001-7
McPhillips,, K., Janssen,, W. J., Ghosh,, M., Byrne,, A., Gardai,, S., Remigio,, L., … Henson,, P. (2007). TNF‐alpha inhibits macrophage clearance of apoptotic cells via cytosolic phospholipase A2 and oxidant‐dependent mechanisms. Journal of Immunology, 178(12), 8117–8126.
Meagher,, L. C., Cousin,, J. M., Seckl,, J. R., & Haslett,, C. (1996). Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. Journal of Immunology, 156(11), 4422–4428.
Michlewska,, S., Dransfield,, I., Megson,, I. L., & Rossi,, A. G. (2009). Macrophage phagocytosis of apoptotic neutrophils is critically regulated by the opposing actions of pro‐inflammatory and anti‐inflammatory agents: Key role for TNF‐alpha. The FASEB Journal, 23(3), 844–854. https://doi.org/10.1096/fj.08-121228
Minegishi,, Y., Saito,, M., Tsuchiya,, S., Tsuge,, I., Takada,, H., Hara,, T., … Karasuyama,, H. (2007). Dominant‐negative mutations in the DNA‐binding domain of STAT3 cause hyper‐IgE syndrome. Nature, 448(7157), 1058–1062. https://doi.org/10.1038/nature06096
Mollinedo,, F., Lopez‐Perez,, R., & Gajate,, C. (2008). Differential gene expression patterns coupled to commitment and acquisition of phenotypic hallmarks during neutrophil differentiation of human leukaemia HL‐60 cells. Gene, 419(1–2), 16–26. https://doi.org/10.1016/j.gene.2008.04.015
Mott,, J., & Rikihisa,, Y. (2000). Human granulocytic ehrlichiosis agent inhibits superoxide anion generation by human neutrophils. Infection and Immunity, 68(12), 6697–6703.
Moulding,, D. A., Walter,, C., Hart,, C. A., & Edwards,, S. W. (1999). Effects of staphylococcal enterotoxins on human neutrophil functions and apoptosis. Infection and Immunity, 67(5), 2312–2318.
Muller,, S., & Diaz,, A. (2017). Single‐cell mRNA sequencing in Cancer research: Integrating the genomic fingerprint. Frontiers in Genetics, 8, 73. https://doi.org/10.3389/fgene.2017.00073
Muller,, W. A., Weigl,, S. A., Deng,, X., & Phillips,, D. M. (1993). PECAM‐1 is required for transendothelial migration of leukocytes. The Journal of Experimental Medicine, 178(2), 449–460.
Mullick,, A., Elias,, M., Harakidas,, P., Marcil,, A., Whiteway,, M., Ge,, B., … Thomas,, D. Y. (2004). Gene expression in HL60 granulocytoids and human polymorphonuclear leukocytes exposed to Candida albicans. Infection and Immunity, 72(1), 414–429.
Murphy,, B. M., O`Neill,, A. J., Adrain,, C., Watson,, R. W., & Martin,, S. J. (2003). The apoptosome pathway to caspase activation in primary human neutrophils exhibits dramatically reduced requirements for cytochrome C. The Journal of Experimental Medicine, 197(5), 625–632.
Murray,, J., Barbara,, J. A., Dunkley,, S. A., Lopez,, A. F., Van Ostade,, X., Condliffe,, A. M., … Chilvers,, E. R. (1997). Regulation of neutrophil apoptosis by tumor necrosis factor‐alpha: Requirement for TNFR55 and TNFR75 for induction of apoptosis in vitro. Blood, 90(7), 2772–2783.
Musser,, J. M., & DeLeo,, F. R. (2005). Toward a genome‐wide systems biology analysis of host‐pathogen interactions in group a Streptococcus. The American Journal of Pathology, 167(6), 1461–1472. https://doi.org/10.1016/S0002-9440(10)61232-1
Myones,, B. L., Dalzell,, J. G., Hogg,, N., & Ross,, G. D. (1988). Neutrophil and monocyte cell surface p150,95 has iC3b‐receptor (CR4) activity resembling CR3. The Journal of Clinical Investigation, 82(2), 640–651. https://doi.org/10.1172/JCI113643
Norris,, P. C., Libreros,, S., Chiang,, N., & Serhan,, C. N. (2017). A cluster of immunoresolvents links coagulation to innate host defense in human blood. Science Signaling, 10(490), eaan1471. https://doi.org/10.1126/scisignal.aan1471
Nunoi,, H., Rotrosen,, D., Gallin,, J. I., & Malech,, H. L. (1988). Two forms of autosomal chronic granulomatous disease lack distinct neutrophil cytosol factors. Science, 242(4883), 1298–1301.
Ofengeim,, D., Giagtzoglou,, N., Huh,, D., Zou,, C., & Yuan,, J. (2017). Single‐cell RNA sequencing: Unraveling the brain one cell at a time. Trends in Molecular Medicine, 23(6), 563–576. https://doi.org/10.1016/j.molmed.2017.04.006
O`Neill,, A. J., Doyle,, B. T., Molloy,, E., Watson,, C., Phelan,, D., Greenan,, M. C., … Watson,, R. W. (2004). Gene expression profile of inflammatory neutrophils: Alterations in the inhibitors of apoptosis proteins during spontaneous and delayed apoptosis. Shock, 21(6), 512–518.
Orr,, Y., Wilson,, D. P., Taylor,, J. M., Bannon,, P. G., Geczy,, C., Davenport,, M. P., & Kritharides,, L. (2007). A kinetic model of bone marrow neutrophil production that characterizes late phenotypic maturation. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 292(4), R1707–R1716. https://doi.org/10.1152/ajpregu.00627.2006
O`Shea,, J. J., & Murray,, P. J. (2008). Cytokine signaling modules in inflammatory responses. Immunity, 28(4), 477–487. https://doi.org/10.1016/j.immuni.2008.03.002
Pedersen,, C. C., Borup,, R., Fischer‐Nielsen,, A., Mora‐Jensen,, H., Fossum,, A., Cowland,, J. B., & Borregaard,, N. (2016). Changes in gene expression during G‐CSF‐induced emergency granulopoiesis in humans. Journal of Immunology, 197(5), 1989–1999. https://doi.org/10.4049/jimmunol.1502690
Persson,, Y. A., Blomgran‐Julinder,, R., Rahman,, S., Zheng,, L., & Stendahl,, O. (2008). Mycobacterium tuberculosis‐induced apoptotic neutrophils trigger a pro‐inflammatory response in macrophages through release of heat shock protein 72, acting in synergy with the bacteria. Microbes and Infection, 10(3), 233–240. https://doi.org/10.1016/j.micinf.2007.11.007
Plagge,, M., & Laskay,, T. (2017). Early production of the neutrophil‐derived lipid mediators LTB4 and LXA4 is modulated by intracellular infection with leishmania major. BioMed Research International, 2017, 2014583. https://doi.org/10.1155/2017/2014583
Polak,, D., Hafner,, C., Briza,, P., Kitzmuller,, C., Elbe‐Burger,, A., Samadi,, N., … Bohle,, B. (2019). A novel role for neutrophils in IgE‐mediated allergy: Evidence for antigen presentation in late‐phase reactions. The Journal of Allergy and Clinical Immunology, 143(3), 1143–1152. https://doi.org/10.1016/j.jaci.2018.06.005
Pryde,, J. G., Walker,, A., Rossi,, A. G., Hannah,, S., & Haslett,, C. (2000). Temperature‐dependent arrest of neutrophil apoptosis. Failure of Bax insertion into mitochondria at 15 degrees C prevents the release of cytochrome c. The Journal of Biological Chemistry, 275(43), 33574–33584. https://doi.org/10.1074/jbc.M001008200
Qin,, Y., Wu,, L., Ouyang,, Y., Zhou,, P., Zhou,, H., Wang,, Y., … Shen,, N. (2017). MiR‐125a is a critical modulator for neutrophil development. PLoS Genetics, 13(10), e1007027. https://doi.org/10.1371/journal.pgen.1007027
Rabellino,, E. M., Ross,, G. D., & Polley,, M. J. (1978). Membrane receptors of mouse leukocytes. I. Two types of complement receptors for different regions of C3. Journal of Immunology, 120(3), 879–885.
Renshaw,, S. A., Parmar,, J. S., Singleton,, V., Rowe,, S. J., Dockrell,, D. H., Dower,, S. K., … Whyte,, M. K. (2003). Acceleration of human neutrophil apoptosis by TRAIL. Journal of Immunology, 170(2), 1027–1033.
Ronnerblad,, M., Andersson,, R., Olofsson,, T., Douagi,, I., Karimi,, M., Lehmann,, S., … Consortium,, F. (2014). Analysis of the DNA methylome and transcriptome in granulopoiesis reveals timed changes and dynamic enhancer methylation. Blood, 123(17), e79–e89. https://doi.org/10.1182/blood-2013-02-482893
Roos,, D. (2016). Chronic granulomatous disease. British Medical Bulletin, 118(1), 50–63. https://doi.org/10.1093/bmb/ldw009
Rorvig,, S., Ostergaard,, O., Heegaard,, N. H., & Borregaard,, N. (2013). Proteome profiling of human neutrophil granule subsets, secretory vesicles, and cell membrane: Correlation with transcriptome profiling of neutrophil precursors. Journal of Leukocyte Biology, 94(4), 711–721. https://doi.org/10.1189/jlb.1212619
Rosen,, H., & Klebanoff,, S. J. (1977). Formation of singlet oxygen by the myeloperoxidase‐mediated antimicrobial system. The Journal of Biological Chemistry, 252(14), 4803–4810.
Rosen,, H., & Klebanoff,, S. J. (1979). Bactericidal activity of a superoxide anion‐generating system. A model for the polymorphonuclear leukocyte. The Journal of Experimental Medicine, 149(1), 27–39.
Ross,, G. D., Jarowski,, C. I., Rabellino,, E. M., & Winchester,, R. J. (1978). The sequential appearance of Ia‐like antigens and two different complement receptors during the maturation of human neutrophils. The Journal of Experimental Medicine, 147(3), 730–744.
Royer‐Pokora,, B., Kunkel,, L. M., Monaco,, A. P., Goff,, S. C., Newburger,, P. E., Baehner,, R. L., … Orkin,, S. H. (1986). Cloning the gene for an inherited human disorder‐‐chronic granulomatous disease‐‐on the basis of its chromosomal location. Nature, 322(6074), 32–38. https://doi.org/10.1038/322032a0
Rubel,, C., Gomez,, S., Fernandez,, G. C., Isturiz,, M. A., Caamano,, J., & Palermo,, M. S. (2003). Fibrinogen‐CD11b/CD18 interaction activates the NF‐kappa B pathway and delays apoptosis in human neutrophils. European Journal of Immunology, 33(5), 1429–1438. https://doi.org/10.1002/eji.200323512
Sabroe,, I., Jones,, E. C., Usher,, L. R., Whyte,, M. K., & Dower,, S. K. (2002). Toll‐like receptor (TLR)2 and TLR4 in human peripheral blood granulocytes: A critical role for monocytes in leukocyte lipopolysaccharide responses. Journal of Immunology, 168(9), 4701–4710.
Sabroe,, I., Prince,, L. R., Jones,, E. C., Horsburgh,, M. J., Foster,, S. J., Vogel,, S. N., … Whyte,, M. K. (2003). Selective roles for toll‐like receptor (TLR)2 and TLR4 in the regulation of neutrophil activation and life span. Journal of Immunology, 170(10), 5268–5275.
Sakamoto,, E., Hato,, F., Kato,, T., Sakamoto,, C., Akahori,, M., Hino,, M., & Kitagawa,, S. (2005). Type I and type II interferons delay human neutrophil apoptosis via activation of STAT3 and up‐regulation of cellular inhibitor of apoptosis 2. Journal of Leukocyte Biology, 78(1), 301–309. https://doi.org/10.1189/jlb.1104690
Saliba,, A. E., Li,, L., Westermann,, A. J., Appenzeller,, S., Stapels,, D. A., Schulte,, L. N., … Vogel,, J. (2016). Single‐cell RNA‐seq ties macrophage polarization to growth rate of intracellular Salmonella. Nature Microbiology, 2, 16206. https://doi.org/10.1038/nmicrobiol.2016.206
Savill,, J. (1997). Apoptosis in resolution of inflammation. Journal of Leukocyte Biology, 61(4), 375–380.
Savill,, J. S., Wyllie,, A. H., Henson,, J. E., Walport,, M. J., Henson,, P. M., & Haslett,, C. (1989). Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. The Journal of Clinical Investigation, 83(3), 865–875. https://doi.org/10.1172/JCI113970
Scheel‐Toellner,, D., Wang,, K., Assi,, L. K., Webb,, P. R., Craddock,, R. M., Salmon,, M., & Lord,, J. M. (2004). Clustering of death receptors in lipid rafts initiates neutrophil spontaneous apoptosis. Biochemical Society Transactions, 32(Pt 5), 679–681. https://doi.org/10.1042/BST0320679
Scheel‐Toellner,, D., Wang,, K., Craddock,, R., Webb,, P. R., McGettrick,, H. M., Assi,, L. K., … Lord,, J. M. (2004). Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood, 104(8), 2557–2564. https://doi.org/10.1182/blood-2004-01-0191
Schmeling,, D. J., Peterson,, P. K., Hammerschmidt,, D. E., Kim,, Y., Verhoef,, J., Wilkinson,, B. J., & Quie,, P. G. (1979). Chemotaxigenesis by cell surface components of Staphylococcus aureus. Infection and Immunity, 26(1), 57–63.
Schwartz,, J. T., Bandyopadhyay,, S., Kobayashi,, S. D., McCracken,, J., Whitney,, A. R., Deleo,, F. R., & Allen,, L. A. (2013). Francisella tularensis alters human neutrophil gene expression: Insights into the molecular basis of delayed neutrophil apoptosis. Journal of Innate Immunity, 5(2), 124–136. https://doi.org/10.1159/000342430
Schwartz,, J. T., Barker,, J. H., Kaufman,, J., Fayram,, D. C., McCracken,, J. M., & Allen,, L. A. (2012). Francisella tularensis inhibits the intrinsic and extrinsic pathways to delay constitutive apoptosis and prolong human neutrophil lifespan. Journal of Immunology, 188(7), 3351–3363. https://doi.org/10.4049/jimmunol.1102863
Serhan,, C. N., Hong,, S., & Lu,, Y. (2006). Lipid mediator informatics‐lipidomics: Novel pathways in mapping resolution. The AAPS Journal, 8(2), E284–E297. https://doi.org/10.1208/aapsj080233
Serhan,, C. N., Lu,, Y., Hong,, S., & Yang,, R. (2007). Mediator lipidomics: Search algorithms for eicosanoids, resolvins, and protectins. Methods in Enzymology, 432, 275–317. https://doi.org/10.1016/S0076-6879(07)32012-0
Shalek,, A. K., Satija,, R., Adiconis,, X., Gertner,, R. S., Gaublomme,, J. T., Raychowdhury,, R., … Regev,, A. (2013). Single‐cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature, 498(7453), 236–240. https://doi.org/10.1038/nature12172
Showell,, H. J., Freer,, R. J., Zigmond,, S. H., Schiffmann,, E., Aswanikumar,, S., Corcoran,, B., & Becker,, E. L. (1976). The structure‐activity relations of synthetic peptides as chemotactic factors and inducers of lysosomal secretion for neutrophils. The Journal of Experimental Medicine, 143(5), 1154–1169.
Silva,, E., Arcaroli,, J., He,, Q., Svetkauskaite,, D., Coldren,, C., Nick,, J. A., … Abraham,, E. (2007). HMGB1 and LPS induce distinct patterns of gene expression and activation in neutrophils from patients with sepsis‐induced acute lung injury. Intensive Care Medicine, 33(10), 1829–1839. https://doi.org/10.1007/s00134-007-0748-2
Stubbington,, M. J. T., Rozenblatt‐Rosen,, O., Regev,, A., & Teichmann,, S. A. (2017). Single‐cell transcriptomics to explore the immune system in health and disease. Science, 358(6359), 58–63. https://doi.org/10.1126/science.aan6828
Subrahmanyam,, Y. V., Yamaga,, S., Prashar,, Y., Lee,, H. H., Hoe,, N. P., Kluger,, Y., … Weissman,, S. M. (2001). RNA expression patterns change dramatically in human neutrophils exposed to bacteria. Blood, 97(8), 2457–2468.
Sukumaran,, B., Carlyon,, J. A., Cai,, J. L., Berliner,, N., & Fikrig,, E. (2005). Early transcriptional response of human neutrophils to Anaplasma phagocytophilum infection. Infection and Immunity, 73(12), 8089–8099. https://doi.org/10.1128/IAI.73.12.8089-8099.2005
Suttmann,, H., Lehan,, N., Bohle,, A., & Brandau,, S. (2003). Stimulation of neutrophil granulocytes with Mycobacterium bovis bacillus Calmette‐Guerin induces changes in phenotype and gene expression and inhibits spontaneous apoptosis. Infection and Immunity, 71(8), 4647–4656.
Suzuki,, S., Kobayashi,, M., Chiba,, K., Horiuchi,, I., Wang,, J., Kondoh,, T., … Asaka,, M. (2002). Autocrine production of epithelial cell‐derived neutrophil attractant‐78 induced by granulocyte colony‐stimulating factor in neutrophils. Blood, 99(5), 1863–1865.
Swain,, S. D., Rohn,, T. T., & Quinn,, M. T. (2002). Neutrophil priming in host defense: Role of oxidants as priming agents. Antioxidants %26 Redox Signaling, 4(1), 69–83. https://doi.org/10.1089/152308602753625870
Tamassia,, N., Le Moigne,, V., Calzetti,, F., Donini,, M., Gasperini,, S., Ear,, T., … Cassatella,, M. A. (2007). The MyD88‐independent pathway is not mobilized in human neutrophils stimulated via TLR4. Journal of Immunology, 178(11), 7344–7356.
Theilgaard‐Monch,, K., Jacobsen,, L. C., Borup,, R., Rasmussen,, T., Bjerregaard,, M. D., Nielsen,, F. C., … Borregaard,, N. (2005). The transcriptional program of terminal granulocytic differentiation. Blood, 105(4), 1785–1796. https://doi.org/10.1182/blood-2004-08-3346
Theilgaard‐Monch,, K., Knudsen,, S., Follin,, P., & Borregaard,, N. (2004). The transcriptional activation program of human neutrophils in skin lesions supports their important role in wound healing. Journal of Immunology, 172(12), 7684–7693.
Theilgaard‐Monch,, K., Porse,, B. T., & Borregaard,, N. (2006). Systems biology of neutrophil differentiation and immune response. Current Opinion in Immunology, 18(1), 54–60. https://doi.org/10.1016/j.coi.2005.11.010
Thomas,, D. C. (2017). The phagocyte respiratory burst: Historical perspectives and recent advances. Immunology Letters, 192, 88–96. https://doi.org/10.1016/j.imlet.2017.08.016
Touret,, N., Paroutis,, P., & Grinstein,, S. (2005). The nature of the phagosomal membrane: Endoplasmic reticulum versus plasmalemma. Journal of Leukocyte Biology, 77(6), 878–885. https://doi.org/10.1189/jlb.1104630
Touret,, N., Paroutis,, P., Terebiznik,, M., Harrison,, R. E., Trombetta,, S., Pypaert,, M., … Grinstein,, S. (2005). Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell, 123(1), 157–170. https://doi.org/10.1016/j.cell.2005.08.018
Tsukahara,, Y., Lian,, Z., Zhang,, X., Whitney,, C., Kluger,, Y., Tuck,, D., … Newburger,, P. E. (2003). Gene expression in human neutrophils during activation and priming by bacterial lipopolysaccharide. Journal of Cellular Biochemistry, 89(4), 848–861. https://doi.org/10.1002/jcb.10526
Usher,, L. R., Lawson,, R. A., Geary,, I., Taylor,, C. J., Bingle,, C. D., Taylor,, G. W., & Whyte,, M. K. (2002). Induction of neutrophil apoptosis by the Pseudomonas aeruginosa exotoxin pyocyanin: A potential mechanism of persistent infection. Journal of Immunology, 168(4), 1861–1868.
van den Berg,, J. M., Weyer,, S., Weening,, J. J., Roos,, D., & Kuijpers,, T. W. (2001). Divergent effects of tumor necrosis factor alpha on apoptosis of human neutrophils. Journal of Leukocyte Biology, 69(3), 467–473.
van Raam,, B. J., Sluiter,, W., de Wit,, E., Roos,, D., Verhoeven,, A. J., & Kuijpers,, T. W. (2008). Mitochondrial membrane potential in human neutrophils is maintained by complex III activity in the absence of supercomplex organisation. PLoS One, 3(4), e2013. https://doi.org/10.1371/journal.pone.0002013
Ventura,, C. L., Malachowa,, N., Hammer,, C. H., Nardone,, G. A., Robinson,, M. A., Kobayashi,, S. D., & DeLeo,, F. R. (2010). Identification of a novel Staphylococcus aureus two‐component leukotoxin using cell surface proteomics. PLoS One, 5(7), e11634. https://doi.org/10.1371/journal.pone.0011634
Volpp,, B. D., Nauseef,, W. M., & Clark,, R. A. (1988). Two cytosolic neutrophil oxidase components absent in autosomal chronic granulomatous disease. Science, 242(4883), 1295–1297.
Vono,, M., Lin,, A., Norrby‐Teglund,, A., Koup,, R. A., Liang,, F., & Lore,, K. (2017). Neutrophils acquire the capacity for antigen presentation to memory CD4(+) T cells in vitro and ex vivo. Blood, 129(14), 1991–2001. https://doi.org/10.1182/blood-2016-10-744441
Voyich,, J. M., Braughton,, K. R., Sturdevant,, D. E., Whitney,, A. R., Said‐Salim,, B., Porcella,, S. F., … DeLeo,, F. R. (2005). Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. Journal of Immunology, 175(6), 3907–3919.
Walmsley,, S. R., Print,, C., Farahi,, N., Peyssonnaux,, C., Johnson,, R. S., Cramer,, T., … Chilvers,, E. R. (2005). Hypoxia‐induced neutrophil survival is mediated by HIF‐1alpha‐dependent NF‐kappaB activity. The Journal of Experimental Medicine, 201(1), 105–115. https://doi.org/10.1084/jem.20040624
Walz,, A., Peveri,, P., Aschauer,, H., & Baggiolini,, M. (1987). Purification and amino acid sequencing of NAF, a novel neutrophil‐activating factor produced by monocytes. Biochemical and Biophysical Research Communications, 149(2), 755–761.
Wang,, R., Braughton,, K. R., Kretschmer,, D., Bach,, T. H., Queck,, S. Y., Li,, M., … Otto,, M. (2007). Identification of novel cytolytic peptides as key virulence determinants for community‐associated MRSA. Nature Medicine, 13(12), 1510–1514. https://doi.org/10.1038/nm1656
Ward,, C., Chilvers,, E. R., Lawson,, M. F., Pryde,, J. G., Fujihara,, S., Farrow,, S. N., … Rossi,, A. G. (1999). NF‐kappaB activation is a critical regulator of human granulocyte apoptosis in vitro. The Journal of Biological Chemistry, 274(7), 4309–4318.
Ward,, C., Dransfield,, I., Chilvers,, E. R., Haslett,, C., & Rossi,, A. G. (1999). Pharmacological manipulation of granulocyte apoptosis: Potential therapeutic targets. Trends in Pharmacological Sciences, 20(12), 503–509.
Watson,, R. W., Redmond,, H. P., Wang,, J. H., Condron,, C., & Bouchier‐Hayes,, D. (1996). Neutrophils undergo apoptosis following ingestion of Escherichia coli. Journal of Immunology, 156(10), 3986–3992.
Whitlock,, B. B., Gardai,, S., Fadok,, V., Bratton,, D., & Henson,, P. M. (2000). Differential roles for alpha(M)beta(2) integrin clustering or activation in the control of apoptosis via regulation of akt and ERK survival mechanisms. The Journal of Cell Biology, 151(6), 1305–1320.
Whyte,, M. K., Hardwick,, S. J., Meagher,, L. C., Savill,, J. S., & Haslett,, C. (1993). Transient elevations of cytosolic free calcium retard subsequent apoptosis in neutrophils in vitro. The Journal of Clinical Investigation, 92(1), 446–455. https://doi.org/10.1172/JCI116587
Whyte,, M. K., Meagher,, L. C., MacDermot,, J., & Haslett,, C. (1993). Impairment of function in aging neutrophils is associated with apoptosis. Journal of Immunology, 150(11), 5124–5134.
Wong,, J. J., Ritchie,, W., Gao,, D., Lau,, K. A., Gonzalez,, M., Choudhary,, A., … Holst,, J. (2014). Identification of nuclear‐enriched miRNAs during mouse granulopoiesis. Journal of Hematology %26 Oncology, 7, 42. https://doi.org/10.1186/1756-8722-7-42
Wright,, H. L., Thomas,, H. B., Moots,, R. J., & Edwards,, S. W. (2013). RNA‐seq reveals activation of both common and cytokine‐specific pathways following neutrophil priming. PLoS One, 8(3), e58598. https://doi.org/10.1371/journal.pone.0058598
Yamanaka,, R., Barlow,, C., Lekstrom‐Himes,, J., Castilla,, L. H., Liu,, P. P., Eckhaus,, M., … Xanthopoulos,, K. G. (1997). Impaired granulopoiesis, myelodysplasia, and early lethality in CCAAT/enhancer binding protein epsilon‐deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 94(24), 13187–13192.
Yoshiie,, K., Kim,, H. Y., Mott,, J., & Rikihisa,, Y. (2000). Intracellular infection by the human granulocytic ehrlichiosis agent inhibits human neutrophil apoptosis. Infection and Immunity, 68(3), 1125–1133.
Yoshimura,, T., Matsushima,, K., Tanaka,, S., Robinson,, E. A., Appella,, E., Oppenheim,, J. J., & Leonard,, E. J. (1987). Purification of a human monocyte‐derived neutrophil chemotactic factor that has peptide sequence similarity to other host defense cytokines. Proceedings of the National Academy of Sciences of the United States of America, 84(24), 9233–9237.
Yost,, C. C., Denis,, M. M., Lindemann,, S., Rubner,, F. J., Marathe,, G. K., Buerke,, M., … Zimmerman,, G. A. (2004). Activated polymorphonuclear leukocytes rapidly synthesize retinoic acid receptor‐alpha: A mechanism for translational control of transcriptional events. The Journal of Experimental Medicine, 200(5), 671–680. https://doi.org/10.1084/jem.20040224
Yuan,, X., Berg,, N., Lee,, J. W., Le,, T. T., Neudecker,, V., Jing,, N., & Eltzschig,, H. (2018). MicroRNA miR‐223 as regulator of innate immunity. Journal of Leukocyte Biology, 104(3), 515–524. https://doi.org/10.1002/JLB.3MR0218-079R
Zhang,, B., Hirahashi,, J., Cullere,, X., & Mayadas,, T. N. (2003). Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: Cross‐talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. The Journal of Biological Chemistry, 278(31), 28443–28454. https://doi.org/10.1074/jbc.M210727200
Zhang,, X., Kluger,, Y., Nakayama,, Y., Poddar,, R., Whitney,, C., DeTora,, A., … Newburger,, P. E. (2004). Gene expression in mature neutrophils: Early responses to inflammatory stimuli. Journal of Leukocyte Biology, 75(2), 358–372. https://doi.org/10.1189/jlb.0903412
Zheng,, C., Zheng,, L., Yoo,, J. K., Guo,, H., Zhang,, Y., Guo,, X., … Zhang,, Z. (2017). Landscape of infiltrating T cells in liver cancer revealed by single‐cell sequencing. Cell, 169(7), 1342–1356. https://doi.org/10.1016/j.cell.2017.05.035
Zhu,, Y. P., Padgett,, L., Dinh,, H. Q., Marcovecchio,, P., Blatchley,, A., Wu,, R., … Hedrick,, C. C. (2018). Identification of an early unipotent neutrophil progenitor with pro‐tumoral activity in mouse and human bone marrow. Cell Reports, 24(9), 2329–2341. https://doi.org/10.1016/j.celrep.2018.07.097
Zilbauer,, M., Rayner,, T. F., Clark,, C., Coffey,, A. J., Joyce,, C. J., Palta,, P., … Smith,, K. G. (2013). Genome‐wide methylation analyses of primary human leukocyte subsets identifies functionally important cell‐type‐specific hypomethylated regions. Blood, 122(25), e52–e60. https://doi.org/10.1182/blood-2013-05-503201
Zilionis,, R., Engblom,, C., Pfirschke,, C., Savova,, V., Zemmour,, D., Saatcioglu,, H. D., … Klein,, A. M. (2019). Single‐cell transcriptomics of human and mouse lung cancers reveals conserved myeloid populations across individuals and species. Immunity, 50, 1317–1334. https://doi.org/10.1016/j.immuni.2019.03.009

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Role of neutrophils in innate immunity: a systems biology‐level approach
Scott D. Kobayashi,Frank R. DeLeo
Published Online: November 13 2009
DOI: 10.1002/wsbm.32

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