Programmed cell death of erythrocyte, an apoptotic phenomenon. Impact on blood transfusion

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?
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
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cell death by caspase family proteinases. J Biol
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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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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
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Gardner R.T., Raff K.D., Raff M.C., Constitutive
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