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The Journal of Immunology, Vol 148, Issue 7 2207-2216, Copyright © 1992 by American Association of Immunologists

ARTICLES

Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages

VA Fadok, DR Voelker, PA Campbell, JJ Cohen, DL Bratton and PM Henson
Department of Medicine, National Jewish Center for Immunology and Respiratory Medicine, Denver, CO 80206.

During normal tissue remodeling, macrophages remove unwanted cells, including those that have undergone programmed cell death, or apoptosis. This widespread process extends to the deletion of thymocytes (negative selection), in which cells expressing inappropriate Ag receptors undergo apoptosis, and are phagocytosed by thymic macrophages. Although phagocytosis of effete leukocytes by macrophages has been known since the time of Metchnikoff, only recently has it been recognized that apoptosis leads to surface changes that allow recognition and removal of these cells before they are lysed. Our data suggest that macrophages specifically recognize phosphatidylserine that is exposed on the surface of lymphocytes during the development of apoptosis. Macrophage phagocytosis of apoptotic lymphocytes was inhibited, in a dose-dependent manner, by liposomes containing phosphatidyl-L-serine, but not by liposomes containing other anionic phospholipids, including phosphatidyl-D-serine. Phagocytosis of apoptotic lymphocytes was also inhibited by the L isoforms of compounds structurally related to phosphatidylserine, including glycerophosphorylserine and phosphoserine. The membranes of apoptotic lymphocytes bound increased amounts of merocyanine 540 dye relative to those of normal cells, indicating that their membrane lipids were more loosely packed, consistent with a loss of membrane phospholipid asymmetry. Apoptotic lymphocytes were shown to express phosphatidylserine (PS) externally, because PS on their surfaces was accessible to derivatization by fluorescamine, and because apoptotic cells expressed procoagulant activity. These observations suggest that apoptotic lymphocytes lose membrane phospholipid asymmetry and expose phosphatidylserine on the outer leaflet of the plasma membrane. Macrophages then phagocytose apoptotic lymphocytes after specific recognition of the exposed PS.


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 Am. J. Physiol. Cell Physiol.Home page
Y. Cao, S. Adhikari, A. D. Ang, P. K. Moore, and M. Bhatia
Mechanism of induction of pancreatic acinar cell apoptosis by hydrogen sulfide
Am J Physiol Cell Physiol, September 1, 2006; 291(3): C503 - C510.
[Abstract] [Full Text] [PDF]

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 JCBHome page
E. F. Corbett-Nelson, D. Mason, J. G. Marshall, Y. Collette, and S. Grinstein
Signaling-dependent immobilization of acylated proteins in the inner monolayer of the plasma membrane
J. Cell Biol., July 17, 2006; 174(2): 255 - 265.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
D. K. Moss, V. M. Betin, S. D. Malesinski, and J. D. Lane
A novel role for microtubules in apoptotic chromatin dynamics and cellular fragmentation
J. Cell Sci., June 1, 2006; 119(11): 2362 - 2374.
[Abstract] [Full Text] [PDF]

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 J. Leukoc. Biol.Home page
S. J. Gardai, D. L. Bratton, C. A. Ogden, and P. M. Henson
Recognition ligands on apoptotic cells: a perspective
J. Leukoc. Biol., May 1, 2006; 79(5): 896 - 903.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
L. Wang, J. F. Scabilloni, J. M. Antonini, Y. Rojanasakul, V. Castranova, and R. R. Mercer
Induction of secondary apoptosis, inflammation, and lung fibrosis after intratracheal instillation of apoptotic cells in rats
Am J Physiol Lung Cell Mol Physiol, April 1, 2006; 290(4): L695 - L702.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Nakaya, M. Tanaka, Y. Okabe, R. Hanayama, and S. Nagata
Opposite Effects of Rho Family GTPases on Engulfment of Apoptotic Cells by Macrophages
J. Biol. Chem., March 31, 2006; 281(13): 8836 - 8842.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. E. Mitchell, M. Cvetanovic, N. Tibrewal, V. Patel, O. R. Colamonici, M. O. Li, R. A. Flavell, J. S. Levine, R. B. Birge, and D. S. Ucker
The Presumptive Phosphatidylserine Receptor Is Dispensable for Innate Anti-inflammatory Recognition and Clearance of Apoptotic Cells
J. Biol. Chem., March 3, 2006; 281(9): 5718 - 5725.
[Abstract] [Full Text] [PDF]

Home page
 Molecular Cancer TherapeuticsHome page
H. Caldas, F. O. Jaynes, M. W. Boyer, S. Hammond, and R. A. Altura
Survivin and Granzyme B-induced apoptosis, a novel anticancer therapy.
Mol. Cancer Ther., March 1, 2006; 5(3): 693 - 703.
[Abstract] [Full Text] [PDF]

Home page
 Hum ReprodHome page
M. Izawa, T. Harada, I. Deura, F. Taniguchi, T. Iwabe, and N. Terakawa
Drug-induced apoptosis was markedly attenuated in endometriotic stromal cells
Hum. Reprod., March 1, 2006; 21(3): 600 - 604.
[Abstract] [Full Text] [PDF]

Home page
 Arterioscler. Thromb. Vasc. Bio.Home page
R. R. Bach
Tissue Factor Encryption
Arterioscler Thromb Vasc Biol, March 1, 2006; 26(3): 456 - 461.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
J. L. M. Wanderley, M. E. C. Moreira, A. Benjamin, A. C. Bonomo, and M. A. Barcinski
Mimicry of Apoptotic Cells by Exposing Phosphatidylserine Participates in the Establishment of Amastigotes of Leishmania (L) amazonensis in Mammalian Hosts
J. Immunol., February 1, 2006; 176(3): 1834 - 1839.
[Abstract] [Full Text] [PDF]

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 Sci SignalHome page
M. C. Martinez, C. Kunzelmann, and J.-M. Freyssinet
Phosphatidylserine and Signal Transduction: Who Needs Whom?
Sci. Signal., January 17, 2006; 2006(318): pe3 - pe3.
[Abstract] [Full Text] [PDF]

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 Genes Dev.Home page
W.-X. Zong and C. B. Thompson
Necrotic death as a cell fate.
Genes & Dev., January 1, 2006; 20(1): 1 - 15.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Z. Weihua, R. Tsan, A. J. Schroit, and I. J. Fidler
Apoptotic Cells Initiate Endothelial Cell Sprouting via Electrostatic Signaling
Cancer Res., December 15, 2005; 65(24): 11529 - 11535.
[Abstract] [Full Text] [PDF]

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 JNMHome page
H. H. Boersma, B. L.J.H. Kietselaer, L. M.L. Stolk, A. Bennaghmouch, L. Hofstra, J. Narula, G. A.K. Heidendal, and C. P.M. Reutelingsperger
Past, Present, and Future of Annexin A5: From Protein Discovery to Clinical Applications
J. Nucl. Med., December 1, 2005; 46(12): 2035 - 2050.
[Abstract] [Full Text] [PDF]

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 JNMHome page
D. Hartung, M. Sarai, A. Petrov, F. Kolodgie, N. Narula, J. Verjans, R. Virmani, C. Reutelingsperger, L. Hofstra, and J. Narula
Resolution of Apoptosis in Atherosclerotic Plaque by Dietary Modification and Statin Therapy
J. Nucl. Med., December 1, 2005; 46(12): 2051 - 2056.
[Abstract] [Full Text] [PDF]

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 Biol. Bull.Home page
G. A. Blanco, J. Bustamante, M. Garcia, and S. E. Hajos
Hydrogen Peroxide Induces Apoptotic-Like Cell Death in Coelomocytes of Themiste petricola (Sipuncula)
Biol. Bull., December 1, 2005; 209(3): 168 - 183.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
R. Hanayama and S. Nagata
Impaired involution of mammary glands in the absence of milk fat globule EGF factor 8
PNAS, November 15, 2005; 102(46): 16886 - 16891.
[Abstract] [Full Text] [PDF]

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 Anesth. Analg.Home page
T. Ohara, T. Itoh, and M. Takahashi
Immunosuppression by Morphine-Induced Lymphocyte Apoptosis: Is It a Real Issue?
Anesth. Analg., October 1, 2005; 101(4): 1117 - 1122.
[Abstract] [Full Text] [PDF]

Home page
 J. Immunol.Home page
L. Frisoni, L. Mcphie, L. Colonna, U. Sriram, M. Monestier, S. Gallucci, and R. Caricchio
Nuclear Autoantigen Translocation and Autoantibody Opsonization Lead to Increased Dendritic Cell Phagocytosis and Presentation of Nuclear Antigens: A Novel Pathogenic Pathway for Autoimmunity?
J. Immunol., August 15, 2005; 175(4): 2692 - 2701.
[Abstract] [Full Text] [PDF]

Home page
 Molecular Cancer TherapeuticsHome page
C. Plasencia, R. Dayam, Q. Wang, J. Pinski, T. R. Burke Jr., D. I. Quinn, and N. Neamati
Discovery and preclinical evaluation of a novel class of small-molecule compounds in hormone-dependent and -independent cancer cell lines
Mol. Cancer Ther., July 1, 2005; 4(7): 1105 - 1113.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
U. Wellmann, M. Letz, M. Herrmann, S. Angermuller, J. R. Kalden, and T. H. Winkler
The evolution of human anti-double-stranded DNA autoantibodies
PNAS, June 28, 2005; 102(26): 9258 - 9263.
[Abstract] [Full Text] [PDF]

Home page
 Infect. Immun.Home page
D. R. Boettner, C. D. Huston, J. A. Sullivan, and W. A. Petri Jr.
Entamoeba histolytica and Entamoeba dispar Utilize Externalized Phosphatidylserine for Recognition and Phagocytosis of Erythrocytes
Infect. Immun., June 1, 2005; 73(6): 3422 - 3430.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
Z. Medarova, S. Bonner-Weir, M. Lipes, and A. Moore
Imaging {beta}-Cell Death With a Near-Infrared Probe
Diabetes, June 1, 2005; 54(6): 1780 - 1788.
[Abstract] [Full Text] [PDF]

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 Vasc MedHome page
S Soumian, C Albrecht, A. Davies, and R. Gibbs
ABCA1 and atherosclerosis
Vascular Medicine, May 1, 2005; 10(2): 109 - 119.
[Abstract] [PDF]

Home page
 JNMHome page
J. F. Tait, C. Smith, and F. G. Blankenberg
Structural Requirements for In Vivo Detection of Cell Death with 99mTc-Annexin V
J. Nucl. Med., May 1, 2005; 46(5): 807 - 815.
[Abstract] [Full Text] [PDF]

Home page
 Infect. Immun.Home page
S. L. Fink and B. T. Cookson
Apoptosis, Pyroptosis, and Necrosis: Mechanistic Description of Dead and Dying Eukaryotic Cells
Infect. Immun., April 1, 2005; 73(4): 1907 - 1916.
[Full Text] [PDF]

Home page
 Mol. Biol. CellHome page
G. B. John, Y. Shang, L. Li, C. Renken, C. A. Mannella, J. M.L. Selker, L. Rangell, M. J. Bennett, and J. Zha
The Mitochondrial Inner Membrane Protein Mitofilin Controls Cristae Morphology
Mol. Biol. Cell, March 1, 2005; 16(3): 1543 - 1554.
[Abstract] [Full Text] [PDF]

Home page
 J. Immunol.Home page
P. R. Hoffmann, J. A. Kench, A. Vondracek, E. Kruk, D. L. Daleke, M. Jordan, P. Marrack, P. M. Henson, and V. A. Fadok
Interaction between Phosphatidylserine and the Phosphatidylserine Receptor Inhibits Immune Responses In Vivo
J. Immunol., February 1, 2005; 174(3): 1393 - 1404.
[Abstract] [Full Text] [PDF]

Home page
 Physiol. GenomicsHome page
K. Kwong, R. A. Vaishnav, Y. Liu, N. Subhedar, A. J. Stromberg, M. L. Getchell, and T. V. Getchell
Target ablation-induced regulation of macrophage recruitment into the olfactory epithelium of Mip-1{alpha}-/- mice and restoration of function by exogenous MIP-1{alpha}
Physiol Genomics, December 15, 2004; 20(1): 73 - 86.
[Abstract] [Full Text] [PDF]

Home page
 J. Immunol.Home page
S. D. Fleming, R. P. Egan, C. Chai, G. Girardi, V. M. Holers, J. Salmon, M. Monestier, and G. C. Tsokos
Anti-Phospholipid Antibodies Restore Mesenteric Ischemia/Reperfusion-Induced Injury in Complement Receptor 2/Complement Receptor 1-Deficient Mice
J. Immunol., December 1, 2004; 173(11): 7055 - 7061.
[Abstract] [Full Text] [PDF]


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