Publication Cover
Redox Report
Communications in Free Radical Research
Volume 8, 2003 - Issue 3
629
Views
41
CrossRef citations to date
0
Altmetric
Reviews

Apoptosis and macrophage clearance of neutrophils: regulation by reactive oxygen species

&
Pages 143-150 | Published online: 19 Jul 2013

REFERENCES

  • Nathan C. Points of control in inflammation. Nature 2002; 420: 846–852.
  • Lawrence T, Willoughby DA, Gilroy DW. Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat Rev Immunol 2002; 2: 787–795.
  • Weiss SJ. Tissue destruction by neutrophils. N Engl J Med 1989; 320: 365–376.
  • Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980; 68: 251–306.
  • Savill J. Apoptosis in resolution of inflammation. J Leukoc Biol 1997; 61: 375–380.
  • Ward I, Dransfield I, Chilvers ER, Haslett I, Rossi AG. Pharmacological manipulation of granulocyte apoptosis: potential therapeutic targets. Trends Pharmacol Sci 1999; 20: 503–509.
  • Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM, 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.
  • Akgul C, Moulding DA, Edwards SW. Molecular control of neutrophil apoptosis. FEBS Lett 2001; 487: 318–322,
  • 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.
  • 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.
  • Brach MA, deVos S, Gruss HJ, 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.
  • Ravagnan L, Roumier T, Kroemer G. Mitochondria, the killer organelles and their weapons. J Cell Physiol 2002; 192: 131–137.
  • Fadeel B, Zhivotovsky B, Orrenius S. All along the watchtower: on the regulation of apoptosis regulators. FASEB J 1999; 13: 1647–1657.
  • Peachman KK, Lyles DS, Bass DA. Mitochondria in eosinophils: functional role in apoptosis but not respiration. Proc Natl Acad Sci USA 2001; 98: 1717–1722.
  • Watson RW, O'Neill A, Brannigen AE et al. Regulation of Fas antibody induced neutrophil apoptosis is both caspase and mitochondrial dependent. FEBS Lett 1999; 453: 67–71.
  • 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.
  • Villunger A, Scott C, Bouillet P. Strasser A. Essential role for the BH3-only protein Bim, but redundant roles for Bax, Bc1-2, and Bcl-w in the control of granulocyte survival. Blood 2003; 101: 2393–2400.
  • Watson RW, Rotstein OD, Nathens AB, Parodo J, Marshall JC. Neutrophil apoptosis is modulated by endothelial transmigration and adhesion molecule engagement. J Immunol 1997; 158: 945–953.
  • Walzog B, Jeblonski F, Zakrzewicz A, Gaehtgens P. Beta2 integrins (CD11/CD18) promote apoptosis of human neutrophils. FASEB J 1997; 11: 1177–1186.
  • Frisch SM, Screaton RA. Anoikis mechanisms. Curr Opin Cell Biol 2001; 13: 555–562.
  • Krammer PH. CD95's deadly mission in the immune system. Nature 2000; 407: 789–795.
  • Iwai K, Miyawaki T, Takizawa T et al. Differential expression of bc1-2 and susceptibility to anti-Fas-mediated cell death in peripheral blood lymphocytes, monocytes, and neutrophils. Blood 1994; 84: 1201–1208.
  • Fadeel B, fkhlin A, Henter J-I, Orrenius S, Hampton MB. Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood 1998; 92: 4808–4818.
  • 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.
  • Murray J, Barbara JA, Dunkley SA 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.
  • Yamashita K, Takahashi A, Kobayashi S et al. Caspases mediate tumor necrosis factor-alpha-induced neutrophil apoptosis and downregulation of reactive oxygen production. Blood 1999; 93: 674–685.
  • Renshaw SA, Parmar JS, Singleton V et al. Acceleration of human neutrophil apoptosis by TRAIL. J Immunol 2003; 170: 1027–1033.
  • 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.
  • Brown SB, Savill J. Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. J Immunol 1999; 162: 480–485.
  • Fecho K, Cohen PL. Fas ligand (g1d)- and Fas (1pr)-deficient mice do not show alterations in the extravasation or apoptosis of inflammatory neutrophils. J Leukoc Biol 1998; 64: 373–383.
  • Villunger A, O'Reilly LA, Holler N, Adams J, Strasser A. Fas ligand, B c1-2, 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.
  • Hengartner MO. The biochemistry of apoptosis. Nature 2000; 407: 770–776.
  • Fadeel B, Orrenius S, Zhivotovsky B. The most unkindest cut of all: on the multiple roles of mammalian caspases. Leukemia 2000; 14: 1514–1525.
  • Sanghavi DM, Thelen M, Thomberry NA, Casciola-Rosen L, Rosen A. Caspase-mediated proteolysis during apoptosis: insights from apoptotic neutrophils. FEBS Lett 1998; 422: 179–184.
  • Rowe SJ, Allen L, Ridger VC, Hellewell PG, Whyte MK. Caspase-l-deficient mice have delayed neutrophil apoptosis and a prolonged inflammatory response to lipopolysaccharide-induced acute lung injury. J Immunol 2002; 169: 6401–6407.
  • 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.
  • Squier MK, Sehnert AJ, Sellins KS, Malkinson AM, Takano E, Cohen JJ. Calpain and calpastatin regulate neutrophil apoptosis. J Cell Physiol 1999; 178: 311–319.
  • 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.
  • Chandra J, Samali A, Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 2000; 29: 323–333.
  • Carmody RJ, Cotter TG. Signalling apoptosis: a radical approach. Redox Report 2001; 6: 77–90.
  • Hampton MB, Orrenius S. Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis. FEBS Lett 1997; 414: 552–556.
  • Hampton MB, Fadeel B, Orrenius S. Redox regulation of the caspases during apoptosis. Ann NY Acad Sci 1998; 854: 328–335.
  • Nobel CS, Burgess DH, Zhivotovsky B, Burkitt MJ, Orrenius S, Slater AF. Mechanism of dithiocarbamate inhibition of apoptosis: thiol oxidation by dithiocarbamate disulfides directly inhibits processing of the caspase-3 proenzyme. Chem Res Toxicol 1997; 10: 636–643.
  • Babior BM. NADPH oxidase: an update. Blood 1999; 93: 1464–1476.
  • Takei H, Araki A, Watanabe H, Ichinose A, Sendo F. Rapid killing of human neutrophils by the potent activator phorbol 12-myristate 13-acetate (PMA) accompanied by changes different from typical apoptosis or necrosis. J Leukoc Biol 1996; 59: 229–240.
  • Roos D, de Boer M, Kuribayashi F et al. Mutations in the X-linked and autosomal recessive forms of chronic granulomatous disease. Blood 1996; 87: 1663–1681.
  • Goldblatt D, Thrasher AJ. Chronic granulomatous disease. Clin Exp Immunol 2000; 122: 1–9.
  • 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.
  • Watson RW, Redmond HP, Wang JH, Condron C, B ouchier-Hayes D. Neutrophils undergo apoptosis following ingestion of Escherichia coli. J Immunol 1996; 156: 3986–3992.
  • Gamberale R, Giordano M, Trevani AS, Andonegui G, Geffner JR. Modulation of human neutrophil apoptosis by immune complexes. J Immunol 1998; 161: 3666–3674.
  • Ottonello L, Frumento G, Arduino N, Dapino P. Tortolina G, Dallegri F. Immune complex stimulation of neutrophil apoptosis: investigating the involvement of oxidative and nonoxidative pathways. Free Radic Biol Med 2001; 30: 161–169.
  • Tsurubuchi T, Aratani Y, Maeda N, Koyama H. Retardation of early-onset PMA-induced apoptosis in mouse neutrophils deficient in myeloperoxidase. J Leukoc Biol 2001; 70: 52–58.
  • Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 1998; 92: 3007–3017.
  • van den Dobbelsteen DJ, Nobel CS, Schlegel J, Cotgreave IA, Orrenius S, Slater AF. Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J Biol Chem 1996; 271: 15420–15427.
  • Ghibelli L, Fanelli C, Rotilio G et al. Rescue of cells from apoptosis by inhibition of active GSH extrusion. FASEB J 1998; 12: 479–486.
  • Watson RW. Redox regulation of neutrophil apoptosis. Antioxid Redox Signal 2002; 4: 97–104.
  • 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.
  • Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature 1997; 390: 350–351.
  • Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. 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 1998; 101: 890–898.
  • Huynh A, Bratton DL, Henson PM. Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences. J Clin Invest 2001; 108: 957–962.
  • Balasubramanian K, Schroit AJ. Aminophospholipid asymmetry: a matter of life and death. Annu Rev Physiol 2003; 65: 701–734.
  • Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 1992; 148: 2207–2216.
  • Martin SJ, Reutelingsperger CP, McGahon AJ et al. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of B c1-2 and Abl. J Exp Med 1995; 182: 1545–1556.
  • Homburg CH, de Haas M, von dem Borne AE, Verhoeven AJ, Reutelingsperger CP, 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.
  • Fadok VA, de Cathelineau A, Daleke DL, Henson PM, Bratton DL. Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. J Biol Chem 2001; 276: 1071–1077.
  • Kagan VE, Gleiss B, Tyurina YY et al. A role for oxidative stress in apoptosis: oxidation and externalization of phosphatidylserine is required for macrophage clearance of cells undergoing Fas-mediated apoptosis. J Immunol 2002; 169: 487–499.
  • Fadeel B, Gleiss B, Högstrand K et al. Phosphatidylserine exposure during apoptosis is a cell type-specific event and does not correlate with plasma membrane phospholipid scramblase expression. Biochem Biophys Res Commun 1999; 266: 504–511.
  • Cocco RE, Ucker DS. Distinct modes of macrophage recognition for apoptotic and necrotic cells are not specified exclusively by phosphatidylserine exposure. Mol Biol Cell 2001; 12: 919–930.
  • Watanabe Y, Shiratsuchi A, Shimizu K, Takizawa T, Nakanishi Y. Role of phosphatidylserine exposure and sugar chain desialylation at the surface of influenza virus-infected cells in efficient phagocytosis by macrophages. J Biol Chem 2002; 277: 18222–18228.
  • Savill J, Dransfield I, Hogg N, Haslett C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 1990; 343: 170–173.
  • Savill J, Hogg N, Ren Y, Haslett C. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest 1992; 90: 1513–1522.
  • Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 2002; 417: 182–187.
  • Balasubramanian K, Schroit AJ. Characterization of phosphatidylserine-dependent beta2-glycoprotein I macrophage interactions. Implications for apoptotic cell clearance by phagocytes. J Biol Chem 1998; 273: 29272–29277.
  • ML, Fadok VA, Henson PM. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-betal secretion and the resolution of inflammation. J Clin Invest 2002; 109: 41–50.
  • Botto M, Dell'Agnola C, Bygrave AE et al. Homozygous Clq deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 1998; 19: 56–59.
  • Scott RS, McMahon EJ, Pop SM et al. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 2001; 411: 207–211.
  • O'Brien BA, Huang Y, Geng X, Dutz JP, Finegood DT. Phagocytosis of apoptotic cells by macrophages from NOD mice is reduced. Diabetes 2002; 51: 2481–2488.
  • Fadok V Anderson HA, Maylock CA, Williams JA, Paweletz CP, Shu H, Shacter E. Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat Immunol 2003; 4: 87–91.
  • Brown S, Heinisch I, Ross E, Shaw K, Buckley CD, Savill J. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature 2002; 418: 200–203.
  • Ritov VB, Banni S, Yalowich JC et al. Non-random peroxidation of different classes of membrane phospholipids in live cells detected by metabolically integrated cis-parinaric acid. BiochimBiophys Acta 1996; 1283: 127–140.
  • Kagan YE, Fabisiak JP, Shvedova AA et al. Oxidative signaling pathway for externalization of plasma membrane phosphatidylserine during apoptosis. FEBS Lett 2000; 477: 1–7.
  • Kagan YE, Borisenko GG, Serinkan BF et al. Appetizing rancidity of apoptotic cells for macrophages: oxidation, externalization, and recognition of phosphatidylserine. Am J Physiol 2003; 285: 1–17.
  • Matsura T, Serinkan BF, Jiang J, Kagan YE. Phosphatidylserine peroxidation/externalization during staurosporine-induced apoptosis in HL-60 cells. FEBS Lett 2002; 524: 25–30.
  • Koty PP, Tyurina YY, Tyurin VA, Li SX, Kagan YE. Depletion of Bc1-2 by an antisense oligonucleotide induces apoptosis accompanied by oxidation and externalization of phosphatidyl-serine in NCI-H226 lung carcinoma cells. Mol Cell Biochem 2002; 234-235: 125-133.
  • Arroyo A, Modriansky M, Serinkan FB et al. NADPH oxidase-dependent oxidation and externalization of phosphatidylserine during apoptosis in Me2S0-differentiated HL-60 cells. Role in phagocytic clearance. J Biol Chem 2002; 277: 49965–49975.
  • Coxon A, Rieu P. Barkalow FJ et al. A novel role for the beta 2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity 1996; 5: 653–666.
  • Chang MK, Bergmark C, Laurila A et al. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc Natl Acad Sci USA 1999; 96: 6353–6358.
  • Chang MK, Binder CJ, Torzewski M, Witztum JL. C-reactive protein binds to both oxidized LDL and apoptotic cells through recognition of a common ligand: phosphorylcholine of oxidized phospholipids. Proc Natl Acad Sci USA 2002; 99: 13043–13048.
  • Fadok VA, Bratton DL, Guthrie L, Henson PM. Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: role of proteases. J Immunol 2001; 166: 6847–6854.
  • Vandivier RW, Fadok VA, Hoffmann PR et al. Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. J Clin Invest 2002; 109: 661–670.
  • Scaffidi P. Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418: 191–195.
  • Teder P. Vandivier RW, Jiang D et al. Resolution of lung inflammation by CD44. Science 2002; 296: 155–158.
  • Yang S, Panoskaltsis-Mortari A, Shukla M, Blazar BR, Haddad IY. Exuberant inflammation in nicotinamide adenine dinucleotide phosphate-oxidase-deficient mice after allogeneic marrow transplantation. J Immunol 2002; 168: 5840–5847.
  • Hampton MB, Vissers MC, Keenan JI, Winterbourn CC Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils: possible impairment in chronic granulomatous disease. J Leukoc Biol 2002; 71: 775–781.
  • Forman HJ, Tones M. Redox signaling in macrophages. Mol Aspects Med 2001; 22: 189–216.
  • Hoidal JR, Fox RB, Repine JE. Defective oxidative metabolic responses in vitro of alveolar macrophages in chronic granulomatous disease. Am Rev Respir Dis 1979; 120: 613–618.
  • Kinnula VL, Soini Y, Kvist-Makela K, Savolainen ER, Koistinen P. Antioxidant defense mechanisms in human neutrophils. Antioxid Redox Signal 2002; 4: 27–34.
  • Rahman I, MacNee W. Regulation of redox glutathione levels and gene transcription in lung inflammation: therapeutic approaches. Free Radic Biol Med 2000; 28: 1405–1420.s

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.