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

Journal of Experimental Medicine

Volumn 182, Issue 5, 1995, Pages 1545-1556

  Martin, Seamus J ^a   Reutelingsperger, Chris P M ^b   McGahon, Anne J ^a   Rader, James A ^a   Van Schie, Rob C A A ^c   LaFace, Drake M ^a   Green, Douglas R ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE DERIVATIVE; CYCLOHEXIMIDE; DACTINOMYCIN; DEXAMETHASONE; DNA FRAGMENT; ETOPOSIDE; IMMUNOGLOBULIN M; LIPOSOME; MEMBRANE PHOSPHOLIPID; MONOCLONAL ANTIBODY; PHOSPHATIDIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; SPHINGOMYELIN; STAUROSPORINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL DEATH; CELL MEMBRANE; CONTROLLED STUDY; EXOCYTOSIS; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NEUTROPHIL; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; THYMOCYTE;

ANIMAL; ANNEXIN V; ANTIGENS, CD95; APOPTOSIS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL MARKERS; CARRIER PROTEINS; CELL CYCLE; HUMAN; LEUKEMIA, T-CELL, ACUTE; MEMBRANE GLYCOPROTEINS; MEMBRANE LIPIDS; MEMBRANE PROTEINS; MICE; MODELS, BIOLOGICAL; NEUTROPHILS; P-GLYCOPROTEIN; PHAGOCYTOSIS; PHOSPHATIDYLSERINES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-ABL; PROTO-ONCOGENE PROTEINS C-BCL-2; RECOMBINANT FUSION PROTEINS; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.; THYMUS GLAND; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0028800947     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.182.5.1545     Document Type: Article

References (51)

1. Wyllie, A.H., J.F.R. Kerr, and A.R. Currie. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251-306.
2. Ellis, R.E., J. Yuan, and H.R. Horvitz. 1991. Mechanisms and function of cell death. Annu. Rev. Cell Biol. 7:663-698.
3. Cohen, J.J., R.C. Duke, V.A. Fadok, and K.S. Sellins. 1992. Apoptosis and programmed cell death in immunity. Annu. Rev. Immunol. 10:267-293.
4. Raff, M.C. 1992. Social controls on cell survival and cell death. Nature (Lond.). 356:397-400.
5. Kerr, J.F.R., A.H. Wyllie, and A.R. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br.J. Cancer. 26:239-257.
6. Newman, S.L., J.E. Henson, and P.M. Henson. 1982. Phagocytosis of senescent neutrophils by human monocytederived macrophages and rabbit inflammatory macrophages. J. Exp. Med. 156:430-442.
7. Morris, R.G., A.D. Hargreaves, E. Duval, and A.H. Wyllie. 1984. Hormone-induced death. II. Surface changes in thymocytes undergoing apoptosis. Am.J. Pathol. 115:426-431.
8. Duvall, E., A.H. Wyllie, and R.G. Morris. 1985. Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology. 56:351-358.
9. Savill, J.S., P.M. Henson, and C. Haslett. 1989. Phagocytosis of aged human neutrophils by macrophages is mediated by a novel "charge-sensitive" recognition mechanism. J. Clin. Invest. 84:1518-1527.
10. Savill, J.S., V. Fadok, P. Henson, and C. Haslett. 1993. Phagocyte recognition of cells undergoing apoptosis. Immunol. Today. 14:131-136.
11. Savill, J.S., A.H. Wyllie, J.E. Henson, M.J. Walport, P.M. Henson, and C. Haslett. 1989. 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.
12. Savill, J.S., I. Dransfield, N. Hogg, and C. Haslett. 1990. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature (Lond.). 343:170-173.
13. Savill, J.S., N. Hogg, Y. Ren, and C. Haslett. 1992. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90:1513-1529.
14. Haslett, C., J.S. Savill, M.K.B. Whyte, M. Stem, I. Dransfield, and L.C. Meagher. 1994. Granulocyte apoptosis and the control of inflammation. Philos. Trans. R. Soc. Lond. Ser. B. 345:327-333.
15. Fadok, V.A., D.R. Voelker, P.A. Campbell, J.J. Cohen, D.L. Bratton, and P.M. Henson. 1992. Exposure of phosphati dylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207-2216.
16. Fadok, V.A., J.S. Savill, C. Haslett, D.L. Bratton, D.E. Doherty, P.A. Campbell, and P.M. Henson. 1992. Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J. Immunol. 149:4029-4035.
17. Fadok, V.A., D.J. Laszlo, P.W. Noble, L. Weinstein, D.W.H. Riches, and P.M. Henson. 1993. Particle digestibility is required for induction of the phosphatidylserine recognition mechanism used by murine macrophages to phagocytose apoptotic cells. J. Immunol. 151:4274-4285.
18. Tait, J.F., D. Gibson, and K. Fujikawa. 1989. Phospholipid binding properties of human placental anticoagulant protein 1, a member of the lipocortin family. J. Biol. Chem. 264: 7944-7949.
19. Andree, H.A.M., C.P.M. Reutelingsperger, R. Hauptmann, H.C. Hemker, W.T. Hermens, and G.M. Willems. 1990. Binding of vascular anticoagulant a (VACct) to planar phospholipid bilayers. J. Biol. Chem. 265:4923-4928.
20. Raynal, P., and H.B. Pollard. 1994. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium and phospholipid-binding proteins. Biochim. Biophys. Acta. 1197:63-93.
21. Thiagarajan, P., andJ.F. Tait. 1990. Binding of annexin V/ placental anticoagulant protein I to platelets. Evidence for phosphatidylserine exposure in the procoagulant response of activated platelets. J. Biol. Chem. 265:17420-17423.
22. Reutelingsperger, C.P.M., G. Homstra, and H.C. Hemker. 1985. Isolation and partial purification of a novel anticoagulant from arteries of human umbilical cord. Eur. J. Biochem. 151:625-629.
23. Dachary-Prigent, J., J-.M. Freyssinet, J-.M. Pasquet, J-.C. Carron, and A.T. Nurden. 1993. Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: a flow cytometry study showing a role for free sulfhydryl groups. Blood. 81:2554-2565.
24. Koopman, G., C.P.M. Reutelingsperger, G.A.M. Kuijten, R.M.J. Keehnen, S.T. Pals, and M.H.J. van Oers. 1994. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood. 84:1415-1420.
25. McGahon, A.J., S.J. Martin, R.P. Bissonnette, A. Mahboubi, Y. Shi, R.J. Mogil, W.K. Nishioka, and D.R. Green. 1995. The end of the (cell) line: methods for the study of apoptosis in vitro. Methods Cell Biol. 46:153-185.
26. Darzynkiewicz, Z., S. Bruno, G. Del Bino, W. Gorczca, M.A. Hotz, P. Lassota, and F. Traganos. 1992. Features of apoptotic cells measured by flow cytometry. Cytometry. 13: 795-808.
27. Maurer-Fogy, I., C.P.M. Reutelingsperger, J. Pieters, G. Bodo, C. Statowa, and R. Hauptmann. 1988. Cloning and expression of cDNA for human vascular anticoagulant, a Ca2+ dependent phospholipid binding protein. Eur. J. Biochem. 174:585-592.
28. Martin, S.J., P.M. Matear, and A. Vyakamam. 1994. HIV infection of CD4+ T cells in vitro: differential induction of apoptosis in these cells. J. Immunol. 152:330-342.
29. Yonehara, S., A. Ishii, and M. Yonehara. 1989. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen codownregulated with the receptor of tumor necrosis factor. J. Exp. Med. 169:1747-1756.
30. Suda, T., and S. Nagata. 1994. Purification and characterization of the Fas-ligand that induces apoptosis. J. Exp. Med. 179:873-879.
31. Rouvier, E., M.-F. Luciani, and P. Goldstein. 1993. Fas involvement in Ca2+-independent T cell-mediated cytotoxicityj. Exp. Med. 177:195-200.
32. Ogasawara, J., R. Watanabe-Fukunaga, M. Adachi, A. Matsuzawa, T. Kasugai, Y. Kitamura, N. Itoh, T. Suda, and S. Nagata. 1993. Lethal effect of anti-fas antibody in mice. Nature (Lond.). 364:806-809.
33. Van Meer, G. 1993. Transport and sorting of membrane lipids. Curr. Opin. Cell Biol. 5:661-673.
34. Wyllie, A.H., R.G. Morris, A.L. Smith, and D. Dunlop. 1984. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J. Pathol. 142:67-77.
35. Martin, S.J., S.V. Lennon, A.M. Bonham, and T.G. Cotter. 1990. Induction of apoptosis (programmed cell death) in human leukemic HL-60 cells by inhibition of RNA or protein synthesis. J. Immunol. 145:1859-1867.
36. Martin, S.J., and T.G. Cotter. 1991. Ultraviolet B irradiation of human leukaemia HL-60 cells in vitro induces apoptosis. Int.J. Radiat. Biol. 59:1001-1016.
37. Martin, S.J., G.A, O’Brien, W.K. Nishioka, A.J. McGahon, T. Saido, and D.R. Green. 1995. Proteolysis of Fodrin (nonerythroid spectrin) during apoptosis. J. Biol. Chem. 270:6425-6428.
38. Lennon, S.V., S.J. Martin, and T.G. Cotter. 1991. Dose dependent induction of apoptosis in human tumor cell lines by widely diverging stimuli. Cell Prolif. 24:203-214.
39. Shi, Y., B.M. Sahai, and D.R. Green. 1989. Cyclosporin A inhibits activation-induced cell death in T-cell hybridomas and thymocytes. Nature (Lond.). 339:625-626.
40. Brunner, T., R.J. Mogil, D. LaFace, N.J. Yoo, A. Mahboubi, F. Echeverri, S.J. Martin, W.R. Force, D.H. Lynch, C.F. Ware, and D.R. Green. 1995. Cell autonomous Fas (CD95)/ Fas-ligand interaction mediates activation-induced apoptosis in T cell hybridomas. Nature (Lond.). 373:441-444.
41. Korsmeyer, S.J. 1992. Bcl-2: a repressor oflymphocyte death. Immunol. Today. 13:285-288.
42. McGahon, A.J., T.G. Cotter, and D.R. Green. 1994. The Abl oncogene family and apoptosis. Cell Death Diff. 1:77-83.
43. Hall, S.E., J.S. Savill, P.M. Henson, and C. Haslett. 1994. Apoptotic neutrophils are phagocytosed by fibroblasts with participation of the fibroblast vitronectin receptor and involvement of a mannose/fucose-specific lectin. J. Immunol. 153:3218-3227.
44. Flora, P.K., and C.D. Gregory. 1994. Recognition of apoptotic cells by human macrophages: inhibition by a monocyte/ macrophage-specific monoclonal antibody. Eur. J. Immunol. 24:2625-2632.
45. Kishimoto, H., C.D. Surh, andj. Sprent. 1995. Upregulation of surface markers on dying thymocytes. J. Exp. Med. 181: 649-655.
46. Higgins, C.F. 1994. Flip-flop: the transmembrane translocation of lipids. Cell. 79:393-395.
47. Ruetz, S., and P. Gros. 1994. Phosphatidylcholine translocase: a physiological role for the mdr2 gene. Cell. 77:1071-1081.
48. Sune, A., P. Bette-Bobillo, A. Bienvenue, P. Fellmann, and P.F. Devaux. 1987. Selective outside-inside translocation of aminophospholipids in human placenta. Biochemistry. 26: 2972-2978.
49. Bevers, E.M., R.H.J. Tilly, J.M.G. Senden, P. Comfurius, and R.F.A. Zwall. 1989. Exposure of endogenous phosphati dylserine at the outer surface of stimulated platelets is reversed by restoration of aminophospholipid translocase activity. Biochemistry. 28:2382-2387.
50. Williamson, P., J. Bateman, K. Kozarsky, and K. Mattocks. 1982. Involvement of spectrin in the maintenance of phasestate asymmetry in the erythrocyte membrane. Cell. 30:725-733.
51. Lagasse, E., and I.L. Weissman. 1994. bcl-2 inhibits apoptosis of neutrophils but not their engulfment by macrophages. J. Exp. Med. 179:1047-1052.