Role of neutrophils in innate immunity: A systems biology-level approach

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 1, Issue 3, 2009, Pages 309-333

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

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; NEUTROPHIL; REVIEW; SYSTEMS BIOLOGY;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; MODELS, IMMUNOLOGICAL; NEUTROPHILS; SYSTEMS BIOLOGY;

EID: 79952115434     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.32     Document Type: Review

References (204)

1. Homburg CH, Roos D. Apoptosis of neutrophils. Curr Opin Hematol 1996, 3:94-99.
2. Kasprisin DO, Harris MB. The role of RNA metabolism in polymorphonuclear leukocyte phagocytosis. J Lab Clin Med 1977, 90:118-124.
3. Kasprisin DO, Harris MB. The role of protein synthesis in polymorphonuclear leukocyte phagocytosis II. Exp Hematol 1978, 6:585-589.
4. Holland SM, DeLeo FR, Elloumi HZ, Hsu AP, Uzel G, et al. STAT3 Mutations in the Hyper-IgE Syndrome. N Engl J Med 2007, 357:1608-1619.
5. Friedman AD. Transcriptional regulation of granulocyte and monocyte development. Oncogene 2002, 21:3377-3390.
6. McDonald PP. Transcriptional regulation in neutrophils: teaching old cells new tricks. Adv Immunol 2004, 8:21-48.
7. Bainton DF, Ullyot JL, Farquhar MG. The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. J Exp Med 1971, 134:907-934.
8. Cline MJ. Phagocytosis and synthesis of ribonucleic acid in human granulocytes. Nature 1966, 212:1431-1433.
9. Cline MJ. Ribonucleic acid biosynthesis in human leukocytes. Effects of phagocytosis on RNA metabolism. Blood 1966, 28:188-200.
10. Walmsley SR, Print C, Farahi N, Peyssonnaux C, Johnson RS, et al. Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J ExpMed 2005, 201:105-115.
11. Jonsson H, Allen P, Peng SL. Inflammatory arthritis requires Foxo3a to prevent Fas ligand-induced neutrophil apoptosis. Nat Med 2005, 11:666-671.
12. Kosak ST, Scalzo D, Alworth SV, Li F, Palmer S, et al. Coordinate gene regulation during hematopoiesis is related to genomic organization. PLoS Biol 2007, 5:e309.
13. Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, LamMH, et al. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 2008, 451:1125-1129.
14. Lindemann SW, Yost CC, Denis MM, McIntyre TM, Weyrich AS, et al. Neutrophils alter the inflammatory milieu by signal-dependent translation of constitutive messenger RNAs. Proc Natl Acad Sci U S A 2004, 101:7076-7081.
15. Yost CC, Denis MM, Lindemann S, Rubner FJ, Marathe GK, et al. Activated polymorphonuclear leukocytes rapidly synthesize retinoic acid receptoralpha: a mechanism for translational control of transcriptional events. J ExpMed 2004, 200:671-680.
16. Cline MJ. Production and distribution of neutrophils. In: Cline MJ ed. The White Cell. Cambridge, Massachusetts: Harvard University Press; 1975, 22-38.
17. Athens JW, Haab OP, Raab SO, Mauer AM, Ashenbrucker H, et al. Leukokinetic studies. IV. The total blood, circulating and marginal granulocyte pools and the granulocyte turnover rate in normal subjects. J Clin Invest 1961, 40:989-995.
18. Dale DC, Liles WC, Llewellyn C, Price TH. Effects of granulocyte-macrophage colony-stimulating factor (GM-CSF) on neutrophil kinetics and function in normal human volunteers. Am JHematol 1998, 57:7-15.
19. Dancey JT, Deubelbeiss KA, Harker LA, Finch CA. Neutrophil kinetics in man. J Clin Invest 1976, 58:705-715.
20. Cronkite EP, Fliedner TM. Granulocytopoiesis. N Engl J Med 1964, 270:1403-1408.
21. Fliedner TM, Cronkite EP, Robertson JS. Granulocytopoiesis. I. Senescence and random loss of neutrophilic granulocytes in human beings. Blood 1964, 24:402-414.
22. Fliedner TM, Cronkite EP, Killmann SA, Bond VP. Granulocytopoiesis. II. Emergence and pattern of labeling of neutrophilic granulocytes in humans. Blood 1964, 24:683-700.
23. Orr Y, Wilson DP, Taylor JM, Bannon PG, Geczy C, et al. A kinetic model of bone marrow neutrophil production that characterizes late phenotypic maturation. Am J Physiol Regul Integr Comp Physiol 2007, 292:R1707-R1716.
24. Aglietta M, Piacibello W, Sanavio F, Stacchini A, Apra F, et al. Kinetics of human hemopoietic cells after in vivo administration of granulocytemacrophage colony-stimulating factor. J Clin Invest 1989, 83:551-557.
25. Laterveer L, Lindley IJ, Heemskerk DP, Camps JA, Pauwels EK, et al. Rapid mobilization of hematopoietic progenitor cells in rhesus monkeys by a single intravenous injection of interleukin-8. Blood 1996, 87:781-788.
26. Lian Z, Wang L, Yamaga S, Bonds W, Beazer-Barclay Y, et al. Genomic and proteomic analysis of the myeloid differentiation program. Blood 2001, 98:513-524.
27. Lian Z, Kluger Y, Greenbaum DS, Tuck D, Gerstein M, et al. Genomic and proteomic analysis of the myeloid differentiation program: global analysis of gene expression during induced differentiation in the MPRO cell line. Blood 2002, 100:3209-3220.
28. Iida S, Kohro T, Kodama T, Nagata S, Fukunaga R. Identification of CCR2, flotillin, and gp49B genes as newG-CSF targets during neutrophilic differentiation. J Leukoc Biol 2005, 78:481-490.
29. Martinelli S, Urosevic M, Daryadel A, Oberholzer PA, Baumann C, et al. Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation. J Biol Chem 2004, 279:44123-44132.
30. Theilgaard-Mönch K, Knudsen S, Follin P, Borregaard N. The transcriptional activation program of human neutrophils in skin lesions supports their important role in wound healing. J Immunol 2004, 172:7684-7693.
31. Ferrari F, Bortoluzzi S, Coppe A, Basso D, Bicciato S, et al. Genomic expression during human myelopoiesis. BMC Genomics 2007, 8:264.
32. Mollinedo F, Lopez-Perez R, Gajate C. Differential gene expression patterns coupled to commitment and acquisition of phenotypic hallmarks during neutrophil differentiation of human leukaemia HL-60 cells. Gene 2008, 419:16-26.
33. Kluger Y, Tuck DP, Chang JT, Nakayama Y, Poddar R, et al. Lineage specificity of gene expression patterns. Proc Natl Acad Sci U S A 2004, 101:6508-6513.
34. Theilgaard-Monch K, Porse BT, Borregaard N. Systems biology of neutrophil differentiation and immune response. Curr Opin Immunol 2006, 18:54-60.
35. Theilgaard-Monch K, Jacobsen LC, Borup R, Rasmussen T, Bjerregaard MD, et al. The transcriptional program of terminal granulocytic differentiation. Blood 2005, 105:1785-1796.
36. Le CV, Cowland JB, Calafat J, Borregaard N. 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. Proc Natl Acad Sci U S A 1996, 93:6454-6457.
37. Lawrence MB, Springer TA. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 1991, 65:859-873.
38. MullerWA,Weigl SA, Deng X, PhillipsDM. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med 1993, 178:449-460.
39. Diamond MS, Staunton DE, de Fougerolles AR, Stacker SA, Garcia-Aguilar J, et al. ICAM-1 (CD54): a counter-receptor for Mac-1 (CD11b/CD18). J Cell Biol 1990, 111:3129-3139.
40. Khan AI, Kerfoot SM, Heit B, Liu L, Andonegui G, et al. Role of CD44 and hyaluronan in neutrophil recruitment. J Immunol 2004, 173:7594-7601.
41. Cooper D, Lindberg FP, Gamble JR, Brown EJ, VadasMA. Transendothelialmigration of neutrophils involves integrin- associated protein (CD47). Proc Natl Acad Sci U S A 1995, 92:3978-3982.
42. Walz A, Peveri P, Aschauer H, Baggiolini M. Purification and amino acid sequencing of NAF, a novel neutrophil-activating factor produced by monocytes. Biochem Biophys Res Commun 1987, 149:755-761.
43. Yoshimura T, Matsushima K, Tanaka S, Robinson EA, Appella E, et al. Purification of a human monocyte-derived neutrophil chemotactic factor that has peptide sequence similarity to other host defense cytokines. Proc Natl Acad Sci U S A 1987, 84:9233-9237.
44. EhrengruberMU, Geiser T, Deranleau DA. Activation of human neutrophils by C3a and C5A: comparison of the effects on shape changes, chemotaxis, secretion, and respiratory burst. FEBS Lett 1994, 346:181-184.
45. Showell HJ, Freer RJ, Zigmond SH, Shiffmann E, Aswanikumar S, et al. The structure-activity relations of synthetic peptides as chemotactic factors and inducers of lysosomal enzyme secretion for neutrophils. J ExpMed 1976, 143:1154-1169.
46. Schmeling DJ, Peterson PK, Hammerschmidt DE, Kim Y, Verhoef J, et al. Chemotaxigenesis by cell surface components of Staphylococcus aureus. Infect Immun 1979, 26:57-63.
47. Boxer LA, Axtell R, Suchard S. The role of the neutrophil in inflammatory diseases of the lung. Blood Cells 1990, 16:25-42.
48. Edwards SW, Hallett MB. Seeing the wood for the trees: the forgotten role of neutrophils in rheumatoid arthritis. Immunol Today 1997, 18:320-324.
49. Swain SD, Rohn TT, Quinn MT. Neutrophil priming in host defense: role of oxidants as priming agents. Antioxid Redox Signal 2002, 4:69-83.
50. Sheppard FR, Kelher MR, Moore EE, McLaughlin NJ, Banerjee A, et al. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J Leukoc Biol 2005, 78:1025-1042.
51. Guthrie LA, McPhail LC, Henson PM, Johnston RB Jr. Priming of neutrophils for enhanced release of oxygen metabolites by bacterial lipopolysaccharide. Evidence for increased activity of the superoxideproducing enzyme. J ExpMed 1984, 160:1656-1671.
52. Kobayashi SD, Voyich JM, Burlak C, DeLeo FR. Neutrophils in the innate immune response. Arch Immunol Ther Exp (Warsz) 2005, 53:505-517.
53. DeLeo FR, Renee J, Mccormick S, Nakamura M, Apicella M, et al. Neutrophils exposed to bacterial lipopolysaccharide upregulate NADPH oxidase assembly. J Clin Invest 1998, 101:455-463.
54. Zhang XQ, Kluger Y, Nakayama Y, Poddar R, Whitney C, et al. Gene expression in mature neutrophils: early responses to inflammatory stimuli. J Leukoc Biol 2004, 75:358-372.
55. Boldt K, Rist W, Weiss SM, Weith A, Lenter MC. FPRL-1 induces modifications of migration-associated proteins in human neutrophils. Proteomics 2006, 6:4790-4799.
56. Coldren CD, Nick JA, Poch KR, Woolum MD, Fouty BW, et al. Functional and genomic changes induced by alveolar transmigration in human neutrophils. Am J Physiol Lung Cell Mol Physiol 2006, 291:L1267-L1276.
57. Suzuki S, Kobayashi M, Chiba K, Horiuchi I, Wang J, et al. Autocrine production of epithelial cellderived neutrophil attractant-78 induced by granulocyte colony-stimulating factor in neutrophils. Blood 2002, 99:1863-1865.
58. Kobayashi SD, Voyich JM, Whitney AR, DeLeo FR. Spontaneous neutrophil apoptosis and regulation of cell survival by granulocyte macrophage-colony stimulating factor. J Leukoc Biol 2005, 78:1408-1418.
59. Whyte MK, Meagher LC, MacDermot J, Haslett C. Impairment of function in aging neutrophils is associated with apoptosis. J Immunol 1993, 150:5124-5134.
60. Cohn ZA, Morse SI. Functional and metabolic properties of polymorphonuclear leucocytes. II. The influence of a lipopolysaccharide endotoxin. J Exp Med 1960, 111:689-704.
61. Dahinden CA, Galanos C, Fehr J. Granulocyte activation by endotoxin. I. Correlation between adherence and other granulocyte functions, and role of endotoxin structure on biologic activity. J Immunol 1983, 130:857-862.
62. Sabroe I, Jones EC, Usher LR, WhyteMK, Dower SK. Toll-like receptor (TLR)2 and TLR4 in human peripheral blood granulocytes: a critical role for monocytes in leukocyte lipopolysaccharide responses. J Immunol 2002, 168:4701-4710.
63. Tsukahara Y, Lian Z, Zhang XQ, Whitney C, Kluger Y, et al. Gene expression in human neutrophils during activation and priming by bacterial lipopolysaccharide. J Cell Biochem 2003, 89:848-861.
64. O'Neill AJ, Doyle BT, Molloy E, Watson C, Phelan D, et al. Gene expression profile of inflammatory neutrophils: alterations in the inhibitors of apoptosis proteins during spontaneous and delayed apoptosis. Shock 2004, 21:512-518.
65. Silva E, Arcaroli J, He Q, Svetkauskaite D, Coldren C, et al.HMGB1 and LPS induce distinct patterns of gene expression and activation in neutrophils from patients with sepsis-induced acute lung injury. Intensive Care Med 2007, 33:1829-1839.
66. Fessler MB,Malcolm KC, Duncan MW, Worthen GS. A genomic and proteomic analysis of activation of the human neutrophil by lipopolysaccharide and its mediation by p38 mitogen-activated protein kinase. J Biol Chem 2002, 277:31291-31302.
67. Tamassia N, Le MV, Calzetti F, Donini M, Gasperini S, et al. The MyD88-independent pathway is not mobilized in human neutrophils stimulated via TLR4. J Immunol 2007, 178:7344-7356.
68. Malcolm KC, Arndt PG, Manos EJ, Jones DA, Worthen GS. Microarray analysis of lipopolysaccharide-treated human neutrophils. Am J Physiol Lung Cell Mol Physiol 2003, 284:L663-L670.
69. Hayashi F, Means TK, Luster AD. Toll-like receptors stimulate human neutrophil function. Blood 2003, 102:2660-2669.
70. Sabroe I, Prince LR, Jones EC, Horsburgh MJ, Foster SJ, et al. Selective roles for Toll-like receptor (TLR)2 and TLR4 in the regulation of neutrophil activation and life span. J Immunol 2003, 170:5268-5275.
71. Kurt-Jones EA, Mandell L, Whitney C, Padgett A, Gosselin K, et al. Role of toll-like receptor 2 (TLR2) in neutrophil activation: GM-CSF enhances TLR2 expression and TLR2-mediated interleukin 8 responses in neutrophils. Blood 2002, 100:1860-1868.
72. Bellocchio S, Moretti S, Perruccio K, Fallarino F, Bozza S, et al. TLRs govern neutrophil activity in aspergillosis. J Immunol 2004, 173:7406-7415.
73. Lotz S, Aga E, Wilde I, van ZG, Hartung T, et al. Highly purified lipoteichoic acid activates neutrophil granulocytes and delays their spontaneous apoptosis via CD14 and TLR2. J Leukoc Biol 2004, 75:467-477.
74. Mantovani B. Different roles of IgG and complement receptors in phagocytosis by polymorphonuclear leukocytes. J Immunol 1975, 115:15-17.
75. Nauseef WM, Clark RA. Granulocytic phagocytes. In: Mandell G, Bennett JE, Dolin R. eds. Principles and Practica of Infectious Diseases. New York: Churchill Livingstone; 2000, 89-112.
76. Fleit HB, Wright SD, Unkeless JC. Human neutrophil Fc gamma receptor distribution and structure. Proc Natl Acad Sci U S A 1982, 79:3275-3279.
77. Albrechtsen M, Yeaman GR, Kerr MA. Characterization of the IgA receptor from human polymorphonuclear leucocytes. Immunology 1988, 64:201-205.
78. Gounni AS, Lamkhioued B, Koussih L, Ra C, Renzi PM, et al. Human neutrophils express the high-affinity receptor for immunoglobulin E (Fc epsilon RI): role in asthma. FASEB J 2001, 15:940-949.
79. Eggleton P, Ghebrehiwet B, Sastry KN, Coburn JP, Zaner KS, et al. 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. J Clin Invest 1995, 95:1569-1578.
80. Rabellino EM, Ross GD, PolleyMJ. Membrane receptors of mouse leukocytes. I. Two types of complement receptors for different regions of C3. J Immunol 1978, 120:879-885.
81. Ross GD, Jarowski CI, Rabellino EM, Winchester RJ. The sequential appearance of Ia-like antigens and two different complement receptors during the maturation of human neutrophils. J Exp Med 1978, 147:730-744.
82. Dana N, Todd RF III, Pitt J, Springer TA, Arnaout MA. Deficiency of a surface membrane glycoprotein (Mo1) in man. J Clin Invest 1984, 73:153-159.
83. Hickstein DD, Ozols J, Williams SA, Baenziger JU, Locksley RM, et al. Isolation and characterization of the receptor on human neutrophils that mediates cellular adherence. J Biol Chem 1987, 262:5576-5580.
84. Myones BL, Dalzell JG, Hogg N, Ross GD. Neutrophil and monocyte cell surface p150,95 has iC3b-receptor (CR4) activity resembling CR3. J Clin Invest 1988, 82:640-651.
85. Quinn MT, Gauss KA. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with non-phagocyte oxidases. J Leukoc Biol 2004, 76:760-781.
86. Guichard C, Pedruzzi E, Dewas C, Fay M, Pouzet C, et al. Interleukin-8-induced priming of neutrophil oxidative burst requires sequential recruitment of NADPH oxidase components into lipid rafts. J Biol Chem 2005, 280:37021-37032.
87. phox. J Biol Chem 1999, 274:20704-20708.
88. Brown GE, Stewart MQ, Bissonnette SA, Elia AEH, Wilker E, et al. Distinct ligand-dependent roles for p38 MAPK in priming and activation of the neutrophil NADPH oxidase. J Biol Chem 2004, 279:27059-27068.
89. Klebanoff SJ. Myeloperoxidase-halide-hydrogen peroxide antibacterial system. J Bacteriol 1968, 95:2131-2138.
90. Klebanoff SJ. Role of the superoxide anion in the myeloperoxidase-mediated antimicrobial system. J Biol Chem 1974, 249:3724-3728.
91. Rosen H, Klebanoff SJ. Formation of singlet oxygen by the myeloperoxidase-mediated antimicrobial system. J Biol Chem1977, 252:4803-4810.
92. Rosen H, Klebanoff SJ. Bactericidal activity of a superoxide anion-generating system. A model for the polymorphonuclear leukocyte. J Exp Med 1979, 149:27-39.
93. Kobayashi SD, DeLeo FR. An apoptosis differentiation programme in human polymorphonuclear leucocytes. Biochem Soc Trans 2004, 32:474-476.
94. Subrahmanyam YVBK, Yamaga S, Prashar Y, Lee HH, Hoe NP, et al. RNA expression patterns change dramatically in human neutrophils exposed to bacteria. Blood 2001, 97:2457-2468.
95. Kobayashi SD, Voyich JM, Buhl CL, Stahl RM, DeLeo FR.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 2002, 99:6901-6906.
96. Kobayashi SD, Braughton KR, Whitney AR, Voyich JM, Schwan TG, et al. Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proc Natl Acad Sci U S A 2003, 100:10948-10953.
97. Borjesson DL, Kobayashi SD, Whitney AR, Voyich JM, Argue CM, et al. Insights into pathogen immune evasion mechanisms: Anaplasma phagocytophilum fails to induce an apoptosis differentiation program in human neutrophils. J Immunol 2005, 174:6364-6372.
98. Suttmann H, Lehan N, Bohle A, Brandau S. Stimulation of neutrophil granulocytes with Mycobacterium bovis bacillus Calmette-Guerin induces changes in phenotype and gene expression and inhibits spontaneous apoptosis. Infect Immun 2003, 71:4647-4656.
99. Mullick A, Elias M, Harakidas P, Marcil A, WhitewayM, et al. Gene expression in HL60 granulocytoids and human polymorphonuclear leukocytes exposed to Candida albicans. Infect Immun 2004, 72:414-429.
100. Fradin C, Mavor AL, Weindl G, Schaller M, Hanke K, et al. The early transcriptional response of human granulocytes to infection with Candida albicans is not essential for killing but reflects cellular communications. Infect Immun 2007, 75:1493-1501.
101. Sukumaran B, Carlyon JA, Cai JL, Berliner N, Fikrig E. Early transcriptional response of human neutrophils to Anaplasma phagocytophilum infection. Infect Immun 2005, 73:8089-8099.
102. Lee HC, Kioi M, Han J, Puri RK, Goodman JL. Anaplasma phagocytophilum-induced gene expression in both human neutrophils and HL-60 cells. Genomics 2008, 92:144-151.
103. Lee HC, Goodman JL. Anaplasma phagocytophilum causes global induction of antiapoptosis in human neutrophils. Genomics 2006, 88:496-503.
104. Burlak C, Whitney AR, Mead DJ, Hackstadt T, DeLeo FR. Maturation of human neutrophil phagosomes includes incorporation ofmolecular chaperones and endoplasmic reticulum quality controlmachinery. Mol Cell Proteomics 2006, 5:620-634.
105. Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, et al. The phagosome proteome: insight into phagosome functions. J Cell Biol 2001, 152:165-180.
106. Gagnon E, Duclos S, Rondeau C, Chevet E, Cameron PH, et al. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 2002, 110:119-131.
107. Touret N, Paroutis P, Terebiznik M, Harrison RE, Trombetta S, et al. Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 2005, 123:157-170.
108. Touret N, Paroutis P, Grinstein S. The nature of the phagosomalmembrane: endoplasmic reticulum versus plasmalemma. J Leukoc Biol 2005, 77:878-885.
109. Gagnon E, Bergeron JJ, Desjardins M. ER-mediated phagocytosis: myth or reality? J Leukoc Biol 2005, 77:843-845.
110. Houde M, Bertholet S, Gagnon E, Brunet S,Goyette G, et al. Phagosomes are competent organelles for antigen cross-presentation. Nature 2003, 425:402-406.
111. Ackerman AL, Kyritsis C, Tampe R, Cresswell P. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc Natl Acad Sci U S A 2003, 100:12889-12894.
112. Guermonprez P, Saveanu L, Kleijmeer M, Davoust J, van EP, et al. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 2003, 425:397-402.
113. Lominadze G, Powell DW, Luerman GC, Link AJ, Ward RA, et al. Proteomic analysis of human neutrophil granules. Mol Cell Proteomics 2005, 4:1503-1521.
114. Jethwaney D, Islam MR, Leidal KG, de Bernabe DB, Campbell KP, et al. Proteomic analysis of plasma membrane and secretory vesicles from human neutrophils. Proteome Sci 2007, 5:12.
115. Savill J. Apoptosis in resolution of inflammation. J Leukoc Biol 1997, 61:375-380.
116. Shi J, Gilbert GE, Kokubo Y, Ohashi T. Role of the liver in regulating numbers of circulating neutrophils. Blood 2001, 98:1226-1230.
117. Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM, et al. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest 1989, 83:865-875.
118. Meagher LC, Cousin JM, Seckl JR, Haslett C. Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J Immunol 1996, 156:4422-4428.
119. Hannah S, Mecklenburgh K, Rahman I, Bellingan GJ, Greening A, et al. Hypoxia prolongs neutrophil survival in vitro. FEBS Lett 1995, 372:233-237.
120. Murray J, Barbara JA, Dunkley SA, Lopez AF, Van OX, et al. Regulation of neutrophil apoptosis by tumor necrosis factor-alpha: requirement for TNFR55 and TNFR75 for induction of apoptosis in vitro. Blood 1997, 90:2772-2783.
121. Whyte MK, Hardwick SJ, Meagher LC, Savill JS, Haslett C. Transient elevations of cytosolic free calcium retard subsequent apoptosis in neutrophils in vitro. J Clin Invest 1993, 92:446-455.
122. Bours MJ, Swennen EL, Di VF, Cronstein BN, Dagnelie PC. Adenosine 5'-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther 2006, 112:358-404.
123. Savill JS, Henson PM, Haslett C. Phagocytosis of aged human neutrophils by macrophages is mediated by a novel "charge-sensitive" recognition mechanism. J Clin Invest 1989, 84:1518-1527.
124. Hart SP, Ross JA, Ross K, Haslett C, Dransfield I. Molecular characterization of the surface of apoptotic neutrophils: Implications for functional downregulation and recognition by phagocytes. Cell Death Differ 2000, 7:493-503.
125. Homburg CH, de HM, von dem Borne AE, Verhoeven AJ, Reutelingsperger CP, et al. Human neutrophils lose their surface Fc gamma RIII and acquire Annexin V binding sites during apoptosis in vitro. Blood 1995, 85:532-540.
126. Kobayashi SD, Voyich JM, Braughton KR, DeLeo FR. Down-regulation of proinflammatory capacity during apoptosis in human polymorphonuclear leukocytes. J Immunol 2003, 170:3357-3368.
127. Fadok VA, Savill JS, Haslett C, Bratton DL, Doherty DE, et al. Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J Immunol 1992, 149:4029-4035.
128. Lane TA, Lamkin GE. A reassessmnt of the energy requirements for neutrophil migration: adenosine triphosphate depletion enhances chemotaxis. Blood 1984, 64:986-993.
129. Peachman KK, Lyles DS, Bass DA. Mitochondria in eosinophils: functional role in apoptosis but not respiration. Proc Natl Acad Sci U S A 2001, 98:1717-1722.
130. Fossati G, Moulding DA, Spiller DG, Moots RJ, White MR, et al. The mitochondrial network of human neutrophils: role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis. J Immunol 2003, 170:1964-1972.
131. Maianski NA,Mul FP, Van Buul JD, Roos D, Kuijpers TW. Granulocyte colony-stimulating factor inhibits the mitochondria-dependent activation of caspase-3 in neutrophils. Blood 2002, 99:672-679.
132. Pryde JG, Walker A, Rossi AG, Hannah S, Haslett C. Temperature-dependent arrest of neutrophil apoptosis. Failure of Bax insertion into mitochondria at 15 degrees C prevents the release of cytochrome c. J Biol Chem 2000, 275:33574-33584.
133. Maianski NA, Geissler J, Srinivasula SM, Alnemri ES, Roos D, et al. Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death Differ 2004, 11:143-153.
134. El KD, Jozsef L, Khreiss T, Filep JG. Inhibition of K+ efflux prevents mitochondrial dysfunction, and suppresses caspase-3-, apoptosis-inducing factor-, and endonuclease G-mediated constitutive apoptosis in human neutrophils. Cell Signal 2006, 18:2302-2313.
135. Murphy BM, O'Neill AJ, Adrain C, Watson RW, Martin SJ. The apoptosome pathway to caspase activation in primary human neutrophils exhibits dramatically reduced requirements for cytochrome C. J ExpMed 2003, 197:625-632.
136. Hill JM, Vaidyanathan H, Ramos JW, Ginsberg MH, Werner MH. Recognition of ERK MAP kinase by PEA-15 reveals a common docking site within the death domain and death effector domain. EMBO J 2002, 21:6494-6504.
137. Khwaja A, Tatton L. Caspase-mediated proteolysis and activation of protein kinase Cdelta plays a central role in neutrophil apoptosis. Blood 1999, 94:291-301.
138. Brown SB, Savill J. Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. J Immunol 1999, 162:480-485.
139. Scheel-Toellner D, Wang K, Craddock R, Webb PR, McGettrick HM, et al. Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood 2004, 104:2557-2564.
140. Liles WC, Kiener PA, Ledbetter JA, Aruffo A, Klebanoff SJ. Differential expression of Fas (CD95) and Fas ligand on normal human phagocytes: Implications for the regulation of apoptosis in neutrophils. J Exp Med 1996, 184:429-440.
141. Renshaw SA, Parmar JS, Singleton V, Rowe SJ, Dockrell DH, et al. Acceleration of human neutrophil apoptosis by TRAIL. J Immunol 2003, 170:1027-1033.
142. Scheel-Toellner D, Wang K, Assi LK, Webb PR, Craddock RM, et al. Clustering of death receptors in lipid rafts initiates neutrophil spontaneous apoptosis. Biochem Soc Trans 2004, 32:679-681.
143. Conus S, Perozzo R, Reinheckel T, Peters C, Scapozza L, et al. Caspase-8 is activated by cathepsin D initiating neutrophil apoptosis during the resolution of inflammation. J ExpMed 2008, 205:685-698.
144. Zhang B, Hirahashi J, Cullere X, Mayadas TN. Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: cross-talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. J Biol Chem2003, 278:28443-28454.
145. Baumann R, Casaulta C, Simon D, Conus S, Yousefi S, et al. Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway. FASEB J 2003, 17:2221-2230.
146. varado-Kristensson M, Melander F, Leandersson K, Ronnstrand L, Wernstedt C, et al. p38-MAPK signals survival by phosphorylation of caspase-8 and caspase-3 in human neutrophils. J Exp Med 2004, 199:449-458.
147. DeLeo FR. Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis 2004, 9:399-413.
148. Colotta F, Re F, Polentarutti N, Sozzani S, Mantovani A. Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 1992, 80:2012-2020.
149. Biffl WL, Moore EE, Moore FA, Barnett CC Jr. Interleukin-6 suppression of neutrophil apoptosis is neutrophil concentration dependent. J Leukoc Biol 1995, 58:582-584.
150. Kettritz R, Gaido ML, Haller H, Luft FC, Jennette CJ, et al. Interleukin-8 delays spontaneous and tumor necrosis factor-alpha-mediated apoptosis of human neutrophils. Kidney Int 1998, 53:84-91.
151. Dunican AL, Leuenroth SJ, Grutkoski P, Ayala A, Simms HH. TNFalpha-induced suppression of PMN apoptosis is mediated through interleukin-8 production. Shock 2000, 14:284-288.
152. Sakamoto E, Hato F, Kato T, Sakamoto C, Akahori M, et al. Type I and type II interferons delay human neutrophil apoptosis via activation of STAT3 and up-regulation of cellular inhibitor of apoptosis 2. J Leukoc Biol 2005, 78:301-309.
153. Lee A, Whyte MK, Haslett C. Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators. J Leukoc Biol 1993, 54:283-288.
154. van den Berg JM, Weyer S, Weening JJ, Roos D, Kuijpers TW. Divergent effects of tumor necrosis factor alpha on apoptosis of human neutrophils. J Leukoc Biol 2001, 69:467-473.
155. Avdi NJ, Nick JA, Whitlock BB, Billstrom MA, Henson PM, et al. Tumor necrosis factor-activation of the c-Jun N-terminal kinase pathway in human neutrophils. J Biol Chem2001, 276:2189-2199.
156. Ward C, Chilvers ER, Lawson MF, Pryde JG, Fujihara S, et al. NF-kappaB activation is a critical regulator of human granulocyte apoptosis in vitro. J Biol Chem 1999, 274:4309-4318.
157. Whitlock BB, Gardai S, Fadok V, Bratton D, Henson PM. Differential roles for alpha(M)beta(2) integrin clustering or activation in the control of apoptosis via regulation of akt and ERK survival mechanisms. J Cell Biol 2000, 151:1305-1320.
158. Rubel C, Gomez S, Fernandez GC, Isturiz MA, Caamano J, et al. Fibrinogen-CD11b/CD18 interaction activates the NF-kappa B pathway and delays apoptosis in human neutrophils. Eur J Immunol 2003, 33:1429-1438.
159. Gardai S, Whitlock BB, Helgason C, Ambruso D, Fadok V, et al. Activation of SHIP by NADPH oxidase-stimulated Lyn leads to enhanced apoptosis in neutrophils. J Biol Chem 2002, 277:5236-5246.
160. Francois S, El BJ, Dang PM, Pedruzzi E, Gougerot-PocidaloMA, et al. 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. J Immunol 2005, 174:3633-3642.
161. Moulding DA, Walter C, Hart CA, Edwards SW. Effects of staphylococcal enterotoxins on human neutrophil functions and apoptosis. Infect Immun 1999, 67:2312-2318.
162. Liu J, Akahoshi T, Sasahana T, Kitasato H, Namai R, et al. Inhibition of neutrophil apoptosis by verotoxin 2 derived from Escherichia coli O157:H7. Infect Immun 1999, 67:6203-6205.
163. Brigotti M, Carnicelli D, Ravanelli E, Barbieri S, Ricci F, et al. Interactions between Shiga toxins and human polymorphonuclear leukocytes. J Leukoc Biol 2008, 84:1019-1027.
164. Liles WC, Thomsen AR, O'Mahony DS, Klebanoff SJ. Stimulation of human neutrophils and monocytes by staphylococcal phenol-soluble modulin. J Leukoc Biol 2001, 70:96-102.
165. Coxon A, Rieu P, Barkalow FJ, Askari S, Sharpe AH, et al. A novel role for the. 2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity 1996, 5:653-666.
166. Gamberale R, Giordano M, Trevani AS, Andonegui G, Geffner JR. Modulation of human neutrophil apoptosis by immune complexes. J Immunol 1998, 161:3666-3674.
167. Watson RW, Redmond HP, Wang JH, Bouchier-Hayes D. Bacterial ingestion, tumor necrosis factoralpha, and heat induce programmed cell death in activated neutrophils. Shock 1996, 5:47-51.
168. Engelich G, White M, Hartshorn KL. Neutrophil survival is markedly reduced by incubation with influenza virus and Streptococcus pneumoniae: role of respiratory burst. J Leukoc Biol 2001, 69:50-56.
169. Yoshiie K, Kim HY, Mott J, Rikihisa Y. Intracellular infection by the human granulocytic ehrlichiosis agent inhibits human neutrophil apoptosis. Infect Immun 2000, 68:1125-1133.
170. van ZG, Gieffers J, Kothe H, Rupp J, Bollinger A, et al. Chlamydia pneumoniae multiply in neutrophil granulocytes and delay their spontaneous apoptosis. J Immunol 2004, 172:1768-1776.
171. Wang R, Braughton KR, Kretschmer D, Bach TH, Queck SY, et al. Identification of novel cytolytic peptides as key virulence determinants for communityassociated MRSA. Nat Med 2007, 13:1510-1514.
172. Voyich JM, Braughton KR, Sturdevant DE, Whitney AR, Said-Salim B, et al. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 2005, 175:3907-3919.
173. Genestier AL, Michallet MC, Prevost G, Bellot G, Chalabreysse L, et al. Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. J Clin Invest 2005, 115:3117-3127.
174. Usher LR, Lawson RA, Geary I, Taylor CJ, Bingle CD, et al. Induction of neutrophil apoptosis by the Pseudomonas aeruginosa exotoxin pyocyanin: a potential mechanism of persistent infection. J Immunol 2002, 168:1861-1868.
175. Ward C, Dransfield I, Chilvers ER, Haslett C, Rossi AG. Pharmacological manipulation of granulocyte apoptosis: potential therapeutic targets. Trends Pharmacol Sci 1999, 20:503-509.
176. Kobayashi SD, Voyich JM, Somerville GA, Braughton KR, Malech HL, et al. An apoptosis-differentiation program in human polymorphonuclear leukocytes facilitates resolution of inflammation. J Leukoc Biol 2003, 73:315-322.
177. Musser JM, DeLeo FR. Toward a genome-wide systems biology analysis of host-pathogen interactions in group A Streptococcus. Am J Pathol 2005, 167:1461-1472.
178. Mott J, Rikihisa Y. Human granulocytic ehrlichiosis agent inhibits superoxide anion generation by human neutrophils. Infect Immun 2000, 68:6697-6703.
179. Carlyon JA, Latif DA, Pypaert M, Lacy P, Fikrig E. Anaplasma phagocytophilum utilizes multiple host evasion mechanisms to thwart NADPH oxidasemediated killing during neutrophil infection. Infect Immun 2004, 72:4772-4783.
180. Carlyon JA, Chan WT, Galan J, Roos D, Fikrig E. Repression of rac2 mRNA expression by Anaplasma phagocytophila is essential to the inhibition of superoxide production and bacterial proliferation. J Immunol 2002, 169:7009-7018.
181. Banerjee R, Anguita J, Roos D, Fikrig E. Cutting edge: infection by the agent of human granulocytic ehrlichiosis prevents the respiratory burst by down-regulating gp91phox. J Immunol 2000, 164:3946-3949.
182. Persson YA, Blomgran-Julinder R, Rahman S, Zheng L, Stendahl O. 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 Infect 2008, 10:233-240.
183. McPhillips K, JanssenWJ, GhoshM, Byrne A, Gardai S, et al. TNF-alpha inhibits macrophage clearance of apoptotic cells via cytosolic phospholipase A2 and oxidant-dependent mechanisms. J Immunol 2007, 178:8117-8126.
184. Michlewska S, Dransfield I, Megson IL, Rossi AG. Macrophage phagocytosis of apoptotic neutrophils is critically regulated by the opposing actions of proinflammatory and anti-inflammatory agents: key role for TNF-alpha. FASEB J 2009, 23:844-854.
185. Volpp BD, Nauseef WM, Clark RA. Two cytosolic neutrophil oxidase components absent in autosomal chronic granulomatous disease. Science 1988, 242:1295-1297.
186. Curnutte JT, Scott PJ, Mayo LA. Cytosolic components of the respiratory burst oxidase: resolution of four components, two of which are missing in complementing types of chronic granulomatous disease. Proc Natl Acad Sci U S A 1989, 86:825-829.
187. Nunoi H, Rotrosen D, Gallin JI, Malech HL. Two forms of autosomal chronic granulomatous disease lack distinct neutrophil cytosol factors. Science 1988, 242:1298-1301.
188. Hamers MN, deBoer M, Meirhof LJ, Weening RS, Roos D. Complementation in monocyte hybrids revealing genetic heterogeneity in chronic granulomatous disease. Nature 1984, 307:553-555.
189. Royer-Pokora B, Kunkel LM, Monaco AP, Goff SC, Newburger PE, et al. Cloning the gene for an inherited human disorder-chronic granulomatous disease-on the basis of its chromosomal location. Nature 1986, 322:32-38.
190. Lekstrom-Himes JA, Gallin JI. Immunodeficiency diseases caused by defects in phagocytes. N Engl J Med 2000, 343:1703-1714.
191. Kobayashi SD, Voyich JM, Braughton KR, Whitney AR, Nauseef WM, et al. Gene expression profiling provides insight into the pathophysiology of chronic granulomatous disease. J Immunol 2004, 172:636-643.
192. Lekstrom-Himes JA, Kuhns DB, Alvord WG, Gallin JI. Inhibition of human neutrophil IL-8 production by hydrogen peroxide and dysregulation in chronic granulomatous disease. J Immunol 2005, 174:411-417.
193. Lekstrom-Himes J, Xanthopoulos KG. Biological role of the CCAAT/enhancer-binding protein family of transcription factors. J Biol Chem 1998, 273:28545-28548.
194. Yamanaka R, Barlow C, Lekstrom-Himes J, Castilla LH, Liu PP, et al. Impaired granulopoiesis, myelodysplasia, and early lethality in CCAAT/enhancer binding protein epsilon-deficient mice. Proc Natl Acad Sci U S A 1997, 94:13187-13192.
195. Lekstrom-Himes J, Xanthopoulos KG. CCAAT/enhancer binding protein epsilon is critical for effective neutrophil-mediated response to inflammatory challenge. Blood 1999, 93:3096-3105.
196. Gombart AF, Krug U, O'Kelly J, An E, Vegesna V, et al. Aberrant expression of neutrophil and macrophage-related genes in a murine model for human neutrophil-specific granule deficiency. J Leukoc Biol 2005, 78:1153-1165.
197. Davis SD, Schaller J, Wedgwood RJ. Job's Syndrome. Recurrent, "cold", staphylococcal abscesses. Lancet 1966, 1:1013-1015.
198. Minegishi Y, Saito M, Tsuchiya S, Tsuge I, Takada H, et al. Dominant-negative mutations in the DNAbinding domain of STAT3 cause hyper-IgE syndrome. Nature 2007, 448:1058-1062.
199. O'Shea JJ, Murray PJ. Cytokine signaling modules in inflammatory responses. Immunity 2008, 28:477-487.
200. Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and proresolution lipid mediators. Nat Rev Immunol 2008, 8:349-361.
201. Hong S, Porter TF, Lu Y, Oh SF, Pillai PS, et al. Resolvin E1 metabolome in local inactivation during inflammation-resolution. J Immunol 2008, 180:3512-3519.
202. Serhan CN, Lu Y, Hong S, Yang R. Mediator lipidomics: search algorithms for eicosanoids, resolvins, and protectins. Methods Enzymol 2007, 432:275-317.
203. Serhan CN,Hong S, Lu Y. Lipidmediator informaticslipidomics: novel pathways in mapping resolution. AAPS J 2006, 8:E284-E297.
204. Ley TJ, Mardis ER, Ding L, Fulton B, McLellan MD, et al. DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature 2008, 456:66-72.