Constitutive neutrophil apoptosis: Mechanisms and regulation

American Journal of Hematology

Volumn 83, Issue 4, 2008, Pages 288-295

  Luo, Hongbo R ^a,b,c,d   Loison, Fabien ^a,b,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c DANA FARBER HARVARD CANCER CENTER   (United States)

^d Karp Family Research Building ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CASPASE; CYTOKINE; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; CELL ADHESION; CELL FUNCTION; CELL SURVIVAL; ERYTHROCYTE; HOMEOSTASIS; HUMAN; IMMUNOPATHOLOGY; INFLAMMATION; MICROENVIRONMENT; MITOCHONDRION; MOLECULAR MECHANICS; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOOD PLATELETS; CALPAIN; CASPASES; CYTOKINES; ERYTHROCYTES; HOMEOSTASIS; HUMANS; HYDROGEN-ION CONCENTRATION; INFECTION; INFLAMMATION; MITOCHONDRIA; NEUTROPHILS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; RECEPTORS, DEATH DOMAIN; SIGNAL TRANSDUCTION;

EID: 41449105534     PISSN: 03618609     EISSN: 10968652     Source Type: Journal    
DOI: 10.1002/ajh.21078     Document Type: Review

References (148)

1. Akgul C, Moulding DA, Edwards SW. Molecular control of neutrophil apoptosis. FEBS Lett 2001;487:318-322.
2. Maianski NA, Maianski AN, Kuijpers TW, Roos D. Apoptosis of neutrophils. Acta Haematol 2004;111:56-66.
3. Squier MK, Sehnert AJ, Cohen JJ. Apoptosis in leukocytes. J Leukoc Biol 1995;57:2-10.
4. Scheel-Toellner D, Wang KQ, Webb PR, et al. Early events in spontaneous neutrophil apoptosis. Biochem Soc Trans 2004;32 (Part 3):461-464.
5. Webb PR, Wang KQ, Scheel-Toellner D, et al. Regulation of neutrophil apoptosis: A role for protein kinase C and phosphatidylinositol-3-kinase. Apoptosis 2000;5:451-458.
6. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004;303:1532-1535.
7. Fuchs TA, Abed U, Goosmann C, et al. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007;176:231-241.
8. Beiter K, Wartha F, Albiger B, et al. An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 2006;16:401-407.
9. Kanduc D, Mittelman A, Serpico R, et al. Cell death: Apoptosis versus necrosis (review). Int J Oncol 2002;21:165-170.
10. Aigner T. Apoptosis, necrosis, or whatever: How to find out what really happens? J Pathol 2002;198:1-4.
11. Zhivotovsky B. Apoptosis, necrosis and between. Cell Cycle 2004;3:64-66.
12. Savill JS, Wyllie AH, Henson JE, 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.
13. Payne CM, Glasser L, Tischler ME, et al. Programmed cell death of the normal human neutrophil: An in vitro model of senescence. Microsc Res Tech 1994;28:327-344.
14. Savill J. Apoptosis in resolution of inflammation. J Leukoc Biol 1997;61:375-380.
15. Whyte MK, Meagher LC, MacDermot J, Haslett C. Impairment of function in aging neutrophils is associated with apoptosis. J Immunol 1993,150:5124-1534.
16. Dransfield I, Stocks SC, Haslett C. Regulation of cell adhesion molecule expression and function associated with neutrophil apoptosis. Blood 1995;85:3264-3273.
17. Jones J, Morgan BP. Apoptosis is associated with reduced expression of complement regulatory molecules, adhesion molecules and other receptors on polymorphonuclear leucocytes: Functional relevance and role in inflammation. Immunology 1995;86:651-660.
18. Ayub K, Hallett MB. Ca2+ influx shutdown during neutrophil apoptosis: Importance and possible mechanism. Immunology 2004;111:8-12.
19. Tsujimoto Y, Shimizu S. Another way to die: Autophagic programmed cell death. Cell Death Differ 2005;12 (Suppl 2):1528-1534.
20. Bursch W, Ellinger A, Gerner C, et al. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann N Y Acad Sci 2000;926:1-12.
21. von Gunten S, Simon HU. Autophagic-like cell death in neutrophils induced by autoantibodies. Autophagy 2007;3:67-68.
22. Fay AJ, Qian X, Jan YN, Jan LY. SK channels mediate NADPH oxidase-independent reactive oxygen species production and apoptosis in granulocytes. Proc Natl Acad Sci USA 2006;103:17548-17553.
23. Maianski NA, Geissler J, Srinivasula SM, et al. Functional characterization of mitochondria in neutrophils: A role restricted to apoptosis. Cell Death Differ 2004;11:143-153.
24. Pryde JG, Walker A, Rossi AG, et al. 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.
25. Murphy BM, O'Neill AJ, Adrain C, et al. The apoptosome pathway to caspase activation in primary human neutrophils exhibits dramatically reduced requirements for cytochrome C. J Exp Med 2003;197:625-632.
26. Liu CY, Takemasa A, Liles WC, et al. Broad-spectrum caspase inhibition paradoxically augments cell death in TNFα-stimulated neutrophils. Blood 2003;101:295-304.
27. Yamamoto A, Taniuchi S, Tsuji S, et al. Role of reactive oxygen species in neutrophil apoptosis following ingestion of heat-killed Staphylococcus aureus. Clin Exp Immunol 2002;129:479-484.
28. Kasahara Y, Iwai K, Yachie A, et al. Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/APO-1)-mediated apoptosis of neutrophils. Blood 1997;89:1748-1753.
29. Lundqvist-Gustafsson H, Bengtsson T. Activation of the granule pool of the NADPH oxidase accelerates apoptosis in human neutrophils. J Leukoc Biol 1999;65:196-204.
30. Perskvist N, Long M, Stendahl O, Zheng L. Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol 2002;168:6358-6365.
31. Coxon A, Rieu P, Barkalow FJ, et al. A novel role for the β2 integrin CD11b/CD18 in neutrophil apoptosis: A homeostatic mechanism in inflammation. Immunity 1996;5:653-666.
32. Tortorella C, Piazzolla G, Spaccavento F, et al. Age-related effects of oxidative metabolism and cyclic AMP signaling on neutrophil apoptosis. Mech Ageing Dev 1999;110:195-205.
33. Ye J, Wang S, Leonard SS, et al. Role of reactive oxygen species and p53 in chromium(VI)-induced apoptosis. J Biol Chem 1999;274:34974-34980.
34. Huang C, Zhang Z, Ding M, et al. Vanadate induces p53 transactivation through hydrogen peroxide and causes apoptosis. J Biol Chem 2000;275:32516- 32522.
35. 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 Chem 2003;278:28443-28454.
36. Kwon YW, Masutani H, Nakamura H, et al. Redox regulation of cell growth and cell death. Biol Chem 2003;384:991-996.
37. Fortenberry JD, Owens ML, Chen NX, Brown LA. S-nitrosoglutathione inhibits TNFα-induced NFkappaB activation in neutrophils. Inflamm Res 2001;50:89-95.
38. Kamata H, Honda S, Maeda S, et al. Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005;120:649-661.
39. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000;103:239-252.
40. Scheel-Toellner D, Wang K, Assi LK, et al. Clustering of death receptors in lipid rafts initiates neutrophil spontaneous apoptosis. Biochem Soc Trans 2004;32 (Part 5):679-681.
41. Scheel-Toellner D, Wang K, Craddock R, et al. Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood 2004;104:2557-2564.
42. Blomgran R, Zheng L, Stendahl O. Cathepsin-cleaved Bid promotes apoptosis in human neutrophils via oxidative stress-induced lysosomal membrane permeabilization. J Leukoc Biol 2007;81:1213-1223.
43. Blomgran R, Zheng L, Stendahl O. Uropathogenic Escherichia coli triggers oxygen-dependent apoptosis in human neutrophils through the cooperative effect of type 1 fimbriae and lipopolysaccharide. Infect Immun 2004;72:4570-4578.
44. Fortenberry JD, Owens ML, Brown LA. S-nitrosoglutathione enhances neutrophil DNA fragmentation and cell death. Am J Physiol 1999;276(3, Part 1):L435-L442.
45. Fortenberry JD, Owens ML, Brown MR, et al. Exogenous nitric oxide enhances neutrophil cell death and DNA fragmentation. Am J Respir Cell Mol Biol 1998;18:421-428.
46. Taylor EL, Megson IL, Haslett C, Rossi AG. Nitric oxide: A key regulator of myeloid inflammatory cell apoptosis. Cell Death Differ 2003;10:418-430.
47. Ward C, Wong TH, Murray J, et al. Induction of human neutrophil apoptosis by nitric oxide donors: Evidence for a caspase-dependent, cyclic-GMP- independent mechanism. Biochem Pharmacol 2000;59:305-314.
48. Blaylock MG, Cuthbertson BH, Galley HF, et al. The effect of nitric oxide and peroxynitrite on apoptosis in human polymorphonuclear leukocytes. Free Radic Biol Med 1998;25:748-752.
49. Fadeel B, Ahlin A, Henter JI, et al. Involvement of caspases in neutrophil apoptosis: Regulation by reactive oxygen species. Blood 1998;92:4808-4818.
50. Ascenzi P, Salvati L, Bolognesi M, et al. Inhibition of cysteine protease activity by NO-donors. Curr Protein Pept Sci 2001;2:137-153.
51. Ishihara Y, Shimamoto N. Involvement of endonuclease G in nucleosomal DNA fragmentation under sustained endogenous oxidative stress. J Biol Chem 2006;281:6726-6733.
52. Hengartner MO, Horvitz HR. Programmed cell death in Caenorhabditis elegans. Curr Opin Genet Dev 1994;4:581-586.
53. Daigle I, Simon HU. Critical role for caspases 3 and 8 in neutrophil but not eosinophil apoptosis. Int Arch Allergy Immunol 2001;126:147-156.
54. Zhu D, Hattori H, Jo H, et al. Deactivation of phosphatidylinositol 3,4,5-trisphosphate/Akt signaling mediates neutrophil spontaneous death. Proc Natl Acad Sci USA 2006;103:14836-14841.
55. Yuan J, Yankner BA. Apoptosis in the nervous system. Nature 2000;407:802-809.
56. Budihardjo I, Oliver H, Lutter M, et al. Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 1999;15:269-290.
57. Maianski NA, Roos D, Kuijpers TW. Bid truncation, bid/bax targeting to the mitochondria, and caspase activation associated with neutrophil apoptosis are inhibited by granulocyte colony-stimulating factor. J Immunol 2004;172:7024-7030.
58. Fossati G, Moulding DA, Spiller DG, et al. The mitochondrial network of human neutrophils: Role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis. J Immunol 2003;170:1964-19672.
59. Moulding DA, Quayle JA, Hart CA, Edwards SW. Mcl-1 expression in human neutrophils: Regulation by cytokines and correlation with cell survival. Blood 1998;92:2495-2502.
60. Edwards SW, Derouet M, Howse M, Moots RJ. Regulation of neutrophil apoptosis by Mcl-1. Biochem Soc Trans 2004;32 (Part 3):489-492.
61. El Kebir D, 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.
62. Knepper-Nicolai B, Savill J, Brown SB. Constitutive apoptosis in human neutrophils requires synergy between calpains and the proteasome downstream of caspases. J Biol Chem 1998;273:30530-30536.
63. Squier MK, Sehnert AJ, Sellins KS, et al. Calpain and calpastatin regulate neutrophil apoptosis. J Cell Physiol 1999;178:311-319.
64. Altznauer F, Conus S, Cavalli A, et al. Calpain-1 regulates Bax and subsequent Smac-dependent caspase-3 activation in neutrophil apoptosis. J Biol Chem 2004;279:5947-5957.
65. Kobayashi S, Yamashita K, Takeoka T, et al. Calpain-mediated X-linked inhibitor of apoptosis degradation in neutrophil apoptosis and its impairment in chronic neutrophilic leukemia. J Biol Chem 2002;277:33968-33977.
66. Subramanian KK, Jia Y, Zhu D, et al. Tumor suppressor PTEN is a physiologic suppressor of chemoattractant-mediated neutrophil functions. Blood 2007;109:4028-4037,
67. Yang KY, Arcaroli J, Kupfner J, et al. Involvement of phosphatidylinositol 3-kinase γ in neutrophil apoptosis. Cell Signal 2003;15:225-233.
68. Vivanco I, Sawyers CL. Th6 phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2002;2:489-501.
69. Brazil DP, Park J, Hemmings BA. PKB binding proteins. Getting in on the Akt. Cell 2002;111:293-303.
70. Gardai SJ, Hildeman DA, Frankel SK, et al. Phosphorylation of Bax Ser184 by Akt regulates its activity and apoptosis in neutrophils. J Biol Chem 2004;279:21085-21095.
71. Choi M, Rolle S, Wellner M, et al. Inhibition of NF-kappaB by a TAT-NEMO-binding domain peptide accelerates constitutive apoptosis and abrogates LPS-delayed neutrophil apoptosis. Blood 2003;102:2259-2267.
72. Ward C, Chilvers ER, Lawson MF, et al. NF-kappaB activation is a critical regulator of human granulocyte apoptosis in vitro. J Biol Chem 1999;274:4309-4318.
73. Crossley LJ. Neutrophil activation by fMLP regulates FOXO (forkhead) transcription factors by multiple pathways, one of which includes the binding of FOXO to the survival factor Mcl-1. J Leukoc Biol 2003;74:583-592.
74. Alvarado-Kristensson M, Pom-Ares MI, Grethe S, et al. p38 Mitogen-activated protein kinase and phosphatidylinositol 3-kinase activities have opposite effects on human neutrophil apoptosis. FASEB J 2002;16:129-131.
75. Villunger A, O'Reilly LA, Holler N, et al. Fas ligand, Bcl-2, granulocyte colony-stimulating factor, and p38 mitogen-activated protein kinase: Regulators of distinct cell death and survival pathways in granulocytes. J Exp Med 2000; 192:647-658.
76. Alvarado-Kristensson M, Melander F, Leandersson K, et al. p38-MAPK signals survival by phosphorylat on of caspase-8 and caspase-3 in human neutrophils. J Exp Med 2004;199:449-458.
77. Pongracz J, Webb P, Wang K, et al. Spontaneous neutrophil apoptosis involves caspase 3-mediatec activation of protein kinase Cδ. J Biol Chem 1999;274:37329-37334.
78. Khwaja A, Tatton L. Caspase-mediated proteolysis and activation of protein kinase Cδ plays a central role in neutrophil apoptosis. Blood 1999;94:291-301.
79. Sakamoto E, Hato F, Kato T, 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.
80. Murray DA, Wilton JM. Lipopolysaccharide from the periodontal pathogen Porphyromonas gingivalis prevents apoptosis of HL60-derived neutrophils in vitro. Infect Immun 2003;71:7232-7235.
81. Francois S, El Benna J, Dane PM, 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.
82. Zhang X, Kluger Y, Nakayama Y, et al. Gene expression in mature neutrophils: Early responses to inflammatory stimuli. J Leukoc Biol 2004;75:358-372.
83. Wei S, Liu JH, Epling-Burnette PK, et al. Critical role of Lyn kinase in inhibition of neutrophil apoptosis by granulocyte-macrophage colony-stimulating factor. J Immunol 1996;157:5-55-5162.
84. 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.
85. Yasui K, Sekiguchi Y, Ichikawa M, et al. Granulocyte macrophage-colony stimulating factor delays neutrophil apoptosis and primes its function through Ia-type phosphoinositide 3-kinase. J Leukoc Biol 2002;72:1020-1026.
86. Bruno A, Conus S, Schmid I, Simon HU. Apoptotic pathways are inhibited by leptin receptor activation in neutrophils. J Immunol 2005;174:8090-8096.
87. Coxon A, Tang T, Mayadas TN. Cytokine-activated endothelial cells delay neutrophil apoptosis in vitro and in vivo. A role for granulocyte/macrophage colony-stimulating factor. J Exp Med 1999;190:923-934.
88. Ross EA, Douglas MR, Wong SH, et al. Interaction between integrin α9β1 and vascular cell adhesion molecule-1 (VCAM-1) inhibits neutrophil apoptosis. Blood 2006;107:1178-1183.
89. Aoshiba K, Nakajima Y, Yasu S, et al. Red blood cells inhibit apoptosis of human neutrophils. Blood 1993;93:4006-4010.
90. Arruda MA, Rossi AG, de Fretas MS, et al. Heme inhibits human neutrophil apoptosis: Involvement of phosphoinositide 3-kinase, MAPK, and NF-kappaB. J Immunol 2004;173:2023-2030.
91. Andonegui G, Trevani AS, Lopez DH, et al. Inhibition of human neutrophil apoptosis by platelets. J Immunol 1997;158:3372-3377.
92. Liles WC, Kiener PA, Ledbetter JA, et al. 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.
93. Brown SB, Savill J. Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. J Immunol 1999;162:480-485.
94. Renshaw SA, Timmons SJ, Eaton V, et al. Inflammatory neutrophils retain susceptibility to apoptosis mediated via the Fas death receptor. J Leukoc Biol 2000;67:662-668.
95. Watson RW, O'Neill A, Brannigan AE, et al. Regulation of Fas antibody induced neutrophil apoptosis is both caspase and mitochondrial dependent. FEBS Lett 1999;453:67-71.
96. Gross A, Yin XM, Wang K, et al. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 1999;274:1156-1163.
97. Fecho K, Cohen PL. Fas ligand (gld)- and Fas (lpr)-deficient mice do not show alterations in the extravasation or apoptosis of inflammatory neutrophils. J Leukoc Biol 1998;64:373-383.
98. Koga Y, Matsuzaki A, Suminoe A, et al. Neutrophil-derived TNF-related apoptosis-inducing ligand (TRAIL): A novel mechanism of antitumor effect by neutrophils. Cancer Res 2004;64:1037-1043.
99. Kamohara H, Matsuyama W, Shimozato O, et al. Regulation of tumour necrosis factor-related apoptosis-inducing ligand (TRAIL) and TRAIL receptor expression in human neutrophils. Immunology 2004;111:186-194.
100. Lum JJ, Bren G, McClure R, Badley AD. Elimination of senescent neutrophils by TNF-related apoptosis-inducing [corrected] ligand. J Immunol 2005;175:1232-1238.
101. Daigle I, Simon HU. Alternative functions for TRAIL receptors in eosinophils and neutrophils. Swiss Med Wkly 2001;131:231-237.
102. Renshaw SA, Parmar JS, Singleton V, et al. Acceleration of human neutrophil apoptosis by TRAIL. J Immunol 2003;170:1027-1033.
103. Matsuyama W, Yamamoto M, Higashimoto I, et al. TNF-related apoptosis-inducing ligand is involved in neutropenia of systemic lupus erythematosus. Blood 2004;104:184-191.
104. Watson RW, Redmond HP, Wang JH, et al. Neutrophils undergo apoptosis following ingestion of Escherichia coli. J Immunol 1996;156:3986-3992.
105. Colamussi ML, White MR, Crouch E, Hartshorn KL. Influenza A virus accelerates neutrophil apoptosis and markedly potentiates apoptotic effects of bacteria. Blood 1999;93:2395-2403.
106. Kobayashi SD, Voyich JM, Buhl CL, et al. 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 USA 2002;99:6901-6906.
107. Kobayashi SD, Braughton KR, Whitney AR, et al. Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proc Natl Acad Sci USA 2003;100:10948-10953.
108. Akgul C, Edwards SW. Regulation of neutrophil apoptosis via death receptors. Cell Mol Life Sci 2003;60:2402-2408.
109. van den Berg JM, Weyer S, Weening JJ, et al. Divergent effects of tumor necrosis factor α on apoptosis of human neutrophils. J Leukoc Biol 2001;69:467-473.
110. Maianski NA, Roos D, Kuijpers TW. Tumor necrosis factor α induces a caspase-independent death pathway in human neutrophils. Blood 2003;101:1987-1995.
111. Avdi NJ, Nick JA, Whitlock BB, et al. Tumor necrosis factor-α activation of the c-Jun N-terminal kinase pathway in human neutrophils. Integrin involvement in a pathway leading from cytoplasmic tyrosine kinases apoptosis. J Biol Chem 2001;276:2189-2199.
112. Daigle I, Yousefi S, Colonna M, et al. Death receptors bind SHP-1 and block cytokine-induced anti-apoptotic signaling in neutrophils. Nat Med 2002;8:61-67.
113. Chen HC, Wang CJ, Chou CL, et al. Tumor necrosis factor-α induces caspase-independent cell death in human neutrophils via reactive oxidants and is associated with calpain activity. J Biomed Sci 2006;13:261-273.
114. Kilpatrick LE, Lee JY, Haines KM, et al. A role for PKC-δ and PI 3-kinase in TNFα-mediated antiapoptotic signaling in the human neutrophil. Am J Physiol Cell Physiol 2002;283:C48-C57.
115. Cowburn AS, Deighton J, Walmsley SR, Chilvers ER. The survival effect of TNFα in human neutrophils is mediated via NF-kappa B-dependent IL-8 release. Eur J Immunol 2004;34:1733-1743.
116. Dunican AL, Leuenroth SJ, Grutkoski P, et al. TNFα-induced suppression of PMN apoptosis is mediated through interleukin-8 production. Shock 2000;14:284-288; discussion 288-289.
117. Zu YL, Qi J, Gilchrist A, et al. p38 mitogen-activated protein kinase activation is required for human neutrophil function triggered by TNFα or FMLP stimulation. J Immunol 1998;160:1982-1989.
118. Moulding DA, Akgul C, Derouet M, et al. BCL-2 family expression in human neutrophils during delayed and accelerated apoptosis. J Leukoc Biol 2001;70:783-792.
119. Kilpatrick LE, Sun S, Mackie D, et al. Regulation of TNF mediated antiapoptotic signaling in human neutrophils: Role of δ-PKC and ERK1/2. J Leukoc Biol 2006;80:1512-1521.
120. Cross A, Barnes T, Bucknall RC, et al. Neutrophil apoptosis in rheumatoid arthritis is regulated by local oxygen tensions within joints. J Leukoc Biol 2006;80:521-528.
121. Parsey MV, Kaneko D, Shenkar R, Abraham E. Neutrophil apoptosis in the lung after hemorrhage or endotoxemia: Apoptosis and migration are independent of interleukin-1β. Chest 1999;116(1 Suppl):67S-68S.
122. Keel M, Ungethum U, Steckholzer U, et al. Interleukin-10 counterregulates proinflammatory cytokine-induced inhibition of neutrophil apoptosis during severe sepsis. Blood 1997;90:3356-3363.
123. Ertel W, Keel M, Infanger M, et al. Circulating mediators in serum of injured patients with septic complications inhibit neutrophil apoptosis through up-regulation of protein-tyrosine phosphorylation. J Trauma 1998;44:767-775; discussion 775-776.
124. Chitnis D, Dickerson C, Munster AM, Winchurch RA. Inhibition of apoptosis in polymorphonuclear neutrophils from burn patients. J Leukoc Biol 1996;59:835-839.
125. Jimenez MF, Watson RW, Parodo J, et al. Dysregulated expression of neutrophil apoptosis in the systemic inflammatory response syndrome. Arch Surg 1997;132:1263-1269; discussion 1269-1270.
126. Melley DD, Evans TW, Quinlan GJ. Redox regulation of neutrophil apoptosis and the systemic inflammatory response syndrome. Clin Sci (Lond) 2005;108:413-424.
127. Walley KR, Lukacs NW, Standiford TJ, et al. Elevated levels of macrophage inflammatory protein 2 in severe murine peritonitis increase neutrophil recruitment and mortality. Infect Immun 1997;65:3847-3851.
128. Mercer-Jones MA, Heinzelmann M, Peyton JC, et al. Inhibition of neutrophil migration at the site of infection increases remote organ neutrophil sequestration and injury. Shock 1997;8:193-199.
129. Wickel DJ, Cheadle WG, Mercer-Jones MA, Garrison RN. Poor outcome from peritonitis is caused by disease acuity and organ failure, not recurrent peritoneal infection. Ann Surg 1997;225:744-753; discussion 753-756.
130. Akahoshi T, Nagaoka T, Namai R, et al. Prevention of neutrophil apoptosis by monosodium urate crystals. Rheumatol Int 1997;16:231-235.
131. Tudan C, Jackson JK, Blanis L, et al. Inhibition of TNFα-induced neutrophil apoptosis by crystals of calcium pyrophosphate dihydrate is mediated by the extracellular signal-regulated kinase and phosphatidylinositol 3-kinase/Akt pathways up-stream of caspase 3. J Immunol 2000;165:5798-5806.
132. Ina K, Kusugami K, Hosokawa T, et al. Increased mucosal production of granulocyte colony-stimulating factor is related to a delay in neutrophil apoptosis in Inflammatory Bowel disease. J Gastroenterol Hepatol 1999;14:46-53.
133. Ottonello L, Cutolo M, Frumento G, et al. Synovial fluid from patients with rheumatoid arthritis inhibits neutrophil apoptosis: role of adenosine and proinflammatory cytokines. Rheumatology (Oxford) 2002;41:1249-1260.
134. Peng SL. Neutrophil apoptosis in autoimmunity. J Mol Med 2006;84:122-125.
135. Kuijpers TW, Maianski NA, Tool AT, et al. Apoptotic neutrophils in the circulation of patients with glycogen storage disease type 1b (GSD1b). Blood 2003;101:5021-5024.
136. Harper L, Cockwell P, Adu D, Savage CO. Neutrophil priming and apoptosis in anti-neutrophil cytoplasmic autoantibody-associated vasculitis. Kidney Int 2001;59:1729-1738.
137. Rauova L, Gilburd B, Zurgil N, et al. Induction of biologically active antineutrophil cytoplasmic antibodies by immunization with human apoptotic polymorphonuclear leukocytes. Clin Immunol 2002;103:69-78.
138. Ren Y, Tang J, Mok MY, et al. Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum 2003;48:2888-2897.
139. Sendo F, Kato T, Yazawa H. Modulation of neutrophil apoptosis by psychological stress and glucocorticoid. Int J Immunopharmacol 1997;19:511-516.
140. Sendo F, Tsuchida H, Takeda Y, et al. Regulation of neutrophil apoptosis - Its biological significance in inflammation and the immune response. Hum Cell 1996;9:215-222.
141. Savill J, Haslett C. Granulocyte clearance by apoptosis in the resolution of inflammation. Semin Cell Biol 1995;6:385-393.
142. Walker A, Ward C, Taylor EL, et al. Regulation of neutrophil apoptosis and removal of apoptotic cells. Curr Drug Targets Inflamm Allergy 2005;4:447-454.
143. Hughes J, Johnson RJ, Mooney A, et al. Neutrophil fate in experimental glomerular capillary injury in the rat. Emigration exceeds in situ clearance by apoptosis. Am J Pathol 1997;150:223-234.
144. Buckley CD, Ross EA, McGettrick HM, et al. Identification of a phenotypically and functionally distinct population of long-lived neutrophils in a model of reverse endothelial migration. J Leukoc Biol 2006;79:303-311.
145. Schwab JM, Chiang N, Arita M, Serhan CN. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007;447:869-874.
146. Cowburn AS, Sobolewski A, Reed BJ, et al. Aminopeptidase N (CD13) regulates tumor necrosis factor-α-induced apoptosis in human neutrophils. J Biol Chem 2006;281:12458-12467.
147. El Kebir D, Jozsef L, Khreiss T, et al. Aspirin-triggered lipoxins override the apoptosis-delaying action of serum amyloid a in human neutrophils: A novel mechanism for resolution of inflammation. J Immunol 2007;179:616-622.
148. Cowburn AS, White JF, Deighton J, et al. z-VAD-fmk augmentation of TNF α-stimulated neutrophil apoptosis is compound specific and does not involve the generation of reactive oxygen species. Blood 2005;105:2970-2972.