Appetizing rancidity of apoptotic cells for macrophages: Oxidation, externalization, and recognition of phosphatidylserine

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 285, Issue 1 29-1, 2003, Pages

  Kagan, V E ^a   Borisenko, G G ^a   Serinkan, B F ^a   Tyurina, Y Y ^a   Tyurin, V A ^a   Jiang, J ^a   Liu, S X ^a   Shvedova, A A ^b   Fabisiak, J P ^a   Uthaisang, W ^c   Fadeel, B ^c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Apoptosis; Cytochrome c; Macrophage receptor; Phagocytosis; Phosphatidylserine oxidation and externalization

Indexed keywords

CYTOCHROME C; FREE RADICAL; PHOSPHATIDYLSERINE;

APOPTOSIS; CELL DAMAGE; CELL MEMBRANE TRANSPORT; HUMAN; MACROPHAGE; MOLECULAR RECOGNITION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0038508925     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00365.2002     Document Type: Review

References (167)

1. Aljandali A, Pollack H, Yeldandi A, Li Y, Weitzman SA, and Kamp DW. Asbestos causes apoptosis in alveolar epithelial cells: role of iron-induced free radicals. J Lab Clin Med 137: 330-339, 2001.
2. Alonso MA and Millan J. The role of lipid rafts in signalling and membrane trafficking in T lymphocytes. J Cell Sci 114: 3957-3965, 2001.
3. Anderson HA, Englert R, Gursel I, and Shacter E. Oxidative stress inhibits the phagocytosis of apoptotic cells that have externalized phosphatidylserine. Cell Death Differ 9: 616-625, 2002.
4. Arroyo A, Modriansky M, Serinkan FB, Bello RI, Matsura T, Jiang J, Tyurin VA, Tyurina YY, Fadeel B, and Kagan VE. NADPH oxidase-dependent oxidation and externalization of phosphatidylserine during apoptosis in DMSO-differentiated HL-60 cells: role in phagocytic clearance. J Biol Chem 277: 49965-49975, 2002.
5. Balasubramanian K and Schroit AJ. Characterization of phosphatidylserine-dependent beta2-glycoprotein I macrophage interactions. Implications for apoptotic cell clearance by phagocytes. J Biol Chem 273: 29272-29277, 1998.
6. Bevers EM, Comfurius P, Dekkers DW, and Zwaal RF. Lipid translocation across the plasma membrane of mammalian cells. Biochim Biophys Acta 1439: 317-330, 1999.
7. Bratton DL, Fadok VA, Richter DA, Kailey JM, Guthrie LA, and Henson PM. Appearance of phosphatidylserine on apoptotic cells requires calcium-mediated nonspecific flip-flop and is enhanced by loss of the aminophospholipid translocase. J Biol Chem 272: 26159-26165, 1997.
8. Brennan AL and Geddes DM. Cystic fibrosis. Curr Opin Infect Dis 15: 175-182, 2002.
9. Brown S, Heinisch I, Ross E, Shaw K, Buckley CD, and Savill J. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature 418: 200-203, 2002.
10. Buttke TM and Sandstrom PA. Oxidative stress as a mediator of apoptosis. Immunol Today 15: 7-10, 1994.
11. Cai J and Jones DP. Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273: 11401-11404, 1998.
12. Callahan MK, Williamson P, and Schlegel RA. Surface expression of phosphatidylserine on macrophages is required for phagocytosis of apoptotic thymocytes. Cell Death Differ 7: 645-653, 2000.
13. Cappelletti G, Maggioni MG, and Maci R. Apoptosis in human lung epithelial cells: triggering by paraquat and modulation by antioxidants. Cell Biol Int 22: 671-678, 1998.
14. Catisti R and Vercesi AE. The participation of pyridine nucleotides redox state and reactive oxygen in the fatty acidinduced permeability transition in rat liver mitochondria. FEBS Lett 464: 97-101, 1999.
15. Chandra J, Samali A, and Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 29: 323-333, 2000.
16. Chang M, Bergmark C, Laurila A, Horkko S, Han K, Friedman P, Dennis EA, and Witztum JL. 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 96: 6353-6358, 1999.
17. Chang MK, Binder CJ, Torzewski M, and 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 99: 13043-13048, 2002.
18. Chao SK, Hamilton RF, Pfau JC, and Holian A. Cell surface regulation of silica-induced apoptosis by the SR-A scavenger receptor in a murine lung macrophage cell line (MH-S). Toxicol Appl Pharmacol 174: 10-16, 2001.
19. Cocca BA, Seal SN, D'Agnillo P, Mueller YM, Katsikis PD, Rauch J, Weigert M, and Radic MZ. Structural basis for autoantibody recognition of phosphatidylserine-beta 2 glycoprotein I and apoptotic cells. Proc Natl Acad Sci USA 98: 13826-13831, 2001.
20. Cohen JJ. Programmed cell death in the immune system. Adv Immunol 50: 55-85, 1991.
21. Costantini P, Colonna R, and Bernardi P. Induction of the mitochondrial permeability transition by N-ethylmaleimide depends on secondary oxidation of critical thiol groups. Potentiation by copper-ortho-phenanthroline without dimerization of the adenine nucleotide translocase. Biochim Biophys Acta 1365: 385-392, 1998.
22. De Jongh HH, Ritsema T, and Killian JA. Lipid specificity for membrane mediated partial unfolding of cytochrome c. FEBS Lett 360: 255-260, 1995.
23. De Paepe ME, Rubin LP, Jude C, Lesieur-Brooks AM, Mills DR, and Luks FI. Fas ligand expression coincides with alveolar cell apoptosis in late-gestation fetal lung development. Am J Physiol Lung Cell Mol Physiol 279: L967-L976, 2000.
24. Del Rio M, Ruedas G, Medina S, Victor VM, and De la Fuente M. Improvement by several antioxidants of macrophage function in vitro. Life Sci 63: 871-881, 1998.
25. Devaux PF. Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30: 1163-1173, 1991.
26. Devitt A, Moffatt OD, Raykundalia C, Capra JD, Simmons DL, and Gregory CD. Human CD14 mediates recognition and phagocytosis of apoptotic cells. Nature 392: 505-509, 1998.
27. Dillon SR, Mancini M, Rosen A, and Schlissel MS. Annexin V binds to viable B cells and colocalizes with a marker of lipid rafts upon B cell receptor activation. J Immunol 164: 1322-1332, 2000.
28. Dimmeler S, Haendeler J, Nehls M, and Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-lbeta-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J Exp Med 185: 601-607, 1997.
29. Ding J, Wu Z, Crider BP, Ma Y, Li X, Slaughter C, Gong L, and Xie XS. Identification and functional expression of four isoforms of ATPase II, the putative aminophospholipid translocase. Effect of isoform variation on the ATPase activity and phospholipid specificity. J Biol Chem 275: 23378-23386, 2000.
30. Drummen GP, Op den Kamp JA, and Post JA Validation of the peroxidative indicators, cis-parinaric acid and parinaroyl-phospholipids, in a model system and cultured cardiac myocytes. Biochim Biophys Acta 1436: 370-382, 1999.
31. Ellerby HM, Arap W, Ellerby LM, Kain R, Andrusiak R, Del Bio G, Krajewski S, Lombardo CR, Rao R, Ruoslahti E, Bredesen DE, and Pasqualini R. Anti-cancer activity of targeted pro-apoptotic peptides. Nat Med 5: 1032-1038, 1999.
32. Ellis RE, Yuan JY, and Horvitz HR. Mechanisms and functions of cell death. Annu Rev Cell Biol 7: 663-698, 1991.
33. Fabisiak JP, Kagan VE, Ritov VB, Johnson DE, and Lazo JS. Bcl-2 inhibits selective oxidation and externalization of phosphatidylserine during paraquat-induced apoptosis. Am J Physiol Cell Physiol 272: C675-C684, 1997.
34. 2. Am J Physiol Lung Cell Mol Physiol 274: L793-L802, 1998.
35. Fabisiak JP, Tyurin VA, Tyurina YY, Sedlov A, Lazo JS, and Kagan VE. Nitric oxide dissociates lipid oxidation from apoptosis and phosphatidylserine externalization during oxidative stress. Biochemistry 39: 127-138, 2000.
36. Fabisiak JP, Tyurina YY, Tyurin VA, Lazo JS, and Kagan VE. Random versus selective membrane phospholipid oxidation in apoptosis: role of phosphatidylserine. Biochemistry 37: 13781-13790, 1998.
37. Fadeel B, Ahlin A, Henter JI, Orrenius S, and Hampton MB. Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood 92: 4808-4818, 1998.
38. Fadeel B, Gleiss B, Högstrand K, Chandra J, Wiedmer T, Sims PJ, Henter JI, Orrenius S, and Samali A. Phosphatidylserine exposure during apoptosis is a cell type-specific event and does not correlate with plasma membrane phospholipid scramblase expression. Biochem Biophys Res Commun 266: 504-511, 1999.
39. Fadok VA, Bratton DL, and Henson PM. Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences. J Clin Invest 108: 957-962, 2001.
40. Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, and Henson PM. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405: 85-90, 2000.
41. Fadok VA and Chimini G. The phagocytosis of apoptotic cells. Semin Immunol 13: 365-72, 2001.
42. Fadok VA, Savill JS, Haslett C, Bratton DL, Doherty DE, Campbell PA, and Henson PM. Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J Immunol 149: 4029-4035, 1992.
43. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, and Henson PM. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148: 2207-2216, 1992.
44. 3). J Immunol 161: 6250-6257, 1998.
45. Fine A, Anderson NL, Rothstein TL, Williams MC, and Gochuico BR. Fas expression in pulmonary alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 273: L64-L71, 1997.
46. Fine A, Janssen-Heininger Y, Soultanakis RP, Swisher SG, and Uhal BD. Apoptosis in lung pathophysiology. Am J Physiol Lung Cell Mol Physiol 279: L423-L427, 2000.
47. Frey T. Correlated flow cytometric analysis of terminal events in apoptosis reveals the absence of some changes in some model systems. Cytometry 28: 253-263, 1997.
48. Gillotte KL, Horkko S, Witztum JL, and Steinberg D. Oxidized phospholipids, linked to apolipoprotein B of oxidized LDL, are ligands for macrophage scavenger receptors. J Lipid Res 41: 824-833, 2000.
49. Gleiss B, Gogvadze V, Orrenius S, and Fadeel B. Fas-triggered phosphatidylserine exposure is modulated by intracellular ATP. FEBS Lett 519: 153-158, 2002.
50. Gotz ME, Ahlbom E, Zhivotovsky B, Blum-Degen D, Oettel M, Romer W, Riederer P, Orrenius S, and Ceccatelli S. Radical scavenging compound J 811 inhibits hydrogen peroxide-induced death of cerebellar granule cells. J Neurosci Res 56: 420-426, 1999.
51. Gousset K, Wolkers WF, Tsvetkova NM, Oliver AE, Field CL, Walker NJ, Crowe JH, and Tablin F. Evidence for a physiological role for membrane rafts in human platelets. J Cell Physiol 190: 117-128, 2002.
52. Hagimoto N, Kuwano K, Miyazaki H, Kunitake R, Fujita M, Kawasaki M, Kaneko Y, and Hara N. Induction of apoptosis and pulmonary fibrosis in mice in response to ligation of Fas antigen. Am J Respir Cell Mol Biol 17: 272-278, 1997.
53. Hagimoto N, Kuwano K, Nomoto Y, and Kunitake R, and Hara N. Apoptosis and expression of Fas/Fas ligand mRNA in bleomycin-induced pulmonary fibrosis in mice. Am J Respir Cell Mol Biol 16: 91-101, 1997.
54. Hamon Y, Broccardo C, Chambenoit O, Luciani MF, Toti F, Chaslin S, Freyssinet JM, Devaux PF, McNeish J, Marguet D, and Chimini G. ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat Cell Biol 2: 399-406, 2000.
55. Hampton MB, Fadeel B, and Orrenius S. Redox regulation of the caspases during apoptosis. Ann NY Acad Sci 854: 328-335, 1998.
56. Hampton MB and Orrenius S. Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis. FEBS Lett 414: 552-556, 1997.
57. Hampton MB, Vanags DM, Pörn-Ares MI, and Orrenius S. Involvement of extracellular calcium in phosphatidylserine exposure during apoptosis. FEBS Lett 399: 277-282, 1996.
58. Hampton MB, Vissers MC, Keenan JI, and Winterbourn CC. Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils: possible impairment in chronic granulomatous disease. J Leukoc Biol 71: 775-781, 2002.
59. Hampton MB, Zhivotovsky B, Slater AF, Burgess DH, and Orrenius S. Importance of the redox state of cytochrome c during caspase activation in cytosolic extracts. Biochem J 329: 95-99, 1998.
60. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, and Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 417: 182-187, 2002.
61. Hart SP, Dougherty GJ, Haslett C, and Dransfield I. CD44 regulates phagocytosis of apoptotic neutrophil granulocytes, but not apoptotic lymphocytes, by human macrophages. J Immunol 159: 919-925, 1997.
62. Hashimoto S, Kobayashi A, Kooguchi K, Kitamura Y, Onodera H, and Nakajima H. Upregulation of two death pathways of perforin/granzyme and FasL/Fas in septic acute respiratory distress syndrome. Am J Respir Crit Care Med 161: 237-243, 2000.
63. Hedley D and Chow S. Flow cytometric measurement of lipid peroxidation in vital cells using parinaric acid. Cytometry 13: 686-692, 1992.
64. Henson PM, Bratton DL, and Fadok VA. Apoptotic cell removal. Curr Biol 11: R795-R805, 2001.
65. Herrmann A and Devaux PF. Alteration of the aminophospholipid translocase activity during in vivo and artificial aging of human erythrocytes. Biochim Biophys Acta 1027: 41-46, 1990.
66. Hildeman DA, Mitchell T, Teague TK, Henson P, Day BJ, Kappler J, and Marrack PC. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 10: 735-44, 1999.
67. Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, and Korsmeyer SJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241-251, 1993.
68. Hoffmann PR, deCathelineau AM, Ogden CA, Leverrier Y, Bratton DL, Daleke DL, Ridley AJ, Fadok VA, and Henson PM. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol 155: 649-659, 2001.
69. Javadpour MM, Juban MM, Lo WJ, Bishop SM, Alberty JB, Cowell SM, Becker CL, and Mclaughlin ML. De novo antimicrobial peptide with low mammalian cell toxicity. J Med Chem 39: 3107-3113, 1996.
70. Jiang X and Wang X. Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to Apaf-1. J Biol Chem 275: 31199-31203, 2000.
71. Johnston RB. Clinical aspects of chronic granulomatous disease. Curr Opin Hematol 8: 17-22, 2001.
72. Kagan VE. Lipid Peroxidation in Biomembranes. Boca Raton, FL: CRC, 1998, p. 146.
73. Kagan VE, Fabisiak JP, Shvedova AA, Tyurina YY, Tyurin VA, Schor NF, and Kawai K. Oxidative signaling pathway for externalization of plasma membrane phosphatidylserine during apoptosis. FEBS Lett 477: 1-7, 2000.
74. Kagan VE, Gleiss B, Tyurina YY, Tyurin VA, Elenström-Magnusson C, Liu SX, Serinkan FB, Arroyo A, Chandra J, Orrenius S, and Fadeel B. A role for oxidative stress in apoptosis: oxidation and externalization of phosphatidylserine is required for macrophage clearance of cells undergoing Fasmediated apoptosis. J Immunol 169: 487-499, 2002.
75. Kane DJ, Sarafian TA, Anton R, Hahn H, Gralla EB, Valentine JS, Ord T, and Bredesen DE. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262: 1274-1277, 1993.
76. Kawai K, Liu SX, Tyurin VA, Tyurina YY, Borisenko GG, Jiang JF, St Croix CM, Fabisiak JP, Pitt BR, and Kagan VE. Antioxidant and antiapoptotic function of metallothioneins in HL-60 cells challenged with copper nitrilotriacetate. Chem Res Toxicol 13: 1275-1386, 2000.
77. Kawai K, Tyurina Y, Tyurin V, Kagan VE, and Fabisiak JP. Peroxidation and externalization of phosphatidylserine in plasma membrane of HL-60 cells during tert-butyl hydroperoxide-induced apoptosis: role of cytochrome C (Abstract). Toxicol Sci 54: 165, 2000.
78. Kazzaz JA, Horowitz S, Xu J, Khullar P, Niederman MS, Fein AM, Zakeri Z, Lin L, and Rhodes GC. Differential patterns of apoptosis in resolving and nonresolving bacterial pneumonia. Am J Respir Crit Care Med 161: 2043-2050, 2000.
79. Kluck RM, Martin SJ, Hoffman BM, Zhou JS, Green DR, and Newmeyer DD. Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO J 16: 4639-4649, 1997.
80. Koty PP, Tyurina YY, Tyurin VA, Li SX, and Kagan VE. Depletion of Bcl-2 by an antisense oligonucleotide induces apoptosis accompanied by oxidation and externalization of phosphatidylserine in NCI-H226 lung carcinoma cells. Mol Cell Biochem 234-235: 125-33, 2002.
81. Kowaltowski AJ, Vercesi AE, and Fiskum G. Bcl-2 prevents mitochondrial permeability transition and cytochrome c release via maintenance of reduced pyridine nucleotides. Cell Death Differ 7: 903-910, 2000.
82. Kresch MJ, Christian C, Wu F, and Hussain N. Ontogeny of apoptosis during lung development. Pediatr Res 43: 426-431, 1998.
83. Kunzelmann-Marche C, Freyssinet JM, and Martinez MC. Loss of plasma membrane phospholipid asymmetry requires raft integrity. Role of transient receptor potential channels and ERK pathway. J Biol Chem 277: 19876-19881, 2002.
84. Kuwano K, Hagimoto N, Kawasaki M, Yatomi T, Nakamura N, Nagata S, Suda T, Kunitake R, Maeyama T, Miyazaki H, and Hara N. Essential roles of the Fas-Fas ligand pathway in the development of pulmonary fibrosis. J Clin Invest 104: 13-19, 1999.
85. Kuwano K, Kunitake R, Kawasaki M, Nomoto Y, Hagimoto N, Nakanishi Y, and Hara N. P21Waf1/Cip1/Sdi1 and p53 expression in association with DNA strand breaks in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 154: 477-483, 1996.
86. Kuwano K, Miyazaki H, Hagimoto N, Kawasaki M, Fujita M, Kunitake R, Kaneko Y, and Hara N. The involvement of Fas-Fas ligand pathway in fibrosing lung diseases. Am J Respir Cell Mol Biol 20: 53-60, 1999.
87. Kuypers FA, van den Berg JJM, Schalkwijk C, Roelofsen B, and Op den Kamp JAF. Parinaric acid as a sensitive fluorescent probe for the determination of lipid peroxidation. Biochim Biophys Acta 921: 266-274, 1987.
88. Leigh J, Wang H, Bonin A, Peters M, and Ruan X. Silica-induced apoptosis in alveolar and granulomatous cells in vivo. Environ Health Perspect 105: 1241-1245, 1997.
89. Liles WC, Kiener PA, Ledbetter JA, Aruffo A, and 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 184: 429-440, 1996.
90. Lilja H, Laurell CB, and Jeppsson JO. Characterization of the predominant basic protein in human seminal plasma, one cleavage product of the major seminal vesicle protein. Scand J Clin Lab Invest 44: 439-446, 1984.
91. Liu S, Kawai K, Tyurin VA, Tyurina YY, Borisenko GG, Fabisiak JP, Quinn PJ, Pitt BR, and Kagan VE. Nitric oxide-dependent pro-oxidant and pro-apoptotic effect of metallothioneins in HL-60 cells challenged with cupric nitrilotriacetate. Biochem J 354: 397-406, 2001.
92. Mandal D, Moitra PK, Saha S, and Basu J. Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes. FEBS Lett 513: 184-188, 2002.
93. Manno S, Takakuwa Y, and Mohandas N. Identification of a functional role for lipid asymmetry in biological membranes: phosphatidylserine-skeletal protein interactions modulate membrane stability. Proc Natl Acad Sci USA 99: 1943-1948, 2002.
94. Martin SJ, Finucane DM, Amarante-Mendes GP, O'Brien GA, and Green DR. Phosphatidylserine externalization during CD95-induced apoptosis requires ICE/CED-3 protease activity. J Biol Chem 271: 28753-28756, 1996.
95. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, and Green DR. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 182: 1545-1556, 1995.
96. Martinez MC and Freyssinet JM. Deciphering the plasma membrane hallmarks of apoptotic cells: phosphatidylserine transverse redistribution and calcium entry. BMC Cell Biol 2: 20, 2001.
97. Matsura T, Serinkan BF, Jiang J, and Kagan VE. Phosphatidylserine peroxidation/externalization during staurosporine-induced apoptosis in HL-60 cells. FEBS Lett 524: 25-30, 2002.
98. Mattson MP. Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 1: 120-129, 2000.
99. Matute-Bello G, Liles WC, Steinberg KP, Kiener PA, Mongovin S, Chi EY, Jonas M, and Martin TR. Soluble Fas ligand induces epithelial cell apoptosis in humans with acute lung injury (ARDS). J Immunol 163: 2217-2225, 1999.
100. McIntyre JC and Sleight RG. Fluorescence assay for phospholipid membrane asymmetry. Biochemistry 30: 11819-11827, 1991.
101. Mevorach D, Mascarenhas JO, Gershov D, and Elkon KB. Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med 188: 2313-2320, 1998.
102. Mi Z, Mai J, Lu X, and Robins PD. Characterization of a class of cationic peptides able to facilitate efficient protein transduction in vitro and in vivo. Mol Ther 2: 339-347, 2000.
103. Nantes IL, Zucchi MR, Nascimento OR, and Faljoni-Alario A. Effect of heme iron valence state on the conformation of cytochrome c and its association with membrane interfaces: a CD and EPR investigation. J Biol Chem 276: 153-158, 2001.
104. Ogasawara J, Watanabe-Fukunaga R, Adachi M, Matsuzawa A, Kasugai T, Kitamura Y, Itoh N, Suda T, and Nagata S. Lethal effect of the anti-Fas antibody in mice. Nature 364: 806-809, 1993.
105. Oram JF and Lawn RM. ABCA1. The gatekeeper for eliminating excess tissue cholesterol. J Lipid Res 42: 1173-1179, 2001.
106. Pacifici EH, McLeod LL, and Sevanian A. Lipid hydroper-oxide-induced peroxidation and turnover of endothelial cell phospholipids. Free Radic Biol Med 17: 297-309, 1994.
107. Packard BZ, Komoriya A, Brotz TM, and Henkart PA. Caspase 8 activity in membrane blebs after anti-Fas ligation. J Immunol 167: 5061-5066, 2001.
108. Palmgren MG and Axelsen KB. Evolution of P-type ATPases. Biochim Biophys Acta 1365: 37-45, 1998.
109. Pascher T, Chesick JP, Winkler JR, and Gray HB. Protein folding triggered by electron transfer. Science 271: 1558-1560, 1996.
110. Patel T. Apoptosis in hepatic pathophysiology. Clin Liver Dis 4: 295-317, 2000.
111. Persson HL, Svensson AI, and Brunk UT. Alpha-lipoic acid and alpha-lipoamide prevent oxidant-induced lysosomal rupture and apoptosis. Redox Rep 6: 327-334, 2001.
112. Pervaiz S and Clement MV. A permissive apoptotic environment: function of a decrease in intracellular superoxide anion and cytosolic acidification. Biochem Biophys Res Commun 290: 1145-1150, 2002.
113. Pinheiro TJ, Elove GA, Watts A, and Roder H. Structural and kinetic description of cytochrome c unfolding induced by the interaction with lipid vesicles. Biochemistry 36: 13122-13132, 1997.
114. Platt N, da Silva RP, and Gordon S. Recognizing death: the phagocytosis of apoptotic cells. Trends Cell Biol 8: 365-372, 1998.
115. Platt N and Gordon S. Is the class A macrophage scavenger receptor (SR-A) multifunctional? The mouse's tale. J Clin Invest 108: 649-654, 2001.
116. Platt N, Haworth R, Darley L, and Gordon S. The many roles of the class A macrophage scavenger receptor. Int Rev Cytol 212: 1-40, 2002.
117. Podrez EA, Poliakov E, Shen Z, Zhang R, Deng Y, Sun M, Finton PJ, Shan L, Febbraio M, Hajjar DP, Silverstein RL, Hoff HF, Salomon RG, and Hazen SL. A novel family of atherogenic oxidized phospholipids promotes macrophage foam cell formation via the scavenger receptor CD36 and is enriched in atherosclerotic lesions. J Biol Chem 277: 38517-38523, 2002.
118. Podrez EA, Poliakov E, Shen Z, Zhang R, Deng Y, Sun M, Finton PJ, Shan L, Gugiu B, Fox PL, Hoff HF, Salomon RG, and Hazen SL. Identification of a novel family of oxidized phospholipids that serve as ligands for the macrophage scavenger receptor CD36. J Biol Chem 277: 38503-38516, 2002.
119. Pradhan D, Krahling S, Williamson P, and Schlegel RA. Multiple systems for recognition of apoptotic lymphocytes by macrophages. Mol Biol Cell 8: 767-778, 1997.
120. Quinn PJ. Plasma membrane phospholipid asymmetry. Subcell Biochem 36: 39-60, 2002.
121. Raha S and Robinson BH. Mitochondria, oxygen free radicals, and apoptosis. Am J Med Genet 106: 62-70, 2001.
122. Rahman I and MacNee W. Regulation of redox glutathione levels and gene transcription in lung inflammation: therapeutic approaches. Free Radic Biol Med 28: 1405-1420, 2000.
123. Ren Y, Silverstein RL, Allen J, and Savill J. CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J Exp Med 181: 1857-1862, 1995.
124. Ritov VB, Banni S, Yalowich JC, Day BW, Claycamp HG, Corongiu FP, and Kagan VE. Non-random peroxidation of different classes of membrane phospholipids in live cells detected by metabolically integrated cis-parinaric acid. Biochim Biophys Acta 1283: 127-140, 1996.
125. Robertson JD, Chandra J, Gogvadze V, and Orrenius S. Biological reactive intermediates and mechanisms of cell death. Adv Exp Med Biol 500: 1-10, 2001.
126. Robertson JD, Fadeel B, Zhivotovsky B, and Orrenius S. "Centennial" Nobel conference on apoptosis and human disease. Cell Death Differ 9: 468-475, 2002.
127. Roy S, Sen CK, Kobuchi H, and Packer L. Antioxidant regulation of phorbol ester-induced adhesion of human Jurkat T-cells to endothelial cells. Free Radic Biol Med 25: 229-241, 1998.
128. Sambrano GR and Steinberg D. Recognition of oxidatively damaged and apoptotic cells by an oxidized low density lipoprotein receptor on mouse peritoneal macrophages: role of membrane phosphatidylserine. Proc Natl Acad Sci USA 92: 1396-1400, 1995.
129. Sambrano GR, Terpstra V, and Steinberg D. Independent mechanisms for macrophage binding and macrophage phagocytosis of damaged erythrocytes. Evidence of receptor cooperativity. Arterioscler Thromb Vasc Biol 17: 3442-3448, 1997.
130. Sandstrom PA, Tebbey PW, Van Cleave S, and Buttke TM. Lipid hydroperoxides induce apoptosis in T cells displaying a HIV-associated glutathione peroxidase deficiency. J Biol Chem 269: 798-801, 1994.
131. Savill J and Fadok V. Corpse clearance defines the meaning of cell death. Nature 407: 784-788, 2000.
132. Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM, and Haslett C. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest 83: 865-875, 1989.
133. Scavo LM, Ertsey R, Chapin CJ, Allen L, and Kitterman JA. Apoptosis in the development of rat and human fetal lungs. Am J Respir Cell Mol Biol 18: 21-31, 1998.
134. Schittny JC, Djonov V, Fine A, and Burri PH. Programmed cell death contributes to postnatal lung development. Am J Respir Cell Mol Biol 18: 786-793, 1998.
135. Schor NF, Tyurina YY, Fabisiak JP, Tyurin VA, Lazo JS, and Kagan VE. Selective oxidation and externalization of membrane phosphatidylserine: Bcl-2-induced potentiation of the final common pathway for apoptosis. Brain Res 831: 125-130, 1999.
136. Schroit AJ, Madsen JW, and Tanaka Y. In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes. J Biol Chem 260: 5131-5138, 1985.
137. Segura-Valdez L, Pardo A, Gaxiola M, Uhal BD, Becerril C, and Selman M. Upregulation of gelatinases A and B, collagenases 1 and 2, and increased parenchymal cell death in COPD. Chest 117: 684-694, 2000.
138. Serrao KL, Fortenberry JD, Owens ML, Harris FL, and Brown LA. Neutrophils induce apoptosis of lung epithelial cells via release of soluble Fas ligand. Am J Physiol Lung Cell Mol Physiol 280: L298-L305, 2001.
139. Shacter E, Williams JA, Hinson RM, Senturker S, and Lee YJ. Oxidative stress interferes with cancer chemotherapy: inhibition of lymphoma cell apoptosis and phagocytosis. Blood 96: 307-313, 2000.
140. Shidoji Y, Hayashi K, Komura S, Ohishi N, and Yagi K. Loss of molecular interaction between cytochrome c and cardiolipin due to lipid peroxidation. Biochem Biophys Res Commun 264: 343-347, 1999.
141. Shidoji Y, Komura S, Ohishi N, and Yagi K. Interaction between cytochrome c and oxidized mitochondrial lipids. Subcell Biochem 36: 19-37, 2002.
142. Shvedova AA, Tyurina JY, Kawai K, Tyurin VA, Kommineni C, Castranova V, Fabisiak JP, and Kagan VE. Selective peroxidation and externalization of phosphatidylserine in normal human epidermal keratinocytes during oxidative stress induced by cumene hydroperoxide. J Invest Dermatol 118: 1008-1018, 2002.
143. Smith JD, Waelde C, Horwitz A, and Zheng P. Evaluation of the role of phosphatidylserine translocase activity in ABCA1-mediated lipid efflux. J Biol Chem 277: 17797-17803, 2002.
144. Somersan S and Bhardwaj N. Tethering and tickling: a new role for the phosphatidylserine receptor. J Cell Biol 155: 501-504, 2001.
145. Tanaka Y and Schroit AJ. Insertion of fluorescent phosphatidylserine into the plasma membrane of red blood cells. Recognition by autologous macrophages. J Biol Chem 258: 11335-11343, 1983.
146. Tang X, Halleck MS, Schlegel RA, and Williamson P. A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 272: 1495-1497, 1996.
147. Teder P, Vandivier RW, Jiang D, Liang J, Cohn L, Pure E, Henson PM, and Noble PW. Resolution of lung inflammation by CD44. Science 296: 155-158, 2002.
148. Tepper AD, Ruurs P, Wiedmer T, Sims PJ, Borst J, and van Blitterswijk WJ. Sphingomyelin hydrolysis to ceramide during the execution phase of apoptosis results from phospholipid scrambling and alters cell-surface morphology. J Cell Biol 150: 155-164, 2000.
149. Tuominen EK, Wallace CJ, and Kinnunen PK. Phospholipid-cytochrome c interaction: evidence for the extended lipid anchorage. J Biol Chem 277: 8822-8826, 2002.
150. Tyurina YY, Tyurin VA, Liu SX, Smith CA, Shvedova AA, Schor NF, and Kagan VE. Phosphatidylserine peroxidation during apoptosis. A signaling pathway for phagocyte clearance. Subcell Biochem 36: 79-96, 2002.
151. Uhal BD, Joshi I, Hughes WF, Ramos C, Pardo A, and Selman M. Alveolar epithelial cell death adjacent to underlying myofibroblasts in advanced fibrotic human lung. Am J Physiol Lung Cell Mol Physiol 275: L1192-L1199, 1998.
152. Utsugi T, Schroit AJ, Connor J, Bucana CD, and Fidler IJ. Elevated expression of phosphatidylserine in the outer membrane leaflet of human tumor cells and recognition by activated human blood monocytes. Cancer Res 51: 3062-3066, 1991.
153. Van den Eijnde SM, van den Hoff MJ, Reutelingsperger CP, van Heerde WL, Henfling ME, Vermeij-Keers C, Schutte B, Borgers M, and Ramaekers FC. Transient expression of phosphatidylserine at cell-cell contact areas is required for myotube formation. J Cell Sci 114: 3631-3642, 2001.
154. Van Engeland M, Kuijpers HJ, Ramaekers FC, Reutelingsperger CP, and Schutte B. Plasma membrane alterations and cytoskeletal changes in apoptosis. Exp Cell Res 235: 421-430, 1997.
155. Vanags DM, Pörn-Ares MI, Coppola S, Burgess DH, and Orrenius S. Protease involvement in fodrin cleavage and phosphatidylserine exposure in apoptosis. J Biol Chem 271: 31075-31085, 1996.
156. Vandivier RW, Fadok VA, Hoffmann PR, Bratton DL, Penvari C, Brown KK, Brain JD, Accurso FJ, and Henson PM. Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. J Clin Invest 109: 661-670, 2002.
157. Verhoven B, Schlegel RA, and Williamson P. Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J Exp Med 182: 1597-1601, 1995.
158. Wallach D, Varfolomeev EE, Malinin NL, Goltsev YV, Kovalenko AV, and Boldin MP. Tumor necrosis factor receptor and Fas signaling mechanisms. Annu Rev Immunol 17: 331-367, 1999.
159. Ward I, Dransfield I, Chilvers ER, Haslett I, and Rossi AG. Pharmacological manipulation of granulocyte apoptosis: potential therapeutic targets. Trends Pharmacol Sci 20: 503-509, 1999.
160. Williamson P, Christie A, Kohlin T, Schlegel RA, Comfurius P, Harmsma M, Zwaal RF, and Bevers EM. Phospholipid scramblase activation pathways in lymphocytes. Biochemistry 40: 8065-8072, 2001.
161. Zhao J, Zhou Q, Wiedmer T, and Sims PJ. Level of expression of phospholipid scramblase regulates induced movement of phosphatidylserine to the cell surface. J Biol Chem 273: 6603-6606, 1998.
162. Zhou Q, Zhao J, Al-Zoghaibi F, Zhou A, Wiedmer T, Silverman RH, and Sims PJ. Transcriptional control of the human plasma membrane phospholipid scramblase 1 gene is mediated by interferon-alpha. Blood 95: 2593-2599, 2000.
163. Zhou Q, Zhao J, Stout JG, Luhm RA, Wiedmer T, and Sims PJ. Molecular cloning of human plasma membrane phospholipid scramblase. A protein mediating transbilayer movement of plasma membrane phospholipids. J Biol Chem 272: 18240-18244, 1997.
164. Zhou Q, Zhao J, Wiedmer T, and Sims PJ. Normal hemostasis but defective hematopoietic response to growth factors in mice deficient in phospholipid scramblase 1. Blood 99: 4030-4038, 2002.
165. Zhou Z, Hartwieg E, and Horvitz HR. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104: 43-56, 2001.
166. Zhuang J, Ren Y, Snowden RT, Zhu H, Gogvadze V, Savill JS, and Cohen GM. Dissociation of phagocyte recognition of cells undergoing apoptosis from other features of the apoptotic program. J Biol Chem 273: 15628-15632, 1998.
167. Zwaal RFA and Schroit AJ. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 89: 1121-1132, 1997.