Programmed cell death of erythrocyte, an apoptotic phenomenon. Impact on blood transfusion
September 17, 2011
Programmed cell death of erythrocyte, an apoptotic phenomenon. Impact on blood transfusion
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Title: | Programmed cell death of erythrocyte, an apoptotic phenomenon. Impact on blood transfusion |
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Article_Title: | Programmed cell death of erythrocyte, an apoptotic phenomenon. Impact on blood transfusion |
Authors: | Bratosin Daniela, Coralia Cotoraci, Jerome Estaquier |
Affiliation: | 1 National Institute for Biological Science Research and Development, Bucharest, Romania 2 Vasile Goldis “Western University of Arad, Faculty of Biology, Arad, Romania 3 Vasile Goldis” Western University of Arad, Faculty of Medicine, Arad, Romania 4 Unité INSERM U 841, Créteil Henri Mondor, Créteil, France |
Abstract: | Human red blood cells are terminally differentiated cells of the erythroid lineage that are devoid of organelles and have a definite life span of 120 days that is ended by a process of senescence leading to their clearance from the circulation (Bratosin D. et al.,1998). Every day, 360 billions of RBCs are phagocytized, ie 5 millions per second. This fascinating phenomenon of programmed cell death (PCD) raises the following questions: i) what signals the death sentence of RBCs; ii) what are the physiological mechanisms for sequestration of the effete RBDs from the blood stream with such precision? and iii) by what specific membrane signal(s) do the reticulo-endothelial cells distinguish between the truly senescent RBCs and others? |
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References: | Aiken N.C., Satterlee J.D., Galey W.R., Measurement o intracellular Ca2+ in young and old human erythrocytes using 19F-NMR spectroscopy, Biochim. Biophys. Acta, 113, 155, 1992 Allen T.M., Williamson P., Schlegel R.A., Phosphatidylserine as a determinant of reticuloendithelial recognition of liposome models of the erythrocyte surface, Proc. Natl. Acad. Sci. USA, 8067, 1988 Ameisen J.C., The origin of programmed cell death, Science, 272, 1278, 1996 Ameisen J.C., The evolutionary origin and role of programmed cell death in single celled organisms: a new view of executioners, mitochondria, host pathogen interactions, and the role of death in the process of natural selection., In When cells die, Lockshin R., Zakeri Z. and Tilly J., eds (Wiley-Liss, Inc., New York) pp. 3, 1998 Aminoff D., The role of sialoglycoconjugates in the aging and sequestration of red cells from circulation, Blood Cells, 14, 229, 1988 Berg C.P., Engels I.H., Rothbart A., Lauber K., Renz A., Schlosser S.F., Schulze-Osthoff K., Wesselborg S. Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis. Cell Death Differ, 8:1197– 1206, 2001 Bessis M., Généralités sur la senescence et la mort des cellules du sang., In: Cellules du sang normal et pathologique (Bessis M.éd.) Masson, Paris, 188, 1972 Beutler E., Back to the future in RBC preservation, Transfusion, 40:893-895, 2001 Boas F.E., Forman L., Beutler E., Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia, Proc. Natl. Acad. Sci. USA, 95, 3077, 1998 Bratosin D., Mazurier J., Debray H., Lecocq M., Boilly B., Alonso C., Moisei M., Motaş C., Montreuil J., Flow cytofluorimetric analysis of young and senescent human erythrocytes probed with lectins. Evidence that sialic acids control their life span, Glycoconjugate Journal, 12, 258, 1995 Bratosin D., Mazurier J., Tissier J-P., Slomianny C., Estaquier J., Russo-Marie F., Huart J-J., Freyssinet J.M., Aminoff D., Ameisen J.C., Montreuil J., Molecular mechanism of erythrophagocytosis. Characterization of senescent erythrocytes that are phagocytized by macrophages, C. R. Acad. Sci., Paris, Sciences de la vie, 320 , 811, 1997 Bratosin D., Mazurier J., Slomianny C., Aminoff D., Montreuil J., Molecular mechanism of erythrophagocytosis: Flow cytometric quantitation of in vitro erythrocyte phagocytoses by macrophages, Cytometry, 30, 269, 1997 Bratosin D., Mazurier J., Tissier J-P., Estaquier J., Huart J-J., Aminoff D., Montreuil J., Cellular and molecular mechanism of senescent erythrocyte phagocytosis by macrophages. A review, Biochimie, 80, 173, 1998 Bratosin D., Estaquier J., Petit F., Tissier J-P., Trandaburu I., Huart J-J., Ameisen J.C., Montreuil J., Molecular and cellular mechanisms of erythrocyte cell death. An apoptotic phenomenon, Biochimie, 6, S 361, 1999 Bratosin D., Estaquier J., Petit F., Arnoult D., Quatannens B., Tissier J-P., Slomianny C., Sartiaux C., Alonso C., Huart J-J., Montreuil J., Ameisen J.C. , Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria, Cell Death and Differentiation, 8 , 1143, 2001 Bratosin D., Estaquier J., Petit F., Arnoult D., Quatannens B., Tissier J.P., Slomianny C., Sartiaux C., Alonso C., Huart J.J., Montreuil J., Ameisen J.C., Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria. Cell Death Differ, 8:1143–1156, 2001 Bratosin D., Leszczynski S., Sartiaux C., Fontaine O., Descamps J., Huart J. J., Poplineau J., Goudaliez F., Aminoff D., Montreuil J., Improved storage of erythrocytes by prior leukodepletion : Flow cytometric evaluation of stored erythrocytes, Cytometry, 46:351-356, 2001 Bratosin D., Mitrofan L., Palii C., Estaquier J., Montreuil J., A novel fluorescence assay for determination of human erythrocyte viability using Calcein-AM and flow cytometry. Cytometry A, 66A: 78-84, 2005 Bratosin D., Tcacenco L., Sidoroff M., Cotoraci C., Slomianny C., Estaquier J., Montreuil J., Active caspases – 8 and -3 in circulating human erythrocytes purified on immobilized annexin-V. A cytometric demonstration, Cytometry Part A, 75A: 236-244, 2009 Clark M.R., Senescence of red blood cells: progress and problems, Physiol. Rev., 68, 503, 1998 Connor J., Pak C.C., Schroit A. J., Exposure of phosphatidylserine in the outer leaflet of human red blood cells. Relationship to cell density, cell age and clearance by mononuclear cells, J. Biol. Chem., 269, 2399, 1994 Daugas E., Cande C., Kroemer G., Erythrocytes: Death of a mummy, Cell Death Differ., 8, 1131, 2001 Desagher S., Martinou J.C., Mitochondria as the central control point of apoptosis, Trends Cell Biol., 10, 369, 2000 Diaz C., Morkowski J., Schroit A.J., Generation of phenotypically aged phosphatidylserine expressing erythrocytes by dilauroyl phosphatidylcholine induced vesiculisation, Blood 87, 2956, 1996 Earnshaw W.C., Martins L.M., Kaufmann S.H., Mammalian caspases: structure, activation, substrates, and functions during apoptosis, Annu. Rev Biochem., 68, 383, 1999 Fibach E., Sharon R., Changes in ABH antigen expression on red cells during in vivo aging: a flow cytometric Madsen J., Tanaka Y., In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes, J. Biol. Chem., 260, 5131, 1985 Gilmore AP. Anoikis. Cell Death Differ; Suppl. 2:1473- 1477, 2005 Green D. R., J.C., Mitochondria and apoptosis, Science, 281,1309, 1998 Green D.R., Apoptotic pathways: Paper wraps stone blunt scissors, Cell, 102, 1, 2000 Grossmann J. Molecular mechanisms of detachmentinduced apoptosis. Anoikis. Apoptosis, 7:247-260, 2002 Hengartner M., The biochemistry of apoptosis, Nature, 407, 770, 2000 Jacobson M.D., Weil M., Raff M.C., Programmed cell death in animal development, Cell, 88, 347, 1997 Kriebardis A.G., Antonelou M.H., Stamoulis K.E., Economou-Petersen E., Margaritis L.H., Papassideri I.S., Storage-dependent remodeling of the red blood cell membrane is associated with increased immunoglobulin G binding, lipid raft rearrangement, and caspase activation. Transfusion, 47:1212-1220, 2007 Kroemer G., Reed J., Mitochondrial control of cell death, Nature Med., 6, 513, 2000 Lutz H.U., Stammer P., Fasler S., Ingold M., Fehr J., Density separation of human red blood cells on selfforming Percoll gradient. Correlation with cell age, Biochim. Biophys. Acta, analysis, Transfusion, 34, 328, 1994 Mandal D., Moitra P.K., Saha S., Basu J. Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes. FEBS Lett, 513:184-188, 2002 Mandal D., Baudin-Creuza V., Bhattacharyya A., Pathak S., Delaunay J., Kundu M., Basu J., Caspase 3-mediated proteolysis of the N-terminal cytoplasmic domain of the human erythroid anion exchanger 1 (band 3). J Biol Chem, 278:52551- 52558, 2003 Mandal D., Mazumder A., Das P., Kundu M., Basu J., Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J Biol Chem., 280:39460- 39467, 2005 Martinou J.C., Green D., Breaking the mitochondrial barrier, Nature Rev. Mol. Cell Biol., 2, 63, 2001 Mc Evoy L., Williamson P., Schlegel R.A., Membrane phospholipids asymmetry as a determinant of erythrocyte recognition by macrophages, Proc. Natl. Acad. Sci. USA, 83, 3311, 1986 Meier P., Finch A., Evan G., Apoptosis in development., Nature, 407, 796, 2000 Michetti M., Salamino F., Minafra R., Melloni E., Pontremoli S., Calcium binding properties of human erythrocyte calpain., Biochem. J., 325, 721, 1997 Mukherjee K., Chowdhury S., Mondal S., Mandal C., Chandra S., Bhadra R.K., Mandal C., 9-O-acetylated GD3 triggers programmed cell death in mature erythrocytes. Biochem Biophys Res Commun, 362: 651-657, 2007 Nagata S., Apoptotic DNA fragmentation, Exp. Cell Res., 256, 12, 2000 Pietraforte D., Matarrese P., Straface E., Gambardella L., Metere A., Scorza G., Leto T.L., Malorni W., Minetti M., Two different pathways are involved in peroxynitrite-induced senescence and apoptosis of human erythrocytes. Free Radic Biol Med., 42:202- 214, 2007 Raff M.C., Social controls on cell survival and cell death., Nature 356, 397, 1992 Romero P.J., Romero E.A., Effect of cell ageing on Ca2+ influx into human red cells, Cell Calcium, 26, 131, 1999 Romero P.J., Romero E.A., Effect of cell ageing on Ca2+ influx into human red cells. Cell Calcium, 26:131- 137, 1999 Sahara S., Aoto M., Eguchi Y., Imamoto N., Yoneda Y. Tsujimoto Y., Acinus is a caspase-3-activated protein required for apoptotic chromatin condensation. Nature, 401, 168, 1999 Sharon R., Fibach E., Quantitative flow cytometry analysis of ABO red cell antigens, Cytometry, 12, 545, 1991 Savill J., Fadok V., Corpse clearance defines the meaning of cell death, Nature, 407, 784, 2000 Schroit A.J., 1116, 1, 1992 Shiga T., Sekiya M., Maeda N., Kon K., Okazaki M., Cell age-dependent changes in deformability and calcium accumulation of human erythrocytes. Biochim Biophys Acta, 814:289-299, 1985 Shinozuka T., Takei S., Yanagida J., Watanabe H., Ohkuma S., Binding of lectins to “young” and “old” human erythrocytes, Blut, 57,117, 1998 Siegel R.M., Martin D.A., Zheng L., Ng S.Y., Bertin J., Cohen J., Lenardo M.J., Death-effector filaments: novel cytoplasmic structures that recruit caspases and trigger apoptosis. J Cell Biol., 141:1243-1253, 1998 Sperandio S., de Belle I., Bredesen D., An alternative non apoptotic form of programmed cell death, Proc. Natl. Acad. Sci. USA, 97, 14376, 2000 Squier M.K.T., Cohen J.J., Calpain and cell death, Cell Death Differ., 3, 275, 1996 Thornberry N. A., Lazebnik Y., Caspases: enemies within, Science, 281, 1312, 1998 Wang K.K.W., Calpain and caspases: can you tell the difference?, Trends Neurosci. 23, 20, 2000 Weil M., Jacobson M.D., Coles H.S.R., Davies T.J., Gardner R.T., Raff K.D., Raff M.C., Constitutive expression of the machinery for programmed cell death, J. Cell Biol., 133, 1053, 1996 White S.R., Williams P., Wojcik K.R., Sun S., Hiemstra PS, Rabe KF, Dorscheid DR. Initiation of apoptosis by actin cytoskeletal derangement in human airway epithelial cells. Am J Respir Cell Mol Biol., 24:282- 294, 2001 Wolf B.B., Green D.R., Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem., 274:20049-20052, 1999 Wyllie A.H., Golstein P., More than one way to go, Proc. Natl. Acad. Sci.USA, 98, 11, 2001 Zamzami N., Kroemer G., The mitochondrion in apoptosis: how Pandora’s box opens, Nature Rev. Mol. Cell Biol., 2, 67, 2001 Zermati Y., Garrido C., Amsellem S., Fishelson S., Bouscary D., Valensi F., Varet B.., Solary E., Hermine O., Caspase activation is required for terminal erythroid differentiation, J. Exp. Med., 193, 247, 2001 Zermati Y, Garrido C, Amsellem S, Fishelson S, Bouscary D, Valensi F, Varet B, Solary E and Hermine O. Caspase activation is required for terminal erythroid differentiation. J Exp Med,193: 247 -254, 2001 Zwaal R.F.A., Schroit A.J., Pathophysiologic implications of membrane phospholipid asymmetry in blood cells, Blood, 89, 1121, 1997 |
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Correspondence: | Bratosin D |
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Article Title: | Programmed cell death of erythrocyte, an apoptotic phenomenon. Impact on blood transfusion |
Authors: | Bratosin Daniela 1,2, Coralia Cotoraci 3, Jerome Estaquier 4 |
Affiliation: | 1 National Institute for Biological Science Research and Development, Bucharest, Romania 2 Vasile Goldis “Western University of Arad, Faculty of Biology, Arad, Romania 3 Vasile Goldis” Western University of Arad, Faculty of Medicine, Arad, Romania 4 Unité INSERM U 841, Créteil Henri Mondor, Créteil, France |
Abstract: | Human red blood cells are terminally differentiated cells of the erythroid lineage that are devoid of organelles and have a definite life span of 120 days that is ended by a process of senescence leading to their clearance from the circulation (Bratosin D. et al.,1998). Every day, 360 billions of RBCs are phagocytized, ie 5 millions per second. This fascinating phenomenon of programmed cell death (PCD) raises the following questions: i) what signals the death sentence of RBCs; ii) what are the physiological mechanisms for sequestration of the effete RBDs from the blood stream with such precision? and iii) by what specific membrane signal(s) do the reticulo-endothelial cells distinguish between the truly senescent RBCs and others? |
Keywords: | |
References: | Aiken N.C., Satterlee J.D., Galey W.R., Measurement o intracellular Ca2+ in young and old human erythrocytes using 19F-NMR spectroscopy, Biochim. Biophys. Acta, 113, 155, 1992 Allen T.M., Williamson P., Schlegel R.A., Phosphatidylserine as a determinant of reticuloendithelial recognition of liposome models of the erythrocyte surface, Proc. Natl. Acad. Sci. USA, 8067, 1988 Ameisen J.C., The origin of programmed cell death, Science, 272, 1278, 1996 Ameisen J.C., The evolutionary origin and role of programmed cell death in single celled organisms: a new view of executioners, mitochondria, host pathogen interactions, and the role of death in the process of natural selection., In When cells die, Lockshin R., Zakeri Z. and Tilly J., eds (Wiley-Liss, Inc., New York) pp. 3, 1998 Aminoff D., The role of sialoglycoconjugates in the aging and sequestration of red cells from circulation, Blood Cells, 14, 229, 1988 Berg C.P., Engels I.H., Rothbart A., Lauber K., Renz A., Schlosser S.F., Schulze-Osthoff K., Wesselborg S. Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis. Cell Death Differ, 8:1197– 1206, 2001 Bessis M., Généralités sur la senescence et la mort des cellules du sang., In: Cellules du sang normal et pathologique (Bessis M.éd.) Masson, Paris, 188, 1972 Beutler E., Back to the future in RBC preservation, Transfusion, 40:893-895, 2001 Boas F.E., Forman L., Beutler E., Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia, Proc. Natl. Acad. Sci. USA, 95, 3077, 1998 Bratosin D., Mazurier J., Debray H., Lecocq M., Boilly B., Alonso C., Moisei M., Motaş C., Montreuil J., Flow cytofluorimetric analysis of young and senescent human erythrocytes probed with lectins. Evidence that sialic acids control their life span, Glycoconjugate Journal, 12, 258, 1995 Bratosin D., Mazurier J., Tissier J-P., Slomianny C., Estaquier J., Russo-Marie F., Huart J-J., Freyssinet J.M., Aminoff D., Ameisen J.C., Montreuil J., Molecular mechanism of erythrophagocytosis. Characterization of senescent erythrocytes that are phagocytized by macrophages, C. R. Acad. Sci., Paris, Sciences de la vie, 320 , 811, 1997 Bratosin D., Mazurier J., Slomianny C., Aminoff D., Montreuil J., Molecular mechanism of erythrophagocytosis: Flow cytometric quantitation of in vitro erythrocyte phagocytoses by macrophages, Cytometry, 30, 269, 1997 Bratosin D., Mazurier J., Tissier J-P., Estaquier J., Huart J-J., Aminoff D., Montreuil J., Cellular and molecular mechanism of senescent erythrocyte phagocytosis by macrophages. A review, Biochimie, 80, 173, 1998 Bratosin D., Estaquier J., Petit F., Tissier J-P., Trandaburu I., Huart J-J., Ameisen J.C., Montreuil J., Molecular and cellular mechanisms of erythrocyte cell death. An apoptotic phenomenon, Biochimie, 6, S 361, 1999 Bratosin D., Estaquier J., Petit F., Arnoult D., Quatannens B., Tissier J-P., Slomianny C., Sartiaux C., Alonso C., Huart J-J., Montreuil J., Ameisen J.C. , Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria, Cell Death and Differentiation, 8 , 1143, 2001 Bratosin D., Estaquier J., Petit F., Arnoult D., Quatannens B., Tissier J.P., Slomianny C., Sartiaux C., Alonso C., Huart J.J., Montreuil J., Ameisen J.C., Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria. Cell Death Differ, 8:1143–1156, 2001 Bratosin D., Leszczynski S., Sartiaux C., Fontaine O., Descamps J., Huart J. J., Poplineau J., Goudaliez F., Aminoff D., Montreuil J., Improved storage of erythrocytes by prior leukodepletion : Flow cytometric evaluation of stored erythrocytes, Cytometry, 46:351-356, 2001 Bratosin D., Mitrofan L., Palii C., Estaquier J., Montreuil J., A novel fluorescence assay for determination of human erythrocyte viability using Calcein-AM and flow cytometry. Cytometry A, 66A: 78-84, 2005 Bratosin D., Tcacenco L., Sidoroff M., Cotoraci C., Slomianny C., Estaquier J., Montreuil J., Active caspases – 8 and -3 in circulating human erythrocytes purified on immobilized annexin-V. A cytometric demonstration, Cytometry Part A, 75A: 236-244, 2009 Clark M.R., Senescence of red blood cells: progress and problems, Physiol. Rev., 68, 503, 1998 Connor J., Pak C.C., Schroit A. J., Exposure of phosphatidylserine in the outer leaflet of human red blood cells. Relationship to cell density, cell age and clearance by mononuclear cells, J. Biol. Chem., 269, 2399, 1994 Daugas E., Cande C., Kroemer G., Erythrocytes: Death of a mummy, Cell Death Differ., 8, 1131, 2001 Desagher S., Martinou J.C., Mitochondria as the central control point of apoptosis, Trends Cell Biol., 10, 369, 2000 Diaz C., Morkowski J., Schroit A.J., Generation of phenotypically aged phosphatidylserine expressing erythrocytes by dilauroyl phosphatidylcholine induced vesiculisation, Blood 87, 2956, 1996 Earnshaw W.C., Martins L.M., Kaufmann S.H., Mammalian caspases: structure, activation, substrates, and functions during apoptosis, Annu. Rev Biochem., 68, 383, 1999 Fibach E., Sharon R., Changes in ABH antigen expression on red cells during in vivo aging: a flow cytometric Madsen J., Tanaka Y., In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes, J. Biol. Chem., 260, 5131, 1985 Gilmore AP. Anoikis. Cell Death Differ; Suppl. 2:1473- 1477, 2005 Green D. R., J.C., Mitochondria and apoptosis, Science, 281,1309, 1998 Green D.R., Apoptotic pathways: Paper wraps stone blunt scissors, Cell, 102, 1, 2000 Grossmann J. Molecular mechanisms of detachmentinduced apoptosis. Anoikis. Apoptosis, 7:247-260, 2002 Hengartner M., The biochemistry of apoptosis, Nature, 407, 770, 2000 Jacobson M.D., Weil M., Raff M.C., Programmed cell death in animal development, Cell, 88, 347, 1997 Kriebardis A.G., Antonelou M.H., Stamoulis K.E., Economou-Petersen E., Margaritis L.H., Papassideri I.S., Storage-dependent remodeling of the red blood cell membrane is associated with increased immunoglobulin G binding, lipid raft rearrangement, and caspase activation. Transfusion, 47:1212-1220, 2007 Kroemer G., Reed J., Mitochondrial control of cell death, Nature Med., 6, 513, 2000 Lutz H.U., Stammer P., Fasler S., Ingold M., Fehr J., Density separation of human red blood cells on selfforming Percoll gradient. Correlation with cell age, Biochim. Biophys. Acta, analysis, Transfusion, 34, 328, 1994 Mandal D., Moitra P.K., Saha S., Basu J. Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes. FEBS Lett, 513:184-188, 2002 Mandal D., Baudin-Creuza V., Bhattacharyya A., Pathak S., Delaunay J., Kundu M., Basu J., Caspase 3-mediated proteolysis of the N-terminal cytoplasmic domain of the human erythroid anion exchanger 1 (band 3). J Biol Chem, 278:52551- 52558, 2003 Mandal D., Mazumder A., Das P., Kundu M., Basu J., Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J Biol Chem., 280:39460- 39467, 2005 Martinou J.C., Green D., Breaking the mitochondrial barrier, Nature Rev. Mol. Cell Biol., 2, 63, 2001 Mc Evoy L., Williamson P., Schlegel R.A., Membrane phospholipids asymmetry as a determinant of erythrocyte recognition by macrophages, Proc. Natl. Acad. Sci. USA, 83, 3311, 1986 Meier P., Finch A., Evan G., Apoptosis in development., Nature, 407, 796, 2000 Michetti M., Salamino F., Minafra R., Melloni E., Pontremoli S., Calcium binding properties of human erythrocyte calpain., Biochem. J., 325, 721, 1997 Mukherjee K., Chowdhury S., Mondal S., Mandal C., Chandra S., Bhadra R.K., Mandal C., 9-O-acetylated GD3 triggers programmed cell death in mature erythrocytes. Biochem Biophys Res Commun, 362: 651-657, 2007 Nagata S., Apoptotic DNA fragmentation, Exp. Cell Res., 256, 12, 2000 Pietraforte D., Matarrese P., Straface E., Gambardella L., Metere A., Scorza G., Leto T.L., Malorni W., Minetti M., Two different pathways are involved in peroxynitrite-induced senescence and apoptosis of human erythrocytes. Free Radic Biol Med., 42:202- 214, 2007 Raff M.C., Social controls on cell survival and cell death., Nature 356, 397, 1992 Romero P.J., Romero E.A., Effect of cell ageing on Ca2+ influx into human red cells, Cell Calcium, 26, 131, 1999 Romero P.J., Romero E.A., Effect of cell ageing on Ca2+ influx into human red cells. Cell Calcium, 26:131- 137, 1999 Sahara S., Aoto M., Eguchi Y., Imamoto N., Yoneda Y. Tsujimoto Y., Acinus is a caspase-3-activated protein required for apoptotic chromatin condensation. Nature, 401, 168, 1999 Sharon R., Fibach E., Quantitative flow cytometry analysis of ABO red cell antigens, Cytometry, 12, 545, 1991 Savill J., Fadok V., Corpse clearance defines the meaning of cell death, Nature, 407, 784, 2000 Schroit A.J., 1116, 1, 1992 Shiga T., Sekiya M., Maeda N., Kon K., Okazaki M., Cell age-dependent changes in deformability and calcium accumulation of human erythrocytes. Biochim Biophys Acta, 814:289-299, 1985 Shinozuka T., Takei S., Yanagida J., Watanabe H., Ohkuma S., Binding of lectins to “young” and “old” human erythrocytes, Blut, 57,117, 1998 Siegel R.M., Martin D.A., Zheng L., Ng S.Y., Bertin J., Cohen J., Lenardo M.J., Death-effector filaments: novel cytoplasmic structures that recruit caspases and trigger apoptosis. J Cell Biol., 141:1243-1253, 1998 Sperandio S., de Belle I., Bredesen D., An alternative non apoptotic form of programmed cell death, Proc. Natl. Acad. Sci. USA, 97, 14376, 2000 Squier M.K.T., Cohen J.J., Calpain and cell death, Cell Death Differ., 3, 275, 1996 Thornberry N. A., Lazebnik Y., Caspases: enemies within, Science, 281, 1312, 1998 Wang K.K.W., Calpain and caspases: can you tell the difference?, Trends Neurosci. 23, 20, 2000 Weil M., Jacobson M.D., Coles H.S.R., Davies T.J., Gardner R.T., Raff K.D., Raff M.C., Constitutive expression of the machinery for programmed cell death, J. Cell Biol., 133, 1053, 1996 White S.R., Williams P., Wojcik K.R., Sun S., Hiemstra PS, Rabe KF, Dorscheid DR. Initiation of apoptosis by actin cytoskeletal derangement in human airway epithelial cells. Am J Respir Cell Mol Biol., 24:282- 294, 2001 Wolf B.B., Green D.R., Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem., 274:20049-20052, 1999 Wyllie A.H., Golstein P., More than one way to go, Proc. Natl. Acad. Sci.USA, 98, 11, 2001 Zamzami N., Kroemer G., The mitochondrion in apoptosis: how Pandora’s box opens, Nature Rev. Mol. Cell Biol., 2, 67, 2001 Zermati Y., Garrido C., Amsellem S., Fishelson S., Bouscary D., Valensi F., Varet B.., Solary E., Hermine O., Caspase activation is required for terminal erythroid differentiation, J. Exp. Med., 193, 247, 2001 Zermati Y, Garrido C, Amsellem S, Fishelson S, Bouscary D, Valensi F, Varet B, Solary E and Hermine O. Caspase activation is required for terminal erythroid differentiation. J Exp Med,193: 247 -254, 2001 Zwaal R.F.A., Schroit A.J., Pathophysiologic implications of membrane phospholipid asymmetry in blood cells, Blood, 89, 1121, 1997 |
*Correspondence: | Bratosin D |