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Abstract

Neutrophil apoptosis (programmed cell death) is now recognised to play a fundamental role in the physiological resolution of innate immune responses. Early work by Metchnikoff correlated the ingestion of microphages (neutrophils) by macrophages with the resolution of acute inflammation, but nearly 100 years elapsed before the key role of apoptosis in determining the lifespan of granulocytes and their clearance from sites of inflammation was described [1]. Further work showed that apoptosis leads to down-regulation of neutrophil pro-inflammatory functions [2] and this, together with evidence that macrophage clearance of apoptotic granulocytes was anti-inflammatory [3], suggested that apoptosis induction could be a powerful therapeutic strategy to “turn off” neutrophilic inflammation [2].

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References

  1. Savill JS, Henson PM, Haslett C (1989) Phagocytosis of aged human neutrophils by macrophages is mediated by a novel “charge-sensitive” recognition mechanism. J Clin Invest 84: 1518–1527

    PubMed  CAS  Google Scholar 

  2. Whyte MK, Meagher LC, MacDermot J, Haslett C (1993) Impairment of function in aging neutrophils is associated with apoptosis. J Immunol 150: 5124–5134

    PubMed  CAS  Google Scholar 

  3. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101: 890–898

    PubMed  CAS  Google Scholar 

  4. Erjefalt JS, Uller L, Malm-Erjefalt M, Persson CG (2004) Rapid and efficient clearance of airway tissue granulocytes through transepithelial migration. Thorax 59: 136–143

    PubMed  CAS  Google Scholar 

  5. Walsh GM, Sexton DW, Blaylock MG, Convery CM (1999) Resting and cytokine-stimulated human small airway epithelial cells recognize and engulf apoptotic eosinophils. Blood 94: 2827–2835

    PubMed  CAS  Google Scholar 

  6. Stern M, Meagher L, Savill J, Haslett C (1992) Apoptosis in human eosinophils. Programmed cell death in the eosinophil leads to phagocytosis by macrophages and is modulated by IL-5. J Immunol 148: 3543–3549

    PubMed  CAS  Google Scholar 

  7. Simon H-U, Yousefi S, Schranz C, Schapowal A, Bachert C, Blaser K (1997) Direct demonstration of delayed eosinophil apoptosis as a mechanism causing tissue eosinophilia. J Immunol 158: 3902–3908

    PubMed  CAS  Google Scholar 

  8. Farahi N, Cowburn AS, Rossi AG, Chilvers ER (2004) Eating their way out of trouble: Selective uptake of apoptotic eosinophils by bronchial epithelial cells. Clin Exp Allergy 34: 1503–1506

    PubMed  CAS  Google Scholar 

  9. 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: 2012–2020

    PubMed  CAS  Google Scholar 

  10. Lee A, Whyte MKB, Haslett C (1993) Prolongation of in vitro lifespan and functional longevity of neutrophils by inflammatory mediators acting through inhibition of apoptosis. J Leukoc Biol 54: 283–288

    PubMed  CAS  Google Scholar 

  11. Begley CG, Lopez AF, Nicola NA, Warren DJ, Sanderson CJ, Metcalf D (1986) Purified colony-stimulating factors enhance the survival of human neutrophils and eosinophils in vitro: A rapid and sensitive microassay of colony-stimulating factors. Blood 68: 162–166

    PubMed  CAS  Google Scholar 

  12. Lopez AF, Williamson DJ, Gamble JR, Begley CG, Harlan JM, Klebanoff SJ, Walterscorph A, Wong G, Clark SC, Vadas MA (1986) Recombinant human granulocytemacrophage colony-stimulating factor stimulates in vitro mature human neutrophil and eosinophil function, surface receptor expression, and survival. J Clin Invest 78: 1220–1228

    PubMed  CAS  Google Scholar 

  13. Kooijman R, Coopens A, Hooghe-Peters E (2002) IGF-1 inhibits spontaneous apoptosis in human granulocytes. Endocrinology 143: 1206–1212

    PubMed  CAS  Google Scholar 

  14. Ross EA, Douglas MR, Wong SH, Ross EJ, Curnow SJ, Nash GB, Rainger E, Scheel-Toellner D, Lord JM, Salmon M et al (2006) Interaction between integrin alpha9beta1 and vascular cell adhesion molecule-1 (VCAM-1) inhibits neutrophil apoptosis. Blood 107: 1178–1183

    PubMed  CAS  Google Scholar 

  15. McGettrick HM, Lord JM, Wang KQ, Rainger GE, Buckley CD, Nash GB (2006) Chemokine-and adhesion-dependent survival of neutrophils after transmigration through cytokine-stimulated endothelium. J Leukoc Biol 79: 779–788

    PubMed  CAS  Google Scholar 

  16. Walmsley SR, Print C, Farahi N, Peyssonnaux C, Johnson RS, Cramer T, Sobolewski A, Condliffe AM, Cowburn AS, Johnson N, Chilvers ER (2005) Hypoxia-induced neutrophil survival is mediated by HIF-1α-dependent NF-κB activity. J Exp Med 201: 105–115

    PubMed  CAS  Google Scholar 

  17. Martinez D, Vermeulen M, Trevani A, Ceballos A, Sabatte J, Gamberale R, Alvarez ME, Salamone G, Tanos T, Coso OA et al (2006) Extracellular acidosis induces neutrophil activation by a mechanism dependent on activation of phosphatidylinositol 3-kinase/Akt and ERK pathways. J Immunol 176: 1163–1171

    PubMed  CAS  Google Scholar 

  18. Whyte MK, Savill J, Meagher LC, Lee A, Haslett C (1997) Coupling of neutrophil apoptosis to recognition by macrophages: coordinated acceleration by protein synthesis inhibitors. J Leukoc Biol 62: 195–202

    PubMed  CAS  Google Scholar 

  19. Schwedler SB, Filep JG, Galle J, Wanner C, Potempa LA (2006) C-reactive protein: A family of proteins to regulate cardiovascular function. Am J Kidney Dis 47: 212–222

    PubMed  CAS  Google Scholar 

  20. Ertel W, Keel M, Infanger M, Ungethum U, Steckholzer U, Trentz O (1998) Circulating mediators in serum of injured patients with septic complications inhibit neutrophil apoptosis through up-regulation of protein-tyrosine phosphorylation. J Trauma 44: 767–775

    PubMed  CAS  Google Scholar 

  21. Cendoroglo M, Sundaram S, Groves C, Ucci AA, Jaber BL, Pereira BJ (1997) Necrosis and apoptosis of polymorphonuclear cells exposed to peritoneal dialysis fluids in vitro. Kidney Int 52: 1626–34

    PubMed  CAS  Google Scholar 

  22. Buckley CD, Ross EA, McGettrick HM, Osborne CE, Haworth O, Schmutz C, Stone PC, Salmon M, Matharu NM, Vohra RK, Nash GB, Rainger GE (2006) Identification of a phenotypically and functionally distinct population of long-lived neutrophils in a model of reverse endothelial migration. J Leukoc Biol 79: 303–311

    PubMed  CAS  Google Scholar 

  23. Renshaw SA, Timmons SJ, Eaton V, Usher LR, Akil M, Bingle CD, Whyte MK (2000) Inflammatory neutrophils retain susceptibility to apoptosis mediated via the Fas death receptor. J Leukoc Biol 67: 662–668

    PubMed  CAS  Google Scholar 

  24. Renshaw SA, Parmar JS, Singleton V, Rowe SJ, Dockrell DH, Dower SK, Bingle CD, Chilvers ER, Whyte MKB (2003) Acceleration of human neutrophil apoptosis by TRAIL. J Immunol 170: 1027–1033

    PubMed  CAS  Google Scholar 

  25. Genestier AL, Mchallet MC, Prevost G, Bellot G, Chalabreysse L, Peyrol S, Thivolet F, Etienne J, Lina G, Vallette FM et al (2005) Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. J Clin Invest 115: 3117–3127

    PubMed  CAS  Google Scholar 

  26. Cowburn AS, White JF, Deighton J, Walmsley SR, Chilvers ER (2005) z-VAD-fmk augmentation of TNF alpha-stimulated neutrophil apoptosis is compound specific and does not involve the generation of reactive oxygen species. Blood 105: 2970–2972

    PubMed  CAS  Google Scholar 

  27. Watson RW, Redmond HP, Wang JH, Condron C, Bouchier-Hayes D (1996) Neutrophils undergo apoptosis following ingestion of Escherichia coli. J Immunol 156: 3986–3992

    PubMed  CAS  Google Scholar 

  28. DeLeo FR (2004) Modulation of phagocyte apoptosis by bacterial pathogens. Apoptosis 9: 399–413

    PubMed  CAS  Google Scholar 

  29. Kobayashi SD, Voyich JM, Buhl CL, Stahl RM, DeLeo FR (2002) Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: Cell fate is regulated at the level of gene expression. Proc Natl Acad Sci USA 99: 6901–6906

    PubMed  CAS  Google Scholar 

  30. Mayadas TN, Cullere X (2005) Neutrophil β2 integrins: Moderators of life or death decisions. Trends Immunol 26: 388–395

    PubMed  CAS  Google Scholar 

  31. Murray J, Barbara JA, Dunkley SA, Lopez A, van Ostade X, Condliffe AM, Dransfield I, Haslett C, Chilvers ER (1997) Regulation of neutrophil apoptosis by tumour necrosis factor-α: Requirement for TNFR-55 and TNFR-75 for induction of apoptosis in vitro. Blood 90: 2772–2783

    PubMed  CAS  Google Scholar 

  32. Kilpatrick LE, Sun S, Korchak HM (2004) Selective regulation by delta-PKC and PI3-kinase in the assembly of antiapoptotic TNFR-1 signaling complex in neutrophils. Am J Physiol Cell Physiol 287: C633–C642

    PubMed  CAS  Google Scholar 

  33. Iwai K, Miyawaki T, Takizawa T, Konno A, Ohta K, Yachie A, Seki H, Taniguchi N (1994) Differential expression of bcl-2 and susceptibility to anti-Fas-mediated cell death in peripheral blood lymphocytes, monocytes and neutrophils. Blood 84: 1201–1208

    PubMed  CAS  Google Scholar 

  34. Matsumoto K, Schleimer RP, Saito H, Iikura Y, Bochner BS (1995) Induction of apoptosis in human eosinophils by anti-Fas antibody treatment in vitro. Blood 86: 1437–1443

    PubMed  CAS  Google Scholar 

  35. Gardai S, Whitlock BB, Helgason C, Ambruso D, Fadok V, Bratton D, Henson PM (2002) Activation of SHIP by NADPH oxidase-stimulated Lyn leads to enhanced apoptosis in neutrophils. J Biol Chem 277: 5236–5246

    PubMed  CAS  Google Scholar 

  36. Cowburn AS, Sobolewski A, Reed BJ, Deighton J, Murray J, Walmsley SR, Cadwallader KA, Chilvers ER (2006) Aminopeptidase N (CD13) regulates tumour necrosis factor-α-induced apoptosis in human neutrophils. J Biol Chem 281: 12458–12467

    PubMed  CAS  Google Scholar 

  37. Matsuyama W, Yamamoto M, Higashimoto I, Oonakahara K, Watanabe M, Machida K, Yoshimura T, Eiraku N, Kawabata M, Osame M, Arimura K (2004) TNF-related apoptosis-inducing ligand is involved in neutropenia of systemic lupus erythematosus. Blood 104: 184–191

    PubMed  CAS  Google Scholar 

  38. Liles WC, Kiener PA, Ledbetter JA, Aruffo A, Klebanoff SJ (1996) Differential expression of Fas (CD95) and Fas ligand on normal human phagocytes: Implications for the regulation of apoptosis in neutrophils. J Exp Med 184: 429–440

    PubMed  CAS  Google Scholar 

  39. Brown SB, Savill J (1999) Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. J Immunol 162: 480–485

    PubMed  CAS  Google Scholar 

  40. Ottonello L, Tortolina G, Amelotti M, Dallegri F (1999) Soluble Fas ligand is chemotactic for human neutrophilic polymorphonuclear leukocytes. J Immunol 162: 3601–3606

    PubMed  CAS  Google Scholar 

  41. Green DR (2000) Apoptotic pathways: Paper wraps stone blunts scissors. Cell 102: 1–4

    PubMed  CAS  Google Scholar 

  42. Ashkenazi A, Dixit VM (1998) Death receptors: Signaling and modulation. Science 281: 1305–1308

    PubMed  CAS  Google Scholar 

  43. Susin SA, Daugas E, Ravagnan L, Samejima K, Zamzami N, Loeffler M, Costantini P, Ferri KF, Irinopoulou T, Prevost MC et al (2000) Two distinct pathways leading to nuclear apoptosis. J Exp Med 192: 571–580

    PubMed  CAS  Google Scholar 

  44. Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305: 626–629

    PubMed  CAS  Google Scholar 

  45. Roy S, Nicholson DW (2000) Cross-talk in cell death signaling. J Exp Med 192: F21–25

    PubMed  CAS  Google Scholar 

  46. Thornberry NA, Lazebnik Y (1998). Caspases: Enemies within. Science 281: 1312–1316

    PubMed  CAS  Google Scholar 

  47. Bainton DF, Ullyot JL, Farquhar MG (1971) The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. J Exp Med 134: 907–934

    PubMed  CAS  Google Scholar 

  48. Fossati G, Moulding DA, Spiller DG, Moots RJ, White MR, Edwards SW (2003) The mitochondrial network of human neutrophils: Role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis. J Immunol 170: 1964–1972

    PubMed  CAS  Google Scholar 

  49. Martin MC, Dransfield I, Haslett C, Rossi AG (2001) Cyclic AMP regulation of neutrophil apoptosis occurs via a novel protein kinase A-independent signaling pathway. J Biol Chem 276: 45041–45050

    PubMed  CAS  Google Scholar 

  50. Murphy BM, O’Neill AJ, Adrain C, Watson RW, Martin SJ (2003) The apoptosome pathway to caspase activation in primary human neutrophils exhibits dramatically reduced requirements for cytochrome C. J Exp Med 197: 625–632

    PubMed  CAS  Google Scholar 

  51. Maianski NA, Mul FP, van Buul JD, Roos D, Kuijpers TW (2002) Granulocyte colonystimulating factor inhibits the mitochondria-dependent activation of caspase-3 in neutrophils. Blood 99: 672–679

    PubMed  CAS  Google Scholar 

  52. Rowe SJ, Allen L, Ridger VC, Hellewell PG, Whyte MK (2002) Caspase-1-deficient mice have delayed neutrophil apoptosis and a prolonged inflammatory response to lipopolysaccharide-induced acute lung injury. J Immunol 169: 6401–6407

    PubMed  CAS  Google Scholar 

  53. Martinon F, Burns K, Tschopp J (2002) The inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10: 417–426

    PubMed  CAS  Google Scholar 

  54. Fadeel B, Ahlin A, Henter JI, Orrenius S, Hampton MB (1998) Involvement of caspases in neutrophil apoptosis: Regulation by reactive oxygen species. Blood 92: 4808–4818

    PubMed  CAS  Google Scholar 

  55. Goepel F, Weinmann P, Schymeinsky J, Walzog B (2004) Identification of caspase-10 in human neutrophils and its role in spontaneous apoptosis. J Leukoc Biol 75: 836–843

    PubMed  CAS  Google Scholar 

  56. Pryde JG, Walker A, Rossi AG, Hannah S, Haslett C (2000) Temperature-dependent arrest of neutrophil apoptosis. Failure of Bax insertion into mitochondria at 15°C prevents the release of cytochrome c. J Biol Chem 275: 33574–33584

    PubMed  CAS  Google Scholar 

  57. Yamashita K, Takahashi A, Kobayashi A, Hirata H, Mesner PW Jr, Kaufmann SH, Yonehara S, Yamamoto K, Uchiyama T, Sasada M (1999) Caspases mediate tumour necrosis factor alpha induced neutrophil apoptosis and downregulation of reactive oxygen production. Blood 93: 674–685

    PubMed  CAS  Google Scholar 

  58. Scheel-Toellner D, Wang K, Craddock R et al (2004) Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood 104: 2557–2564

    PubMed  CAS  Google Scholar 

  59. Daigle I, Simon HU (2001). Critical role for caspases 3 and 8 in neutrophil but not eosinophil apoptosis. Int Arch Allergy Immunol 126: 147–156

    PubMed  CAS  Google Scholar 

  60. Simon HU (2001) Regulation of eosinophil and neutrophil apoptosis-similarities and differences. Immunol Rev 179: 156–162

    PubMed  CAS  Google Scholar 

  61. Murray J, Walmsley SR, Mecklneburgh KI, Cowburn AS, White JF, Rossi AG, Chilvers ER (2003) Hypoxic regulation of neutrophil apoptosis: Role of reactive oxygen intermediates in constitutive and tumor necrosis factor α-induced cell death. Ann NY Acad Sci 1010: 417–425

    PubMed  CAS  Google Scholar 

  62. Kasahara Y, Iwai K, Yachie A, et al (1997) Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/APO-1)-mediated apoptosis of neutrophils. Blood 89: 1748–1753

    PubMed  CAS  Google Scholar 

  63. Gottlieb RA, Giesing HA, Zhu JY, Engler RL, Babior BM (1995) Cell acidification in apoptosis: Granulocyte colony-stimulating factor delays programmed cell death in neutrophils by up-regulating the vacuolar H(+)-ATPase. Proc Natl Acad Sci USA 92: 5965–5968

    PubMed  CAS  Google Scholar 

  64. Coakley RJ, Taggart C, McElvaney NG, O’Neill SJ (2002) Cytosolic pH and the inflammatory microenvironment modulate cell death in human neutrophils after phagocytosis. Blood 100: 3383–3391

    PubMed  CAS  Google Scholar 

  65. Brown SB, Bailey K, Savill J (1997) Actin is cleaved during constitutive apoptosis. Biochem J 323: 233–237

    PubMed  CAS  Google Scholar 

  66. Sanghavi DM, Thelen M, Thornberry NA, Casciola-Rosen L, Rosen A (1998) Caspase mediated proteolysis during apoptosis: Iinsights from apoptotic neutrophils. FEBS Lett 422: 179–184

    PubMed  CAS  Google Scholar 

  67. Pongracz J, Webb P, Wang K, Deacon E, Lunn OJ, Lord JM (1999) Spontaneous neutrophil apoptosis involves caspase 3-mediated activation of protein kinase C-delta. J Biol Chem 274: 37329–37334

    PubMed  CAS  Google Scholar 

  68. De Souza PM, Kankaanranta H, Michael A, Barnes PJ, Giembycz MA, Lindsay MA (2002) Caspase-catalyzed cleavage and activation of Mst1 correlates with eosinophil but not neutrophil apoptosis. Blood 99: 3432–3438

    PubMed  Google Scholar 

  69. Kobayashi S, Yamashita K, Takeoka T, Ohtsuki T, Suzuki Y, Takahashi R, Yamamoto K, Kaufmann SH, Uchiyama T, Sasada M, Takahashi A (2002) Calpain-mediated X-linked inhibitor of apoptosis degradation in neutrophil apoptosis and its impairment in chronic neutrophilic leukemia. J Biol Chem 277: 33968–33977

    PubMed  CAS  Google Scholar 

  70. Altznauer F, Conus S, Cavalli A, Folkers G, Simon HU (2004) Calpain-1 regulates Bax and subsequent Smac-dependent caspase-3 activation in neutrophil apoptosis. J Biol Chem 279: 5947–5957

    PubMed  CAS  Google Scholar 

  71. Ward C, Chilvers ER, Lawson MF, Pryde JG, Fujihara S, Farrow SN, Haslett C, Rossi AG (1999) NF-kappaB activation is a critical regulator of human granulocyte apoptosis in vitro. J Biol Chem 274: 4309–4318

    PubMed  CAS  Google Scholar 

  72. Cowburn AS, Cadwallader KA, Reed BJ, Farahi N, Chilvers ER (2002) Role of PI3-kinase-dependent Bad phosphorylation and altered transcription in cytokine-mediated neutrophil survival. Blood 100: 2607–2616

    PubMed  CAS  Google Scholar 

  73. Rossi AG, Cousin JM, Dransfield I, Lawson MF, Chilvers ER, Haslett C (1995) Agents that elevate cAMP inhibit human neutrophil apoptosis. Biochem Biophys Res Commun 217: 892–899

    PubMed  CAS  Google Scholar 

  74. Teixeira MM, Rossi AG, Giembycz MA, Hellewell PG (1996) Effects of agents which elevate cyclic AMP on guinea-pig eosinophil homotypic aggregation. Br J Pharmacol 118: 2099–2106

    PubMed  CAS  Google Scholar 

  75. Leuenroth SJ, Grutkoski PS, Ayala A, Simms HH (2000) Suppression of PMN apoptosis by hypoxia is dependent on Mcl-1 and MAPK activity. Surgery 128: 171–177

    PubMed  CAS  Google Scholar 

  76. Aleman M, Schierloh P, de la Barrera SS, Musella RM, Saab MA, Baldini M, Abbate E, Sasiain MC (2004) Mycobacterium tuberculosis triggers apoptosis in peripheral neu trophils involving Toll-like receptor 2 and p38 mitogen protein kinase in tuberculosis patients. Infect Immun 72: 5150–5158

    PubMed  CAS  Google Scholar 

  77. Walker BA, Rocchini C, Boone RH, Ip S, Jacobson MA (1997) Adenosine A2a receptor activation delays apoptosis in human neutrophils. J Immunol 158: 2926–2931

    PubMed  CAS  Google Scholar 

  78. Condliffe AM, Davidson K, Anderson KE, Ellson C, Crabbe T, Okkenhaug K, Vanhaesebroeck B, Turner M, Webb L, Wymann MP et al (2005) Priming of the neutrophil oxidase via temporal regulation of phosphoinositide 3-kinase activity. Blood 106: 1432–1440

    PubMed  CAS  Google Scholar 

  79. Cowburn AS, Deighton J, Walmsley SR, Chilvers ER (2004) Independent roles of phosphoinositide 3-kinase and NF-kappa-B in the regulation of apoptotic thresholds in neutrophils. Eur J Immunol 34: 1733–1743

    PubMed  CAS  Google Scholar 

  80. Micheau O, Tschopp J (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signalling complexes. Cell 114: 148–150

    Google Scholar 

  81. Moulding DA, Quayle JA, Hart CA, Edwards SW (1998) Mcl-1 expression in human neutrophils: Regulation by cytokines and correlation with cell survival. Blood 92: 2495–2502

    PubMed  CAS  Google Scholar 

  82. Moulding DA, Akgul C, Derouet M, White MR, Edwards SW (2001) BCL-2 family expression in human neutrophils during delayed and accelerated apoptosis. J Leukocyte Biol 70: 783–792

    PubMed  CAS  Google Scholar 

  83. Orlofsky A, Somogyi RD, Weiss LM, Prystowsky MB (1999) The murine antiapoptotic protein A1 is induced in inflammatory macrophages and constitutively expressed in neutrophils. J Immunol 163: 412–419

    PubMed  CAS  Google Scholar 

  84. Francois S, El Benna J, Dang PM, Pedruzzi E, Gougerot-Pocidalo MA, 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. J Immunol 174: 3633–3642

    PubMed  CAS  Google Scholar 

  85. Kobayashi SD, Voyich JM, Whitney AR, DeLeo FR (2005) Spontaneous neutrophil apoptosis and regulation of cell survival by granulocyte macrophage-colony stimulating factor. J Leukoc Biol 78: 1408–1418

    PubMed  CAS  Google Scholar 

  86. Chang HY, Yang X (2000) Proteases for cell suicide: Functions and regulation of caspases. Microbiol Mol Biol Rev 64: 821–846

    PubMed  CAS  Google Scholar 

  87. Hasegawa T, Suzuki K, Sakamoto C, Ohta K, Nishiki S, Hino M, Tatsumi N, Kitagawa S (2003) Expression of the inhibitor of apoptosis (IAP) family members in human neutrophils: up-regulation of cIAP2 by granulocyte colony-stimulating factor and overexpression of cIAP2 in chronic neutrophilic leukemia. Blood 101: 1164–1171

    PubMed  CAS  Google Scholar 

  88. Haslett C (1999) Granulocyte apoptosis and its role in the resolution and control of lung inflammation. Am J Respir Crit Care Med 160: S5–11

    PubMed  CAS  Google Scholar 

  89. Zychlinsky A, Sansonetti P (1997) Perspectives series: host/pathogen interactions. Apoptosis in bacterial pathogenesis. J Clin Invest 100: 493–495

    PubMed  CAS  Google Scholar 

  90. Usher LR, Lawson RA, Geary I, Taylor CJ, Bingle CD, Taylor GW, Whyte MK (2002) Induction of neutrophil apoptosis by the Pseudomonas aeruginosa exotoxin pyocyanin: A potential mechanism of persistent infection. J Immunol 168: 1861–1868

    PubMed  CAS  Google Scholar 

  91. Allen L, Dockrell DH, Pattery T, Lee DG, Cornelis P, Hellewell PG, Whyte MK (2005) Pyocyanin production by Pseudomonas aeruginosa induces neutrophil apoptosis and impairs neutrophil-mediated host defenses in vivo. J Immunol 174: 3643–3649

    PubMed  CAS  Google Scholar 

  92. Kobayashi SD, Braughton KR, Whitney AR, Voyich JM, Schwan TG, Musser JM, DeLeo FR (2003) Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proc Natl Acad Sci USA 100: 10948–10953

    PubMed  CAS  Google Scholar 

  93. Bylund J, Campsall PA, Ma RC, Conway BA, Speert DP (2005) Burkholderia cenocepacia induces neutrophil necrosis in chronic granulomatous disease. J Immunol 174: 3562–3569

    PubMed  CAS  Google Scholar 

  94. Hutchinson ML, Poxton IR, Govan JR (1998) Burkholderia cepacia produces a haemolysin that is capable of inducing apoptosis and degranulation of mammalian phagocytes. Infect Immun 66: 2033–2039

    Google Scholar 

  95. Russo TA, Davidson BA, Genagon SA, Warholic NM, Macdonald U, Pawlicki PD, Beanan JM, Olson R, Holm BA, Knight PR 3rd (2005) The E. coli virulence factor hemolysin induces neutrophil apoptosis and necrosis/lysis in vitro and necrosis/lysis and lung injury in a rat pneumonia model. Am J Physiol Lung Cell Mol Physiol 289: L207–L216

    PubMed  CAS  Google Scholar 

  96. Tai PC, Sun L, Spry CJ (1991) Effects of IL-5, granulocyte/macrophage colony-stimulating factor (GM-CSF) and IL-3 on the survival of human blood eosinophils in vitro. Clin Exp Immunol 85: 312–316

    PubMed  CAS  Google Scholar 

  97. Rothenberg ME, Pomerantz JL, Owen W Jr, Avraham S, Soberman RJ, Austen KF, Stevens RL (1988) Characterization of a human eosinophil proteoglycan, and augmentation of its biosynthesis and size by interleukin 3, interleukin 5, and granulocyte/macrophage colony stimulating factor. J Biol Chem 263: 13901–13908

    PubMed  CAS  Google Scholar 

  98. Yamaguchi Y, Suda T, Ohta S, Tominaga K, Minura Y, Kasahara T (1991) Analysis of the survival of mature human eosinophils: interleukin-5 prevents apoptosis in mature human eosinophils. Blood 78: 2542–2547

    PubMed  CAS  Google Scholar 

  99. Gounni AS (2000) Interleukin-9 enhances interleukin-5 receptor expression, differentiation, and survival of human eosinophils. Blood 96: 2163–2171

    PubMed  CAS  Google Scholar 

  100. Luttmann W, Knoechel B, Foerster M, Matthys H, Virchow J Jr, Kroegel C (1996) Activation of human eosinophils by IL-13. Induction of CD69 surface antigen, its relationship to messenger RNA expression, and promotion of cellular viability. J Immunol 157: 1678–1683

    PubMed  CAS  Google Scholar 

  101. Tsukahara K, Nakao A, Hiraguri M, Miike S, Mamura M, Saito Y, Iwamoto I (1999) Tumor necrosis factor-alpha mediates antiapoptotic signals partially via p38 MAP kinase activation in human eosinophils. Int Arch Allergy Immunol 1: 54–59

    Google Scholar 

  102. Conus S, Bruno A, Simon HU (2005) Leptin is an eosinophil survival factor. J Allergy Clin Immunol 116: 1228–1234

    PubMed  CAS  Google Scholar 

  103. Takanaski S, Nonaka R, Xing Z, O’Byrne P, Dolovich J, Jordana M (1994) Interleukin 10 inhibits lipopolysaccharide-induced survival and cytokine production by human peripheral blood eosinophils. J Exp Med 180: 711–715

    PubMed  CAS  Google Scholar 

  104. Ochiai K, Kagami M, Matsumura R, Tomioka H (1997) IL-5 but not interferon-gamma (IFN-gamma) inhibits eosinophil apoptosis by up-regulation of bcl-2 expression. Clin Exp Immunol 107: 198–204

    PubMed  CAS  Google Scholar 

  105. Chihara J, Kakazu T, Higashimoto I, Saito N, Honda K, Sannohe S, Kayaba H, Urayama O (2000) Signaling through the beta2 integrin prolongs eosinophil survival. J Allergy Clin Immunol 106: S99–S103

    PubMed  CAS  Google Scholar 

  106. Tourkin A, Anderson T, LeRoy EC, Hoffman S (1993) Eosinophil adhesion and maturation is modulated by laminin. Cell Adhes Commun 1: 161–176

    PubMed  CAS  Google Scholar 

  107. Anwar AR, Moqbel R, Walsh GM, Kay AB, Wardlaw AJ (1993) Adhesion to fibronectin prolongs eosinophil survival. J Exp Med 177: 839–843

    PubMed  CAS  Google Scholar 

  108. Matsumoto R, Hirashima M, Kita H, Gleich GJ (2002) Biological activities of ecalectin: A novel eosinophil-activating factor. J Immunol 168: 1961–1967

    PubMed  CAS  Google Scholar 

  109. Peacock CD, Misso NL, Watkins DN, Thompson PJ (1999) PGE 2 and dibutyryl cyclic adenosine monophosphate prolong eosinophil survival in vitro. J Allergy Clin Immunol 104: 153–162

    PubMed  CAS  Google Scholar 

  110. Lee E, Robertson T, Smith J, Kilfeather S (2001) Leukotriene receptor antagonists and synthesis inhibitors reverse survival in eosinophils of asthmatic individuals. Am J Respir Crit Care Med 161: 1881–1886

    Google Scholar 

  111. Yasui K, Agematsu K, Shinozaki K, Hokibara S, Nagumo H, Yamada S, Kobayashi N, Komiyama A (2000) Effects of theophylline on human eosinophil functions: Comparative study with neutrophil functions. J Leukoc Biol 68: 194–200

    PubMed  CAS  Google Scholar 

  112. Kim JT, Gleich GJ, Kita H (1997) Roles of CD molecules in survival and activation of human eosinophils. J Immunol 159: 926–933

    PubMed  CAS  Google Scholar 

  113. Beauvais F, Joly F (1999) Effects of nitric oxide on the eosinophil survival in vitro. A role for nitrosyl-heme. FEBS Lett 443: 37–40

    PubMed  CAS  Google Scholar 

  114. Tsuyuki S, Bertrand C, Erard F, Trifilieff A, Tsuyuki J, Wesp M, Anderson G, Coyle AJ (1995) Activation of the Fas receptor on lung eosinophils leads to apoptosis and the resolution of eosinophilic inflammation of the airways. J Clin Invest 96: 2924–2931

    PubMed  CAS  Google Scholar 

  115. Yasui K, Hu B, Nakazawa T, Agematsu K, Komiyama A (1997) Theophylline accelerates human granulocyte apoptosis not via phosphodiesterase inhibition. J Clin Invest 100: 1677–1684

    PubMed  CAS  Google Scholar 

  116. Alam R, Forsythe P, Stafford S, Fukuda Y (1994) Transforming growth factor beta abrogates the effects of hematopoietins on eosinophils and induces their apoptosis. J Exp Med 179: 1041–1045

    PubMed  CAS  Google Scholar 

  117. Wedi B, Raap U, Lewrick H, Kapp A (1998) IL-4-induced apoptosis in peripheral blood eosinophils. J Allergy Clin Immunol 102: 1013–1020

    PubMed  CAS  Google Scholar 

  118. Meagher LC, Cousin JM, Seckl JR, Haslett C (1996) Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J Immunol 156: 4422–4428

    PubMed  CAS  Google Scholar 

  119. Okada S, Hagan JB, Kato M, Bankers-Fulbright JL, Hunt LW, Gleich GJ, Kita H (1998) Lidocaine and its analogues inhibit IL-5-mediated survival and activation of human eosinophils. J Immunol 160: 4010–4017

    PubMed  CAS  Google Scholar 

  120. Hossain M, Okubo Y, Sekiguchi M (1994) Eosinophil viability-enhancing activity in mite-sensitive bronchial asthma. Intern Med 33: 529–535

    PubMed  CAS  Google Scholar 

  121. Bankers-Fulbright JL, Kephart GM, Loegering DA, Bradford AL, Okada S, Kita H, Gleich GJ (1998) Sulfonylureas inhibit cytokine-induced eosinophil survival and activation. J Immunol 160: 5546–5553

    PubMed  CAS  Google Scholar 

  122. Kankaanranta H, Ilmarinen P, Zhang X, Nissinen E, Moilanen E (2006) Anti-eosinophilic activity of orazipone. Mol Pharmacol 69: 1861–1870

    PubMed  CAS  Google Scholar 

  123. Nutku E, Hudson SA, Bochner BS (2005) Mechanism of Siglec-8-induced human eosinophil apoptosis: Role of caspases and mitochondrial injury. Biochem Biophys Res Commun 336: 918–924

    PubMed  CAS  Google Scholar 

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Whyte, M.K.B., Haslett, C., Chilvers, E.R. (2008). Granulocyte apoptosis. In: Rossi, A.G., Sawatzky, D.A. (eds) The Resolution of Inflammation. Progress in Inflammation Research. Birkhäuser Basel. https://doi.org/10.1007/978-3-7643-7506-5_2

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