[en] Regulation of the neutrophil life span by apoptosis provides a fine balance between their function as effector cells of host defence and a safe turnover of these potentially harmful cells. Apoptosis is thus necessary to keep cellular homeostasis under physiologic conditions. Alterations of neutrophil apoptosis are associated with diseases such as bacterial and autoimmune inflammatory diseases where neutrophil apoptosis is delayed. Excessive production of survival factors is often observed in such inflammatory responses and neutrophil survival can be increased several fold. Cytokines withdrawal, as it occurs in the resolution phase of inflammation, leads to the induction of neutrophil apoptosis. Recent studies have shown the involvement of members of the Bcl-2 protein family and caspases in the regulation and execution of neutrophil apoptosis. Cell surface receptors and protein kinases also play critical roles in transducing the signals that result in neutrophil apoptosis or extended survival. The aim of this review is to summarise the principal molecular mechanisms and components of neutrophil apoptosis [fr] La régulation de la vie des neutrophiles par le mécanisme de mort programmée cellulaire qu’est l’apoptose procure un équilibre judicieux entre leur fonction de cellules effectrices dans la défense de l’organisme et le renouvellement sécurisé de ces cellules potentiellement dangereuses. L’apoptose constitue donc un processus nécessaire pour le maintien de l’homéostasie cellulaire dans des conditions physiologiques. Des altérations dans les mécanismes d’apoptose neutrophilique sont associées à certaines maladies telles que des maladies inflammatoires bactériennes ou auto-immunes. La production excessive de facteurs de survie est souvent associée à de telles réponses inflammatoires et la survie du neutrophile peut y être multipliée plusieurs fois. La diminution de la concentration en cytokines, comme elle survient lors de la phase de résolution de l’inflammation, conduit par contre à l’induction de l’apoptose neutrophilique. Des études ont montré l’implication de membres de la famille Bcl-2 et de caspases dans la régulation et l’exécution de l’apoptose neutrophilique. Des récepteurs de surface cellulaire et des protéines kinases jouent également un rôle critique dans la transduction des signaux qui mènent à l’apoptose du neutrophile ou à une augmentation de sa survie. Le but de cette revue est de résumer les composants et les mécanismes moléculaires principaux de l’apoptose neutrophilique
Disciplines :
Veterinary medicine & animal health Biochemistry, biophysics & molecular biology
Author, co-author :
Fievez, Laurence ; Université de Liège - ULiège > Département de sciences fonctionnelles > GIGA-R : Biochimie et biologie moléculaire
Seumois, G.; Université de Liège - ULiège > Département de sciences fonctionnelles > Physiologie - Doyen de la Faculté de Médecine vétérinaire
Lekeux, Pierre ; Université de Liège - ULiège > Département de sciences fonctionnelles > GIGA-R : Biochimie et biologie moléculaire
Bureau, Fabrice ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF) > Biochimie et biologie moléculaire ; Université de Liège - ULiège > GIGA > GIGA Inflammation, Infection & Immunity
AL-SHAMI A., MAHANNA W., NACCACHE P.H. Granulocyte-macrophage colony-stimulating factor-activated signaling pathways in human neutrophils: selective activation of Jak2, Stat3, and Stat5b. J. Biol. Chem., 1998, 273, 1058-1063.
ALTZNAUER F., CONUS S., CAVALLI A., FOLKERS G., SIMON H.U. Calpain-1 regulates Bax and subsequent Smac-dependent caspase-3 activation in neutrophil apoptosis. J. Biol. Chem., 2004, 279, 5947-5957.
AMAN M.J., MIGONE T.S., SASAKI A., ASCHERMAN D.P., ZHU M., SOLDAINI E., IMADA K., MIYAJIMA A., YOSHIMURA A., LEONARD W.J. CIS associates with the interleukin-2 receptor beta chain and inhibits interleukin-2-dependent signaling. J. Biol. Chem., 1999, 274, 30266-30272.
AOSHIBA K., YASUI S., HAYASHI M., TAMAOKI J., NAGAI A. Role of p38-mitogen-activated protein kinase in spontaneous apoptosis of human neutrophils. J. Immunol., 1999, 162, 1692-1700.
ASHKENAZI A., DIXIT V.M. Death receptors: signaling and modulation. Science, 1998, 281, 1305-1308.
BAINTON D.F., ULLYOT J.L., FARQUHAR M.G. The development of neutrophilic polymorphonuclear leukocytes in human bone marrow : origin and content of azurophil and specific granules. J. Exp. Med., 1971, 134, 907-934.
BIFFL W.L., MOORE E.E., MOORE F.A., BARNETT C.C. JR. Interleukin-6 suppression of neutrophil apoptosis is neutrophil concentration dependent. J. Leukoc. Biol., 1995, 58, 582-584.
BLUME-JENSEN P., JANKNECHT R., HUNTER T. The kit receptor promotes cell survival via activation of PI 3-kinase and subsequent Akt-mediated phosphorylation of Bad on Ser136. Curr. Biol., 1998, 8, 779-782.
BORNER C., OLIVIER R., MARTINOU I., MATTMANN C., TSCHOPP J., MARTINOU J.C. Dissection of functional domains in Bcl-2 alpha by site-directed mutagenesis. Biochem. Cell. Biol., 1994, 72, 463-469.
BRACH M.A., DEVOS S., GRUSS H..J., HERRMANN F. Prolongation of survival of human polymorphonuclear neutrophils by granulocyte-macrophage colony-stimulating factor is caused by inhibition of programmed cell death. Blood, 1992, 80, 2920-2924.
BRIZZI M.F., ARONICA M.G., ROSSO A., BAGNARA G.P., YARDEN Y., PEGORARO L. Granulocyte-macrophage colony-stimulating factor stimulates JAK2 signaling pathway and rapidly activates p93fes, STAT1 p91, and STAT3 p92 in polymorphonuclear leukocytes. J. Biol. Chem., 1996, 271, 3562-3567.
BROWN S.B., SAVILL J. Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. J. Immunol., 1999, 162, 480-485.
CANTLEY L.C. The phosphoinositide 3-kinase pathway. Science, 2002, 296, 1655-1657.
CARDONE M.H., ROY N., STENNICKE H.R., SALVESEN G.S., FRANKE T.F., STANBRIDGE E., FRISCH S., REED J.C. Regulation of cell death protease caspase-9 by phosphorylation. Science, 1998, 282, 1318-1321.
CASTRO-ALCARAZ S., MISKOLCI V., KALASAPUDI B., DAVIDSON D., VANCUROVA I. NF-kappa B regulation in human neutrophils by nuclear I kappa B alpha: correlation to apoptosis. J. Immunol., 2002, 169, 3947-3953.
CHANG L., KARIN M. Mammalian MAP kinase signalling cascades. Nature, 2001, 410, 37-40.
CHILVERS E.R., ROSSI A.G., MURRAY J., HASLETT C. Regulation of granulocyte apoptosis and implications for antiinflammatory therapy. Thorax, 1998, 53, 533-534.
CHUANG P.I., YEE E., KARSAN A., WINN R.K., HARLAN J.M. A1 is a constitutive and inducible Bcl-2 homologue in mature human neutrophils. Biochem. Biophys. Res. Commun., 1998, 249, 361-365.
CLARK J.M., VAUGHAN D.W., AIKEN B.W., KAGAN H.M. Elastase-like enzymes in human neutrophils localized by ultrastructural cytochemistry. J. Cell. Biol., 1980, 84, 102-119.
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.
COTTER T.G., LENNON S.V., GLYNN J.M., GREEN D.R. Microfilament-disrupting agents prevent the formation of apoptotic bodies in tumor cells undergoing apoptosis. Cancer Res., 1992, 52, 997-1005.
COWBURN A.S., CADWALLADER K.A., REED B.J., FARAHI N., CHILVERS E.R. Role of PI3-kinase-dependent Bad phosphorylation and altered transcription in cytokine-mediated neutrophil survival. Blood, 2002, 100, 2607-2616.
COX G. Glucocorticoid treatment inhibits apoptosis in human neutrophils: separation of survival and activation outcomes. J. Immunol., 1995, 154, 4719-4725.
DAIGLE I., SIMON H.U. Critical role for caspase 3 and 8 in neutrophil but not eosinophil apoptosis. Int. Arch. Allergy Immunol., 2001, 126, 147-156.
DAIGLE I., YOUSEFI S., COLONNA M., GREEN D.R., SIMON H.U. Death receptors bind SHP-1 and block cytokine-induced anti-apoptotic signaling in neutrophils. Nat. Med., 2002, 8, 61-67.
DEL PESO L., GONZALEZ-GARCIA M., PAGE C., HERRERA R., NUNEZ G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science, 1997, 278, 687-689.
DIBBERT B., WEBER M., NIKOLAIZIK W.H., VOGT P., SCHONI M.H., BLASER K., SIMON H.U. Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. Proc. Natl. Acad. Sci. U.S.A., 1999, 96, 13330-13335.
DOWNWARD J. How BAD phosphorylation is good for survival. Nat. Cell. Biol., 1999, 1, E33-E35.
DRANSFIELD I., BUCKLE A.M., SAVILL J.S., MCDOWALL A., HASLETT C., HOGG N. Neutrophil apoptosis is associated with a reduction in CD16 (Fc gamma RIII) expression. J. Immunol., 1994, 153, 1254-1263.
EPLING-BURNETTE P.K., ZHONG B., BAI F., JIANG K., BAILEY R.D., GARCIA R., JOVE R., DJEU J.Y., LOUGHRAN T.P. JR, WEI S. Cooperative regulation of Mcl-1 by Janus kinase/stat and phosphatidylinositol 3-kinase contribute to granulocyte-macrophage colony-stimulating factor-delayed apoptosis in human neutrophils. J. Immunol., 2001, 166, 7486-7495.
FARROW S.N., BROWN R. New members of the Bcl-2 family and their protein partners. Curr. Opin. Genet. Dev., 1996, 6, 45-49.
FECHO K.L., COHEN P.L. Fas ligand (gld) and Fas (lpr) deficient mice do not show alterations in the extravasation of apoptosis of inflammatory neutrophils. J. Leukoc. Biol., 1998, 64, 373-383.
FRASCH S.C., NICK J.A., FADOK V.A., BRATTON D.L., WORTHEN G.S., HENSON P.M. p38 mitogen-activated protein kinase-dependent and -independent intracellular signal transduction pathways leading to apoptosis in human neutrophils. J. Biol. Chem., 1998, 273, 8389-8397.
GAO G., DOU Q.P. N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome C release and apoptotic cell death. J. Cell. Biochem., 2000, 80, 53-72.
GASMI L., MCLENNAN A.G., EDWARDS S.W. The diadenosine polyphosphates Ap3A and Ap4A and adenosine triphosphate interect with granulocyte-macrophage colony-stimulating factor to delay neutrophil apoptosis: implications for neutrophil-platelet interactions during inflammation. Blood, 1996, 87, 3442-3449.
GIRARD D., PAQUET M.E., PAQUIN R., BEAULIEU A.D. Differential effects of interleukin-15 (IL-15) and IL-2 on human neutrophils: modulation of phagocytosis, cytoskeleton rearrangement, gene expression, and apoptosis by IL-15. Blood, 1996, 88, 3176-3184.
GIRARD D., PAQUIN R., BEAULIEU A.D. Responsiveness of human neutrophils to interleukin-4: induction of cytoskeletal rearrangements, de novo protein synthesis and delay of apoptosis. Biochem. J., 1997, 325, 147-153.
GREEN D.R., FERGUSON T.A. The role of Fas ligand in immune privilege. Nat. Rev. Mol. Cell. Biol., 2001, 2, 917-924.
HAMASAKI A., SENDO F., NAKAYAMA K., ISHIDA N., NEGISHI I., NAKAYAMA K., HATAKEYAMA S. Accelerated neutrophil apoptosis in mice lacking A1-a, a subtype of the bcl-2-related A1 gene. J. Exp. Med., 1998, 188, 1985-1992.
HAMPTON M.B., VISSERS M.C., KEENAN J.I., WINTERBOURN C.C. Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils : possible impairment in chronic granulomatous disease. J. Leukoc. Biol., 2002, 71, 775-781.
HANNAH S., NADRA I., DRANSFIELD I., PRYDE J.G., ROSSI A.G., HASLETT C. Constitutive neutrophil apoptosis in culture is modulated by cell density independently of b2 integrin-mediated adhesion. FEBS Lett., 1998, 421, 141-146.
HARADA H., BECKNELL B., WILM M., MANN M., HUANG L.J., TAYLOR S.S., SCOTT J.D., KORSMEYER S.J. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol. Cell., 1999, 3, 413-422.
HASEGAWA T., SUZUKI K., SAKAMOTO C., OHTA K., NISHIKI S., HINO M., TATSUMI N., KITAGAWA S. 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, 2003, 101, 1164-1171.
HASLETT C., SAVILL J.S., WHYTE M.K., STERN M., DRANSFIELD I., MEAGHER L.C. Granulocyte apoptosis and the control of inflammation. Philos. Trans. R. Soc. Lond., B., Biol. Sci., 1994, 345, 327-333.
HOMBURG C.H., DE HAAS M., VON DEM BORNE A.E., VERHOEVEN A.J., REUTELINGSPERGER C.P., ROOS D. Human neutrophils lose their surface Fc gamma RIII and acquire Annexin V binding sites during apoptosis in vitro. Blood, 1995, 85, 532-540.
IWAI K., MIYAWAKI T., TAKIZAWA T., KONNO A., OHTA K., YACHIE A., SEKI H., TANIGUCHI N. Differential expression of bcl-2 and susceptibility to anti-Fas-mediated cell death in peripheral blood lymphocytes, monocytes, and neutrophils. Blood, 1994, 84, 1201-1208.
KASAHARA Y., IWAI K., YACHIE A., OHTA K., KONNO A., SEKI H., MIYAWAKI T., TANIGUCHI N. Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/APO-1)-mediated apoptosis of neutrophils. Blood, 1997, 89, 1748-1753.
KEEL M., UNGETHUM U., STECKHOLZER U., NIEDERER E., HARTUNG T., TRENTZ O., ERTEL W. Interleukin-10 counterregulates proinflammatory cytokine-induced inhibition of neutrophil apoptosis during severe sepsis. Blood, 1997, 90, 3356-3363.
KHWAJA A., TATTON L. Caspase-mediated proteolysis and activation of protein kinase C delta plays a central role in neutrophil apoptosis. Blood, 1999, 94, 291-301.
KLEBANOFF S.J., OLSZOWSKI S., VAN VOORHIS W.C., LEDBETTER J.A., WALTERSDORPH A.M., SCHLECHTE K.G. Effects of gamma-interferon on human neutrophils: protection from deterioration on storage. Blood, 1992, 80, 225-234.
KLEIN J.B., RANE M.J., SCHERZER J.A., COXON P.Y., KETTRITZ R., MATHIESEN J.M., BURIDI A., MCLEISH K.R. Granulocyte-macrophage colony-stimulating factor delays neutrophil constitutive apoptosis through phosphoinositide 3-kinase and extracellular signal-regulated kinase pathways. J. Immunol., 2000, 164, 4286-4291.
KNEPPER-NICOLAI B., SAVILL J., BROWN S.B. Constitutive apoptosis in human neutrophils requires synergy between calpains and the proteosome downstream of caspases. J. Biol. Chem., 1998, 273, 30530-30536.
KON-KOZLOWSKI M., PANI G., PAWSON T., SIMINOVITCH K.A. The tyrosine phosphatase PTP1C associates with Vav, Grb2, and mSos1 in hematopoietic cells. J. Biol. Chem., 1996, 271, 3856-3862.
KOVANEN P.E., LEONARD W.J. Inhibitors keep cytokines in check. Curr. Biol., 1999, 9, R899-R902.
KREBS D.L., HILTON D.J. SOCS: physiological suppressors of cytokine signaling. J. Cell. Sci., 2000, 113, 2813-2819.
LAGASSE E., WEISSMAN I.L. Bcl-2 inhibits apoptosis of neutrophils but not their engulfment by macrophages. J. Exp. Med., 1994, 179, 1047-1052.
LEE A., WHYTE M.K.B., HASLETT C. Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators. J. Leukoc. Biol., 1993, 54, 283-289.
LEE E., LINDO T., JACKSON N., MENG-CHOONG L., REYNOLDS P., HILL A., HASWELL M., JACKSON S., KILFEATHER S. Reversal of human neutrophil survival by leukotriene B(4) receptor blockade and 5-lipoxygenase and 5-lipoxygenase activating protein inhibitors. Am. J. Respir. Crit. Care Med., 1999, 160, 2079-2085.
LI H., ZHU H., XU C.J., YUAN J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell, 1998, 94, 491-501.
LILES W.C., KLEBANOFF S.J. Regulation of apoptosis in neutrophils-Fas track to death. J. Immunol., 1995, 155, 3289-3291.
LILES W.C., KIENER P.A., LEDBETTER J.A., ARUFFO A., KLEBANOFF S.J. 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.
LINDSTEN T., ROSS A.J., KING A., ZONG W.X., RATHMELL J.C., SHIELS H.A., ULRICH E., WAYMIRE K.G., MAHAR P., FRAUWIRTH K., CHEN Y., WEI M., ENG V.M., ADELMAN D.M., SIMON M.C., MA A., GOLDEN J.A., EVAN G., KORSMEYER S.J., MACGREGOR G.R., THOMPSON C.B. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell., 2000, 6, 1389-1399.
LORENZ U., RAVICHANDRAN K.S., BURAKOFF S.J., NEEL B.G. Lack of SHPTP1 results in src-family kinase hyperactivation and thymocyte hyperresponsiveness. Proc. Natl. Acad. Sci. U.S.A., 1996, 93, 9624-9629.
MAIANSKI N.A., MUL F.P.J., VAN BUUL J.D., KUIJPERS T.W. Granulocyte colony-stimulating factor inhibits the mitochondria-dependent activation of caspase-3 in neutrophils. Blood, 2002, 99, 672-679.
MARINO M.W., DUNN A., GRAIL D., INGLESE M., NOGUCHI Y., RICHARDS E., JUNGBLUTH A., WADA H., MOORE M., WILLIAMSON B., BASU S., OLD L.J. Characterization of tumor necrosis factor-deficient mice. Proc. Natl. Acad. Sci. U.S.A., 1997, 94, 8093-8098.
MATSUMOTO A., SEKI Y., KUBO M., OHTSUKA S., SUZUKI A., HAYASHI I., TSUJI K., NAKAHATA T., OKABE M., YAMADA S., YOSHIMURA A. Suppression of STAT5 functions in liver, mammary glands, and T cells in cytokine-inducible SH2-containing protein 1 transgenic mice. Mol. Cell. Biol., 1999, 19, 6396-6407.
MEAGHER L.C., COUSIN J.M., SECKL J.R., HASLETT C. Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J. Immunol., 1996, 156, 4422-4428.
MOULDING D.A., QUAYLE J.A., HART C.A., EDWARDS S.W. Mcl-1 expression in human neutrophils : regulation by cytokines and correlation with cell survival. Blood, 1998, 92, 2495-2502.
MOULDING D.A., AKGUL C., DEROUET M., WHITE M.R.H., EDWARDS S.W. Bcl-2 family expression in human neutrophils during delayed and accelerated apoptosis. J. Leukoc. Biol., 2001, 70, 783-792.
MURRAY J., BARBARA J.A., DUNKLEY S.A., LOPEZ A.F., VAN OSTADE X., CONDLIFFE A.M., DRANSFIELD I., HASLETT C., CHILVERS E.R. 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.
OTTONELLO L., FRUMENTO G., ARDUINO N., BERTOLOTTO M., DAPINO P., MANCINI M., DALLEGRI F. Differential regulation of spontaneous and immune complex-induced neutrophil apoptosis by proinflammatory cytokines. Role of oxidants, Bax and caspase-3. J. Leukoc. Biol., 2002, 72, 125-132.
PARVATHENANI L.K., BUESCHER E.S., CHACON-CRUZ E., BEEBE S.J. Type I cAMP-dependent protein kinase delays apoptosis in human neutrophils at a site upstream of caspase-3. J. Biol. Chem., 1998, 273, 6736-6743.
PERICLE F., LIU J.H., DIAZ J.I., BLANCHARD D.K., WEI S., FORNI G., DJEU J.Y. Interleukin-2 prevention of apoptosis in human neutrophils. Eur. J. Immunol., 1994, 24, 440-444.
PONGRACZ J., WEBB P., WANG K.Q., DEACON E., LUNN O.J., LORD J.M. Spontaneous neutrophil apoptosis involves caspase 3 mediated activation of PKC-d. J. Biol. Chem., 1999, 274, 37329-37334.
REED J.C. Double identity for proteins of the Bcl-2 family. Nature, 1997, 387, 773-776.
ROSSI A.G., COUSIN J.M., DRANSFIELD I., LAWSON M.F., CHILVERS E.R., HASLETT C. Agents that elevate cAMP inhibit human neutrophil apoptosis. Biochem. Biophys. Res. Commun., 1995, 217, 892-899.
ROWE S.J., ALLEN L., RIDGER V.C., HELLEWELL P.G., WHYTE M.K.B. Caspase-1-deficient mice have delayed neutrophil apoptosis and a prolonged inflammatory response to lipopolysaccharide-induced acute lung injury. J. Immunol., 2002, 169, 6401-6407.
SABROE I., JONES E.C., USHER L.R., WHYTE M.K., DOWER S.K. 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.
SALAMONE G., GIORDANO M., TREVANI A.S., GAMBERALE R., VERMEULEN M., SCHETTINNI J., GEFFNER J.R. Promotion of neutrophil apoptosis by TNF-alpha. J. Immunol., 2001, 166, 3476-3483.
SALVESEN G.S., DUCKETT C.S. IAP proteins : blocking the road to death's door. Mol. Cell. Biol., 2002, 3, 401-410.
SAVILL J.S., WYLLIE A.H., HENSON J.E., WALPORT M.J., HENSON P.M., HASLETT C. 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.
SAVILL J., FADOK V., HENSON P., HASLETT C. Phagocyte recognition of cells undergoing apoptosis. Immunol. Today, 1993, 14, 131-136.
SAVILL J., HASLETT C. Granulocyte clearance by apoptosis in the resolution of inflammation. Semin. Cell. Biol., 1995, 6, 385-393.
SAVILL J., DRANSFIELD I., GREGORY C., HASLETT C. A blast from the past : clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol., 2002, 2, 965-975.
SIMINOVITCH K.A., NEEL B.G. Regulation of B cell signal transduction by SH2-containing protein-tyrosine phosphatases. Semin. Immunol., 1998, 10, 329-347.
SIMON H.U. Novel therapeutic strategies via the apoptosis pathways to resolve chronic eosinophilic inflammation. Cell Death Differ., 1996, 3, 349-356.
SKERRETT S.J. Host defenses against respiratory infection. Med. Clin. North Am., 1994, 78, 941-966.
SONG K., CHEN Y., GOKE R., WILMEN A., SEIDEL C., GOKE A., HILLIARD B., CHEN Y. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is an inhibitor of autoimmune inflammation and cell cycle progression. J. Exp. Med., 2000, 191, 1095-1104.
SQUIER M.K.T., COHEN J.J. Calpain and cell death. Cell Death Differ., 1996, 3, 275-283.
SQUIER M.K.T., SEHNERT A.J., SELLINS K.S., MALKINSON A.M., TAKANO E., COHEN J.J. Calpain and calpastatin regulate neutrophil apoptosis. J. Cell. Physiol., 1999, 178, 311-319.
STRINGER R.E., HART C.A., EDWARDS S.W. Sodium butyrate delays neutrophil apoptosis: role of protein biosynthesis in neutrophil survival. Br. J. Haematol., 1996, 92, 169-175.
TAKEDA Y., WATANABE H., YONEHARA S., YAMASHITA T., SAITO S., SENDO F. Rapid acceleration of neutrophil apoptosis by tumor necrosis factor-alpha. Int. Immunol., 1993, 5, 691-694.
TIDOW N., KASPER B., WELTE K. SH2-containing protein tyrosine phosphatases SHP-1 and SHP-2 are dramatically increased at the protein level in neutrophils from patients with severe congenital neutropenia (Kostmann's syndrome). Exp. Hematol., 1999, 27, 1038-1045.
VAN DEN BERG J.M., WEYER S., WEENING J.J., ROOS D., KUIJPERS T.W. Divergent effects of tumor necrosis factor-a on apoptosis of human neutrophils. J. Leukoc. Biol., 2001, 69, 467-473.
VILLUNGER A., O'REILLY L.A., HOLLER N., ADAMS J., STRASSER A. 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, 647-657.
WALKER N.P., TALANIAN R.V., BRADY K.D., DANG L.C., BUMP N.J., FERENZ C.R., FRANKLIN S., GHAYUR T., HACKETT M.C., HAMMILL L.D., HERZOG L., HUGUNIN M., HOUY W., MANKOVICH J.A., MCGUINESS L., ORLEWICZ E., PASKIND M., PRATT C.A., REIS P., SUMMANI A., TERRANOVA M., WELCH J.P., XIONG L., MÖLLER A., TRACEY D.E., KAMEN R., WONG W.W. Crystal structure of the cysteine protease interleukin-1 beta-converting enzyme: a (p20/p10)2 homodimer. Cell, 1994, 78, 343-352.
WALKER R.I., WILLEMZE R. Neutrophil kinetics and the regulation of granulopoiesis. Rev. Infect. Dis., 1980, 2, 282-292.
WARD I., DRANSFIELD I., CHILVERS E.R., HASLETT I., ROSSI A.G. Pharmacological manipulation of granulocyte apoptosis: potential therapeutic targets. Trends Pharmacol. Sci., 1999, 20, 503-509.
WATSON R.W., REDMOND H.P., WANG J.H., BOUCHIERHAYES D. Bacterial ingestion, tumor necrosis factor-alpha, and heat induce programmed cell death in activated neutrophils. Shock, 1996, 5, 47-51.
WEBB P.R., WANG K.Q., SCHEEL-TOELLNER D., PONGRACZ J., SALMON M., LORD J.M. Regulation of neutrophil apoptosis: a role for protein kinase C and phosphatidylinositol-3-kinase. Apoptosis, 2000, 5, 451-458.
WEI S., LIU J.H., EPLING-BURNETTE P.K., GAMERO A.M., USSERY D., PEARSON E.W., ELKABANI M.E., DIAZ J.I., DJEU J.Y. Critical role of Lyn kinase in inhibition of neutrophil apoptosis by granulocyte-macrophage colony-stimulating factor. J. Immunol., 1996, 157, 5155-5162.
WEINMANN P., GAEHTGENS P., WALZOG B. Bcl-xL and Bax-alpha-mediated regulation of apoptosis of human neutrophils via caspase-3. Blood, 1999, 93, 3106-3115.
WEISS S.J. Tissue destruction by neutrophils. N. Engl. J. Med., 1989, 320, 365-376.
WILSON K.P., BLACK J.A., THOMSON J.A., KIM E.E., GRIFFITH J.P., NAVIA M.A., MURCKO M.A., CHAMBERS S.P., ALDAPE R.A., RAYBUCK S.A., LIVINGSTON D.J. Structure and mechanism of interleukin-1 beta converting enzyme. Nature, 1994, 370, 270-275.
WOO M., HAKEM R., SOENGAS M.S., DUNCAN G.S., SHAHINIAN A., KAGI D., HAKEM A., MCCURRACH M., KHOO W., KAUFMAN S.A., SENALDI G., HOWARD T., LOWE S.W., MAK T.W. Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes. Genes Dev., 1998, 12, 806-819.
YETTER A., UDDIN S., KROLEWSKI J.J., JIAO H., YI T., PLATANIAS L.C. Association of the interferon-dependent tyrosine kinase Tyk-2 with the hematopoietic cell phosphatase. J. Biol. Chem., 1995, 270, 18179-18182.
YIN X.M., OLTVAI Z.N., KORSMEYER S.J. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature, 1994, 369, 321-323.
YOSHIMURA A., OHKUBO T., KIGUCHI T., JENKINS N.A., GILBERT D.J., COPELAND N.G., HARA T., MIYAJIMA A. A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO J., 1995, 14, 2816-2826.
YOUSEFI S., GREEN D.R., BLASER K., SIMON H.U. Protein-tyrosine phosphorylation regulates apoptosis in human eosinophils and neutrophils. Proc. Natl. Acad. Sci. U.S.A., 1994, 91, 10868-10872.
YOUSEFI S., COOPER P.R., MUECK B., POTTER S.L., JARAI G. cDNA representational difference analysis of human neutrophils stimulated by GM-CSF. Biochem. Biophys. Res. Commun., 2000, 277, 401-409.
YU Z., SU L., HOGLINGER O., JARAMILLO M.L., BANVILLE D., SHEN S.H. SHP-1 associates with both platelet-derived growth factor receptor and the p85 subunit of phosphatidylinositol 3-kinase. J. Biol. Chem., 1998, 273, 3687-3694.
YUAN J., SHAHAM S., LEDOUX S., ELLIS H.M., HORVITZ H.R. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell, 1993, 75, 641-652.