Cited by 447

The DOI matches its Crossref record; 297 of the 297 references it cites were found in a registry or an index.

Getting to the Outer Leaflet: Physiology of Phosphatidylserine Exposure at the Plasma Membrane

Bevers, Edouard M., Williamson, Patrick L.·2016·Physiological Reviews

DOI 10.1152/physrev.00020.2015

Open this paper in CoChat — free account

Abstract

Phosphatidylserine (PS) is a major component of membrane bilayers whose change in distribution between inner and outer leaflets is an important physiological signal. Normally, members of the type IV P-type ATPases spend metabolic energy to create an asymmetric distribution of phospholipids between the two leaflets, with PS confined to the cytoplasmic membrane leaflet. On occasion, membrane enzymes, known as scramblases, are activated to facilitate transbilayer migration of lipids, including PS. Recently, two proteins required for such randomization have been identified: TMEM16F, a scramblase regulated by elevated intracellular Ca 2+, and XKR8, a caspase-sensitive protein required for PS exposure in apoptotic cells. Once exposed at the cell surface, PS regulates biochemical reactions involved in blood coagulation, and bone mineralization, and also regulates a variety of cell-cell interactions. Exposed on the surface of apoptotic cells, PS controls their recognition and engulfment by other cells. This process is exploited by parasites to invade their host, and in specialized form is used to maintain photoreceptors in the eye and modify synaptic connections in the brain. This review discusses what is known about the mechanism of PS exposure at the surface of the plasma membrane of cells, how actors in the extracellular milieu sense surface exposed PS, and how this recognition is translated to downstream consequences of PS exposure.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1152/physrev.00020.2015

Cites

297 of 297 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

1 retracted

Items 201–297 of 297

Molecular Determinants of Phospholipid Synergy in Blood Clotting
Tavoosi, N., Davis-Harrison, R. L., Pogorelov, T. V., Ohkubo, Y. Z., Arcario, M. J., Clay, M. C., Rienstra, C. M., Tajkhorshid, E., & Morrissey, J. H. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.251769 · Cited by 123
Mystery of the transformation from amorphous calcium phosphate to hydroxyapatite
Pan, H., Liu, X., Tang, R., & Xu, H. Y. (2010) · Chemical Communications · doi:10.1039/c0cc00971g · Cited by 120
Caenorhabditis elegans transthyretin-like protein TTR-52 mediates recognition of apoptotic cells by the CED-1 phagocyte receptor
Wang, X., Li, W., Zhao, D., Liu, B., Shi, Y., Chen, B., Yang, H., Guo, P., Geng, X., Shang, Z., et al. (2010) · Nature Cell Biology · doi:10.1038/ncb2068 · Cited by 120
Phospholipid Scramblase Activation Pathways in Lymphocytes
Williamson, P., Christie, A. J., Kohlin, T., Schlegel, R., Comfurius, P., Harmsma, M., Zwaal, R. F. A., & Bevers, E. M. (2001) · Biochemistry · doi:10.1021/bi001929z · Cited by 119
Self-citation
Molecular Interactions of Yeast Neo1p, an Essential Member of the Drs2 Family of Aminophospholipid Translocases, and Its Role in Membrane Trafficking within the Endomembrane System
Wicky, S., Schwarz, H., & Singer‐Krüger, B. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.17.7402-7418.2004 · Cited by 117
TMEM16F (Anoctamin 6), an anion channel of delayed Ca2+ activation
Grubb, S., Poulsen, K. A., Juul, C. A., Kyed, T., Klausen, T. K., Larsen, E. H., & Hoffmann, E. K. (2013) · The Journal of General Physiology · doi:10.1085/jgp.201210861 · Cited by 117
Phosphatidylethanolamine augments factor VIIa-tissue factor activity: enhancement of sensitivity to phosphatidylserine
Neuenschwander, P. F., Bianco-Fisher, E., Rezaie, A. R., & Morrissey, J. H. (1995) · Biochemistry · doi:10.1021/bi00043a004 · Cited by 116
ANOs 3–7 in the anoctamin/Tmem16 Cl − channel family are intracellular proteins
Duran, C., Qu, Z., Osunkoya, A. O., Cui, Y., & Hartzell, H. C. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00140.2011 · Cited by 116
Annexin V-Mediated Calcium Flux across Membranes Is Dependent on the Lipid Composition: Implications for Cartilage Mineralization
Kirsch, T., Nah, H.-D., Demuth, D. R., Harrison, G., Golub, E. E., ADAMS, S. L., & Pacifici, M. (1997) · Biochemistry · doi:10.1021/bi9626867 · Cited by 115
Matrix Gla Protein Inhibits Ectopic Calcification by a Direct Interaction with Hydroxyapatite Crystals
O’Young, J., Liao, Y., Xiao, Y., Jalkanen, J., Lajoie, G., Karttunen, M., Goldberg, H. A., & Hunter, G. K. (2011) · Journal of the American Chemical Society · doi:10.1021/ja207628k · Cited by 115
Changes in the properties of normal human red blood cells during in vivo aging
Franco, R. S., Puchulu‐Campanella, E., Barber, L. A., Palascak, M. B., Joiner, C. H., Low, P. S., & Cohen, R. M. (2012) · American Journal of Hematology · doi:10.1002/ajh.23344 · Cited by 114
Annexin A2 and A5 Serve as New Ligands for C1q on Apoptotic Cells
Martin, M., Leffler, J., & Blom, A. M. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.341339 · Cited by 114
Membrane-dependent reactions in blood coagulation: role of the vitamin K-dependent enzyme complexes
Kalafatis, M., Swords, N. A., Rand, M. D., & Mann, K. G. (1994) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/0925-4439(94)90086-8 · Cited by 109
Extracellular annexins and dynamin are important for sequential steps in myoblast fusion
Leikina, E., Melikov, K., Sanyal, S., Verma, S. K., Eun, B., Gebert, C. M., Pfeifer, K. E., Lizunov, V. A., Kozlov, M. M., & Chernomordik, L. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201207012 · Cited by 109
Cooperation between Engulfment Receptors: The Case of ABCA1 and MEGF10
Hamon, Y., Trompier, D., Ma, Z., Venegas, V., Pophillat, M., Mignotte, V., Zhou, Z., & Chimini, G. (2006) · PLoS ONE · doi:10.1371/journal.pone.0000120 · Cited by 109
The TMEM16 Protein Family: A New Class of Chloride Channels?
Galietta, L. J. V. (2009) · Biophysical Journal · doi:10.1016/j.bpj.2009.09.024 · Cited by 107
Crystal Structure of Lactadherin C2 Domain at 1.7Å Resolution with Mutational and Computational Analyses of Its Membrane-binding Motif
Shao, C., Novakovic, V. A., Head, J. W., Seaton, B. A., & Gilbert, G. E. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m705195200 · Cited by 107
Reconstitution of Phospholipid Scramblase Activity from Human Blood Platelets
Comfurius, P., Williamson, P., Smeets, E. F., Schlegel, R., Bevers, E. M., & Zwaal, R. F. A. (1996) · Biochemistry · doi:10.1021/bi9606859 · Cited by 107
Self-citation
Platelet Factor XIII and Calpain Negatively Regulate Integrin αIIbβ3 Adhesive Function and Thrombus Growth
Kulkarni, S., & Jackson, S. P. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m403559200 · Cited by 107
The role of the red cell membrane in thrombin generation
Whelihan, M. F., & Mann, K. G. (2013) · Thrombosis Research · doi:10.1016/j.thromres.2013.01.023 · Cited by 106
Investigations on the C1q–Calreticulin–Phosphatidylserine Interactions Yield New Insights into Apoptotic Cell Recognition
Païdassi, H., Tacnet‐Delorme, P., Verneret, M., Gaboriaud, C., Houen, G., Duus, K., Ling, W. L., Arlaud, G. J., & Frachet, P. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.02.029 · Cited by 105
Requirement of Adaptor Protein GULP during Stabilin-2-mediated Cell Corpse Engulfment
Park, S., Kang, K.-B., Thapa, N., Kim, S.-Y., Lee, S.-J., & Kim, I. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m709105200 · Cited by 105
A novel missense mutation in ABCA1 results in altered protein trafficking and reduced phosphatidylserine translocation in a patient with Scott syndrome
Albrecht, C., McVey, J. H., Elliott, J. I., Sardini, A., Kasza, I., Mumford, A. D., Naoumova, R. P., Tuddenham, E. G. D., Szabó, K., & Higgins, C. F. (2005) · Blood · doi:10.1182/blood-2004-05-2056 · Cited by 104
Exposure of endogenous phosphatidylserine at the outer surface of stimulated platelets is reversed by restoration of aminophospholipid translocase activity
Bevers, E. M., Tilly, R. H. J., Senden, J. M., Comfurius, P., & Zwaal, R. F. A. (1989) · Biochemistry · doi:10.1021/bi00432a007 · Cited by 102
Self-citation
p85α recruitment by the CD300f phosphatidylserine receptor mediates apoptotic cell clearance required for autoimmunity suppression
Tian, L., Choi, S., Murakami, Y., Allen, J. N., Morse, H. C., Qi, C., Krzewski, K., & Coligan, J. E. (2014) · Nature Communications · doi:10.1038/ncomms4146 · Cited by 100
Factor Xa Activation of Factor V Is of Paramount Importance in Initiating the Coagulation System
Schuijt, T. J., Bakhtiari, K., Daffre, S., DePonte, K., Wielders, S. J. H., Marquart, J. A., Hovius, J. W., van der Poll, T., Fikrig, E., Bunce, M. W., et al. (2013) · Circulation · doi:10.1161/circulationaha.113.003191 · Cited by 100
Transbilayer Movement of Phospholipids in Biogenic Membranes
Kol, M. A., de Kroon, A. I. P. M., Killian, J. A., & KRUIJFF, B. D. (2004) · Biochemistry · doi:10.1021/bi036200f · Cited by 99
CED-1, CED-7, and TTR-52 Regulate Surface Phosphatidylserine Expression on Apoptotic and Phagocytic Cells
Mapes, J., Chen, Y.-Z., Kim, A., Mitani, S., Kang, B., & Xue, D. (2012) · Current Biology · doi:10.1016/j.cub.2012.05.052 · Cited by 96
CD300b regulates the phagocytosis of apoptotic cells via phosphatidylserine recognition
Murakami, Y., Tian, L., Voss, O. H., Margulies, D. H., Krzewski, K., & Coligan, J. E. (2014) · Cell Death and Differentiation · doi:10.1038/cdd.2014.86 · Cited by 95
A novel aminophospholipid transporter exclusively expressed in spermatozoa is required for membrane lipid asymmetry and normal fertilization
Wang, L., Beserra, C., & Garbers, D. L. (2003) · Developmental Biology · doi:10.1016/j.ydbio.2003.11.004 · Cited by 94
Specific membrane binding of factor VIII is mediated by O-phospho-L-serine, a moiety of phosphatidylserine
Gilbert, G. E., & Drinkwater, D. (1993) · Biochemistry · doi:10.1021/bi00088a009 · Cited by 94
Insights into platelet-based control of coagulation
Witt, S., Verdoold, R., Cosemans, J. M. E. M., & Heemskerk, J. W. M. (2014) · Thrombosis Research · doi:10.1016/s0049-3848(14)50024-2 · Cited by 93
Ion channel and lipid scramblase activity associated with expression of TMEM16F/ANO6 isoforms
Scudieri, P., Caci, E., Venturini, A., Sondo, E., Pianigiani, G., Marchetti, C., Ravazzolo, R., Pagani, F., & Galietta, L. J. V. (2015) · The Journal of Physiology · doi:10.1113/jp270691 · Cited by 93
TAM receptor ligands in lupus: Protein S but not Gas6 levels reflect disease activity in systemic lupus erythematosus
Suh, C., Hilliard, B. A., Li, S., Merrill, J. T., & Cohen, P. L. (2010) · Arthritis Research & Therapy · doi:10.1186/ar3088 · Cited by 91
Reactive oxygen species and phosphatidylserine externalization in murine sickle red cells
Banerjee, T., & Kuypers, F. A. (2004) · British Journal of Haematology · doi:10.1046/j.1365-2141.2003.04781.x · Cited by 90
Auto-Oxidation and Oligomerization of Protein S on the Apoptotic Cell Surface Is Required for Mer Tyrosine Kinase-Mediated Phagocytosis of Apoptotic Cells
Uehara, H., & Shacter, E. B. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.4.2522 · Cited by 89
Translocation of Phospholipids Is Facilitated by a Subset of Membrane-spanning Proteins of the Bacterial Cytoplasmic Membrane
Kol, M. A., van Dalen, A., de Kroon, A. I. P. M., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301875200 · Cited by 88
Synergistic Effect of Thrombin on Collagen-Induced Platelet Procoagulant Activity Is Mediated Through Protease-Activated Receptor-1
Keuren, J. F. W., Wielders, S. J. H., Ulrichts, H., Hackeng, T. M., Heemskerk, J. W. M., Deckmyn, H., Bevers, E. M., & Lindhout, T. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000167526.31611.f6 · Cited by 87
Self-citation
Transcriptional control of the human plasma membranephospholipid scramblase 1 gene is mediated by interferon-α
Zhou, Q., Zhao, J., Al-Zoghaibi, F., Zhou, A., Wiedmer, T., Silverman, R. H., & Sims, P. J. (2000) · Blood · doi:10.1182/blood.v95.8.2593 · Cited by 87
Molecular mechanism for differential recognition of membrane phosphatidylserine by the immune regulatory receptor Tim4
Tietjen, G. T., Gong, Z., Chen, C.-H., Vargas, E., Crooks, J. E., Cao, K. D., Heffern, C. T. R., Henderson, J. M., Mati Meron, E., Lin, B., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320174111 · Cited by 83
Caspase-mediated activation of Caenorhabditis elegans CED-8 promotes apoptosis and phosphatidylserine externalization
Chen, Y.-Z., Mapes, J., Lee, E.-S., Skeen-Gaar, R. R., & Xue, D. (2013) · Nature Communications · doi:10.1038/ncomms3726 · Cited by 82
Transient Receptor Potential Channels Function as a Coincidence Signal Detector Mediating Phosphatidylserine Exposure
Harper, M. T., Londoño, J. E. C., Quick, K., Londoño, J. C., Flockerzi, V., Philipp, S. E., Birnbaumer, L., Freichel, M., & Poole, A. W. (2013) · Science Signaling · doi:10.1126/scisignal.2003701 · Cited by 81
MerTK-mediated engulfment of pyrenocytes by central macrophages in erythroblastic islands
Toda, S., Segawa, K., & Nagata, S. (2014) · Blood · doi:10.1182/blood-2014-01-547976 · Cited by 80
The role of dead cell clearance in the etiology and pathogenesis of systemic lupus erythematosus: dendritic cells as potential targets
Biermann, M. H. C., Veissi, S., Maueröder, C., Chaurio, R. A., Berens, C., i, M. H., & Munoz, L. E. (2014) · Expert Review of Clinical Immunology · doi:10.1586/1744666x.2014.944162 · Cited by 80
Phosphatidylserine recognition and induction of apoptotic cell clearance by Drosophila engulfment receptor Draper
Tung, T. T., Nagaosa, K., Fujita, Y., Kita, A., Mori, H., Okada, R., Nonaka, S., & Nakanishi, Y. (2013) · The Journal of Biochemistry · doi:10.1093/jb/mvt014 · Cited by 79
Membrane phospholipid asymmetry as a factor in erythrocyte‐endothelial cell interactions
Schlegel, R., Prendergast, T. W., & Williamson, P. (1985) · Journal of Cellular Physiology · doi:10.1002/jcp.1041230210 · Cited by 79
Self-citation
Epidermal Growth Factor-Like Domain Repeat of Stabilin-2 Recognizes Phosphatidylserine during Cell Corpse Clearance
Park, S., Kim, S., Jung, M.-Y., Bae, D.-J., & Kim, I. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01993-07 · Cited by 78
Phosphatidylserine directly and positively regulates fusion of myoblasts into myotubes
Jeong, J., & Conboy, I. M. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.08.128 · Cited by 76
Assembly of the Prothrombinase Complex on Lipid Vesicles Depends on the Stereochemical Configuration of the Polar Headgroup of Phosphatidylserine
Comfurius, P., Smeets, E. F., Willems, G. M., Bevers, E. M., & Zwaal, R. F. A. (1994) · Biochemistry · doi:10.1021/bi00200a012 · Cited by 74
Self-citation
Calcium-activated and apoptotic phospholipid scrambling induced by Ano6 can occur independently of Ano6 ion currents
Kmit, A. H. P., van Kruchten, R., Ousingsawat, J., Mattheij, N. J. A., Senden-Gijsbers, B. L. M. G., Heemskerk, J. W. M., Schreiber, R., Bevers, E. M., & Kunzelmann, K. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.135 · Cited by 73
Self-citation
Identification of a dimerization domain in the TMEM16A calcium-activated chloride channel (CaCC)
Tien, J., Lee, H. Y., Minor, D. L., Jan, Y. N., & Jan, L. Y. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303672110 · Cited by 73
The molecular identity of the mitochondrial Ca2+ sequestration system
Starkov, A. A. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2010.07756.x · Cited by 70
Aminophospholipid Translocase TAT-1 Promotes Phosphatidylserine Exposure during C. elegans Apoptosis
Züllig, S., Neukomm, L. J., Jovanovic, M., Charette, S. J., Lyssenko, N. N., Halleck, M. S., Reutelingsperger, C. P. M., Schlegel, R., & Hengartner, M. O. (2007) · Current Biology · doi:10.1016/j.cub.2007.05.024 · Cited by 70
Membrane Lipid Alterations in Hemoglobinopathies
Kuypers, F. A. (2007) · Hematology · doi:10.1182/asheducation-2007.1.68 · Cited by 70
Toxoplasma gondii exposes phosphatidylserine inducing a TGF-β1 autocrine effect orchestrating macrophage evasion
Seabra, S. H., de Souza, W., & DaMatta, R. A. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.09.114 · Cited by 69
ABCA1, from pathology to membrane function
Zarubica, A., Trompier, D., & Chimini, G. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0108-z · Cited by 68
β-2-Glycoprotein 1-dependent Macrophage Uptake of Apoptotic Cells
Maiti, S. N., Balasubramanian, K., Ramoth, J. A., & Schroit, A. J. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704990200 · Cited by 66
Survival protein anoctamin‐6 controls multiple platelet responses including phospholipid scrambling, swelling, and protein cleavage
Mattheij, N. J. A., Braun, A., van Kruchten, R., Castoldi, E., Pircher, J., Baaten, C. C. F. M. J., Wülling, M., Kuijpers, M. J. E., Köhler, R., Poole, A. W., et al. (2015) · The FASEB Journal · doi:10.1096/fj.15-280446 · Cited by 65
Acceleration of phospholipid flip-flop in the erythrocyte membrane by detergents differing in polar head group and alkyl chain length
Pantaler, E., Kamp, D., & Haest, C. W. M. (2000) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(00)00322-9 · Cited by 63
Contribution of different phospholipid classes to the prothrombin converting capacity of sonicated lipid vesicles
Smeets, E. F., Comfurius, P., Bevers, E. M., et al. (1996) · Thrombosis Research · doi:10.1016/0049-3848(96)00014-x · Cited by 63
Self-citation
Phosphatidylserine exposure in B lymphocytes: a role for lipid packing
Elliott, J. I., Sardini, A., Cooper, J. C., Alexander, D. R., Davanture, S., Chimini, G., & Higgins, C. F. (2006) · Blood · doi:10.1182/blood-2005-11-012328 · Cited by 63
Impaired Platelet Activation in Familial High Density Lipoprotein Deficiency (Tangier Disease)
Nofer, J., Herminghaus, G., Brodde, M. F., Morgenstern, E., Rust, S., Engel, T., Seedorf, U., Assmann, G., Bluethmann, H., & Kehrel, B. E. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405174200 · Cited by 63
Ratcheting of the substrate from the zymogen to proteinase conformations directs the sequential cleavage of prothrombin by prothrombinase
Bianchini, E. P., Orcutt, S. J., Panizzi, P. R., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504704102 · Cited by 62
A molecular-properties-based approach to understanding PDZ domain proteins and PDZ ligandsPreprint
Giallourakis, C. C., Cao, Z., Green, T. J., Wachtel, H., Xie, X. S., Lopez-Ilasaca, M. A., Daly, M. J., Rioux, J. D., & Xavier, R. J. (2006) · Genome Research · doi:10.1101/gr.5285206 · Cited by 60
Transbilayer Movement of Fluorescent Phospholipid Analogues in the Cytoplasmic Membrane of Escherichia coli
Kubelt, J., Menon, A. K., Müller, P. K., et al. (2002) · Biochemistry · doi:10.1021/bi0118714 · Cited by 59
Transbilayer Lipid Diffusion Promoted by Bax: Implications for Apoptosis
Epand, R. F., Martinou, J., Montessuit, S., & Epand, R. M. (2003) · Biochemistry · doi:10.1021/bi035348w · Cited by 58
Phospholipid asymmetry and transmembrane diffusion in photoreceptor disk membranes
Wu, G., & Hubbell, W. L. (1993) · Biochemistry · doi:10.1021/bi00054a020 · Cited by 58
Trypanosoma cruziexposes phosphatidylserine as an evasion mechanism
DaMatta, R. A., Seabra, S. H., Deolindo, P., Arnholdt, A. C. V., Manhães, L., Goldenberg, S., & de Souza, W. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2006.00495.x · Cited by 58
Role of Phosphatidyl-Serine in Bone Repair and Its Technological Exploitation
Merolli, A., & Santin, M. (2009) · Molecules · doi:10.3390/molecules14125367 · Cited by 57
Production and characterization of transformed B-lymphocytes expressing the membrane defect of Scott syndrome.
Kojima, H., Newton‐Nash, D. K., Weiss, H. J., Zhao, J., Sims, P. J., & Wiedmer, T. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117586 · Cited by 54
Asymmetrical Membranes and Surface Tension
Traı̈kia, M., Warschawski, D. E., Lambert, O., Rigaud, J., & Devaux, P. F. (2002) · Biophysical Journal · doi:10.1016/s0006-3495(02)73915-5 · Cited by 53
Facilitated Phosphatidylserine (PS) Flip-Flop and Thrombin Activation Using A Synthetic PS Scramblase
Boon, J. M., Lambert, T. N., Sisson, A. L., Davis, A. P., & Smith, B. D. (2003) · Journal of the American Chemical Society · doi:10.1021/ja029670q · Cited by 51
Dynamic adhesion of eryptotic erythrocytes to immobilized platelets via platelet phosphatidylserine receptors
Walker, B., Towhid, S. T., Schmid, E., Hoffmann, S. M., Abed, M., Münzer, P., Vogel, S., Neis, F., Brucker, S. Y., Gawaz, M., et al. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00318.2013 · Cited by 51
Chondrocytes Utilize a Cholesterol-Dependent Lipid Translocator To Externalize Phosphatidylserine
Damek-Poprawa, M., Golub, E. E., Otis, L. L., Harrison, G., Phillips, C., & Boesze‐Battaglia, K. (2006) · Biochemistry · doi:10.1021/bi0515927 · Cited by 49
Thymosin β4 is involved in stabilin‐2‐mediated apoptotic cell engulfment
Lee, S.-J., So, I.-S., Park, S., & Kim, I. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.03.058 · Cited by 48
Expression of Proteins Controlling Transbilayer Movement of Plasma Membrane Phospholipids in the B Lymphocytes From a Patient With Scott Syndrome
Zhou, Q., Sims, P. J., & Wiedmer, T. (1998) · Blood · doi:10.1182/blood.v92.5.1707 · Cited by 48
Rapid Procoagulant Phosphatidylserine Exposure Relies on High Cytosolic Calcium Rather Than on Mitochondrial Depolarization
Arachiche, A., Kerbiriou‐Nabias, D., Garcin, I., Letellier, T., & Dachary-Prigent, J. (2009) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.190926 · Cited by 47
Analysis and Molecular Modeling of the Formation, Structure, and Activity of the Phosphatidylserine-Calcium-Phosphate Complex Associated with Biomineralization
Wu, L. N. Y., Wu, L. N. Y., Genge, B. R., & Wuthier, R. E. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m707653200 · Cited by 44
The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium: Evidence for rapid flip and flop movement
Hessel, E., Herrmann, A., Müller, P., Schnetkamp, P. P. M., & Hofmann, K. (2000) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2000.01147.x · Cited by 43
Oligomeric Dop1p is Part of the Endosomal Neo1p-Ysl2p-Arl1p Membrane Remodeling Complex
Barbosa, S., Pratte, D., Schwarz, H., Pipkorn, R., & Singer‐Krüger, B. (2010) · Traffic · doi:10.1111/j.1600-0854.2010.01079.x · Cited by 43
Caspase Activity Is Required for Engulfment of Apoptotic Cells
Shklyar, B., Levy‐Adam, F., Hakim‐Mishnaevski, K., & Kurant, E. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00233-13 · Cited by 43
Calcificação vascular: fisiopatologia e implicações clínicas
Liberman, M., Pesaro, A. E. P., do Carmo, L. S., & Junior, C. V. S. (2013) · Einstein (São Paulo) · doi:10.1590/s1679-45082013000300021 · Cited by 42
A TMEM16F point mutation causes an absence of canine platelet TMEM16F and ineffective activation and death‐induced phospholipid scrambling
Brooks, M. B., Catalfamo, J. L., MacNguyen, R., Tim, D., Fancher, S., & McCardle, J. A. (2015) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.13157 · Cited by 42
Daily exposure to a running wheel entrains circadian rhythms in mice in parallel with development of an increase in spontaneous movement prior to running-wheel access
Yamanaka, Y., Honma, S., & Honma, K. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00389.2013 · Cited by 39
C. elegans Secreted Lipid-Binding Protein NRF-5 Mediates PS Appearance on Phagocytes for Cell Corpse Engulfment
Zhang, Y., Wang, H., Kage‐Nakadai, E., Mitani, S., & Wang, X. (2012) · Current Biology · doi:10.1016/j.cub.2012.06.004 · Cited by 39
Role of Phosphatidylserine in Phospholipid Flippase-Mediated Vesicle Transport in Saccharomyces cerevisiae
Takeda, M., Yamagami, K., & Tanaka, K. (2014) · Eukaryotic Cell · doi:10.1128/ec.00279-13 · Cited by 38
Transbilayer Phospholipid Movements in ABCA1-Deficient Cells
Williamson, P., Halleck, M. S., Malowitz, J., Ng, S., Fan, X., Krahling, S., Remaley, A. T., & Schlegel, R. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000729 · Cited by 37
Self-citation
Membrane Binding by Prothrombin Mediates Its Constrained Presentation to Prothrombinase for Cleavage
Bradford, H. N., Orcutt, S. J., & Krishnaswamy, S. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.502005 · Cited by 29
The Phosphatidylserine Binding Site of the Factor Va C2 Domain Accounts for Membrane Binding but Does Not Contribute to the Assembly or Activity of a Human Factor Xa−Factor Va Complex
Majumder, R., Quinn-Allen, M. A., Kane, W. H., & Lentz, B. R. (2004) · Biochemistry · doi:10.1021/bi047962t · Cited by 29
Rational design of small molecules targeting the C2 domain of coagulation factor VIII
Nicolaes, G. A. F., Kulharia, M., Voorberg, J., Kaijen, P. H. P., Wroblewska, A., Wielders, S. J. H., Schrijver, R., Spérandio, O., & Villoutreix, B. O. (2013) · Blood · doi:10.1182/blood-2013-05-503227 · Cited by 28
Recruitment of beta-2-glycoprotein 1 to cell surfaces in extrinsic and intrinsic apoptosis
Balasubramanian, K., Maiti, S. N., & Schroit, A. J. (2005) · APOPTOSIS · doi:10.1007/s10495-005-0817-3 · Cited by 27
Rapid transport of phospholipids across the plasma membrane of Leishmania infantum
Araújo-Santos, J. M., Gamarro, F., Castanys, S., et al. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)00947-1 · Cited by 25
A Hyaluronan Receptor for Endocytosis (HARE) Link Domain N-Glycan Is Required for Extracellular Signal-regulated Kinase (ERK) and Nuclear Factor-κB (NF-κB) Signaling in Response to the Uptake of Hyaluronan but Not Heparin, Dermatan Sulfate, or Acetylated Low Density Lipoprotein (LDL)
Pandey, M. S., & Weigel, P. H. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.565846 · Cited by 21
Structural study of TTR-52 reveals the mechanism by which a bridging molecule mediates apoptotic cell engulfmentPreprint
Kang, Y., Zhao, D., Liang, H., Liu, B., Zhang, Y., Liu, Q., Wang, X., & Liu, Y. (2012) · Genes & Development · doi:10.1101/gad.187815.112 · Cited by 19
Molecular simulation studies of human coagulation factor VIII C domain-mediated membrane binding
Du, J., Wichapong, K., Hackeng, T. M., & Nicolaes, G. A. F. (2014) · Thrombosis and Haemostasis · doi:10.1160/th14-02-0180 · Cited by 15
Decreased motility of human spermatozoa presenting phosphatidylserine membrane translocation-cells selection with the swim-up technique
Kotwicka, M., Jendraszak, M., Skibińska, I., Jędrzejczak, P., & Pawelczyk, L. A. (2011) · Human Cell · doi:10.1007/s13577-011-0024-1 · Cited by 14
The Calcium Gradient Along The Rod Outer Segment
Leibovic, K. N. (2002) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-0121-3_2 · Cited by 1

Characterization of Lipid-Protein Interactions and Lipid-Mediated Modulation of Membrane Protein Function through Molecular Simulation
Muller, M. P., Jiang, T., Sun, C., Lihan, M., Pant, S., Mahinthichaichan, P., Trifan, A., & Tajkhorshid, E. (2019) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00608 · Cited by 282
Transverse distribution of plasma membrane bilayer cholesterol: Picking sides
Steck, T. L., & Lange, Y. (2018) · Traffic · doi:10.1111/tra.12586 · Cited by 141
Molecular insights into human phosphatidylserine synthase 1 reveal its inhibition promotes LDL uptake
Long, T., Li, D., Vale, G., Jiang, Y., Schmiege, P., Yang, Z. J., McDonald, J. G., & Li, X. (2024) · Cell · doi:10.1016/j.cell.2024.08.004 · Cited by 31
The PQ-loop protein Any1 segregates Drs2 and Neo1 functions required for viability and plasma membrane phospholipid asymmetry
Takar, M., Huang, Y., & Graham, T. R. (2019) · Journal of Lipid Research · doi:10.1194/jlr.m093526 · Cited by 12
Structure and function of the human apoptotic scramblase Xkr4
Chakraborty, S., Feng, Z., Lee, S., Alvarenga, O. E., Panda, A., Zhang, S., Bruni, R., Khelashvili, G., Gupta, K., & Accardi, A. (2025) · Nature Communications · doi:10.1038/s41467-025-62739-1 · Cited by 5

See all 447

Authors: Bevers, E. M., & Williamson, P. L.
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 2016-04
Volume: 96
Issue: 2
Pages: 605-645
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.00020.2015
OpenAlex: W2291071386
Cited by: 447
References: 297
FWCI: 2.67
Type: journal article
Language: en
Open access: closed

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.

Getting to the Outer Leaflet: Physiology of Phosphatidylserine Exposure at the Plasma Membrane

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Self-check

Citations

Cites

Cited by

Metadata

Record

About these checks

Data sources