Lipid Asymmetry Model

Courtesy of Peggy Halleck (Penn State University)

“Biochemical Characterization of P4-ATPase Mutations Identified in Patients with Progressive Familial Intrahepatic Cholestasis” A Stone, C Chau, C Eaton, E Foran, M Kapur, E Prevatt, N Belkin, D Kerr, T Kohlin and P Williamson, J Biol Chem, 287: 41139-41151 (2012)

“Mapping functional interactions in a heterodimeric phospholipid pump”’
CF. Puts, R Panatala, H Hennrich, A Tsareva, P Williamson, and JCM Holthuis, J Biol Chem, 287: 30529-40 (2012)

“Outside of the box: Recent News about Phospholipid translocation by P4 ATPases”, A Stone and PL Williamson, J Chem Biol, 5: 131-136 (2012)

 “Phospholipid scramblase: When phospholipid asymmetry goes away”, EM Bevers and PL Williamson, in Transmembrane Dynamics of Lipids, P. Devaux and A. Herrmann, eds, Wiley (New York, 2011)

“Compound heterozygosity for two novel TMEM16F mutations in a patient with Scott syndrome”, E Castoldi, PW Collins, PL Williamson and EM Bevers, Blood: 117: 4399-4400 (2011)

"The flip side of cardiolipin import”, CC Paulusma, RHJ Houwen and PL Williamson Nature Medicine, 17: 413 (2011)

“Phospholipid transport: Sighting a new face of an old friend” P Williamson, Curr Biol, 21: R168-169 (2011)

“Phospholipid Scramblase: An Update”, EM Bevers and P Williamson, FEBS Lett. 584: 2724-2730 (2010)

 "A P4-ATPase protein interaction network reveals a link between aminophospholipid transport and phosphoinositide metabolism" C Puts, G Lenoir,J Krijgsveld, P Williamson and J Holthuis, J Proteome Res 9: 833-842 (2010) 

“Cdc50p plays a vital role in the ATPase reaction cycle of the putative aminophospholipid transporter Drs2p* G Lenoir, P Williamson, CF Puts, JCM Holthuis, J Biol Chem 284: 17596-17967 (2009)

“P.S. to PS (phosphatidylserine)-dependent proteins in apoptotic cell clearance” RA Schlegel and P Williamson Science STKE 2007: pe57 (2007)

“On the origin of lipid asymmetry: the flip side of ion transport” G Lenoir, P Williamson and JCM Holthuis.  Curr Opin Chem Biol 11: 654-661 (2007)

“Transbilayer phospholipid movements in ABCA1-deficient cells” P Williamson, MS Halleck, J Malowitz, S Ng,X Fan,S Krahling, AT Remaley, RA Schlegel. PLoS ONE. 2:e729 (2007)

“Lipid Specific Activation of the Murine P4-ATPase Atp8a1 (ATPase II)” J Paterson, K Renkema, L Burden, M Halleck, RA Schlegel, P Williamson, and DL Daleke Biochemistry 45: 5637-5376 (2006)

“Hide and Seek: The Secret Identity of the Phosphatidylserine Receptor” P Williamson and RA Schlegel J Biol 3: 14 (2004)

“Macrophage Surface Expression of Annexins I and II in the Phagocytosis of Apoptotic Lymphocytes” X Fan, S Krahling, D Smith, P Williamson and
RA Schlegel Mol Biol Cell 15: 2863-2872 (2004)

“Phosphatidylserine expression and phagocytosis of apoptotic thymocytes during differentiation of monocytic cells” MK Callahan, MS Halleck, S Krahling, AJ Henderson, P Williamson and RA Schlegel J Leuk Biol 74: 846-856 (2003)

“Phospholipid Transporters in the Brain” RA Schlegel, MS Halleck, and P Williamson, in Nutrition and Biochemistry of Phospholipids (Bernard F. Szuhaj and Willem van Nieuwenhuyzen, Eds), 1-13 (2003)

“Transbilayer Phospholipid Movement and the Clearance of Apoptotic Cells” P Williamson and R A Schlegel Biochim Biophys Acta 1595: 53-63 (2003)

 “Report from Cell Block #4" (review of Molecular Biology of the Cell, 4th ed, by Alberts et al) P Williamson, Cell 109: 663-664 (2002)

“Reanalysis of ATP11B, a type IV P-type ATPase” MS Halleck, RA Schlegel, and P Williamson, J Biol Chem, 277: 9736-40 (2002)

“Coagulation changes in Individuals with Sickle Cell Trait”, MP Westerman, D Green, A Gilman-Sachs, K Beaman, S Freels, L Boggio, S Allen, L Zuckerman, R Schlegel, and P Williamson, Amer J Hematol, 69: 89-94 (2002)

“Phosphatidylserine exposure and phagocytosis of apoptotic cells.” P Williamson, S van den Eijnde and RA Schlegel.  In Apoptosis, a volume of Methods in Cell Biology (L. Schwartz and J. Ashwell, eds), Academic Press, San Diego, CA. 66: 339-365 (2001)

“Of umbrellas, jazz and slow-steppin’” P. Williamson and RA Schlegel, Cell Death Different 8:104-105 (2001)

“Phosphatidylserine, a Death Knell”, RA. Schlegel and Patrick Williamson,  Cell Death Different 8: 551-563 (2001)

“Phospholipid Scramblase Activation Pathways in Lymphocytes”, P Williamson, A Christie, T Kohlin, RA Schlegel, P Comfurius, M Harmsma, RFA Zwaal, and EM Bevers, Biochemistry 40: 8065-8072 (2001)

“Surface Expression of Phosphatidylserine on Macrophages is Required for Phagocytosis of Apoptotic Thymocytes” MK Callahan, P Williamson, and RA Schlegel, Cell Death Different 7: 645-653 (2000).

“The Central Role of Phosphatidylserine in the Phagocytosis of Apoptotic Thymocytes” RA Schlegel, MK. Callahan and P Williamson, Ann NY Acad Sci 926: 217-225 (2000)

“Exposure of phosphatidylserine is a general feature of macrophage recognition of apoptotic lymphocytes” S Krahling, M K Callahan, P Williamson, and R A Schlegel, Cell Death Different, 6: 183-189 (1999)

“Regulation of phosphatidylserine exposure and phagocytosis of apoptotic T lymphocytes” B Verhoven, S Krahling, R A Schlegel. and P Williamson, Cell Death Different, 6: 262-270 (1999)

“Antiphospholipid Antibodies, Proteins C and S, and Coagulation Changes in Sickle Cell Disease”, M P Westerman, D Green, A Gilman-Sachs, K Beaman, S Freels, L Boggio, S Allen, L Zuckerman, R Schlegel, and P Williamson, J Lab Clin Med, 134: 352-362 (1999)

“Cloning, Expression and Chromosomal Mapping of a Human ATPase II Gene, Member of the Third Subfamily of P-type ATPases and Orthologous to the Presumed Bovine and Murine Aminophospholipid Translocase”, I Mouro, M S Halleck, R A Schlegel, M G Mattei, P Williamson, A Zachowski,  P Devaux, J-P Cartron and Y Colin, Biochem Biophys Res Commun, 257: 333-339 (1999)

“CD14 is a Component of Multiple Recognition Systems used by Macrophages to Phagocytose Apoptotic Lymphocytes”, R A Schlegel, S Krahling, M K Callahan and P Williamson, Cell Death Different, 6: 583-592 (1999)

“Differential Expression of Putative Transbilayer Amphipath Transporters”, MS Halleck, JF Lawler, Jr., S Blackshaw, L Gao, P Nagarajan, C Hacker, S Pyle, JT Newman, Y Nakanishi, H Ando, D Weinstock, P Williamson, and RA Schlegel, Physiol Genomics, 1: 139-150 (1999)

“Engulfment of apoptotic cells involves the redistribution of membrane phosphatidylserine on phagocyte and prey” D Marguet, M-F Luciani, A Moynault, P Williamson, and G Chimini Nature Cell Biology, 1: 454-6 (1999)

“Multiple Members of a Third Subfamily of P-type ATPases Identified by Genomic Sequences and ESTs”, M S Halleck, D Pradhan, C Blackman, C Berkes, P Williamson, and R A Schlegel, Genome Research, 8: 354-361 (1998)

"Phosphatidylserine as a Signal for Recognition and Phagocytosis: The Proteins Involved" R A Schlegel, S Krahling, A J Christie, and P Williamson, in Choline, Phospholipids, Health and Disease (B. Szuhaj and S. Zeisel, eds), American Oil Chemists Society Press, Champaign, IL, pp. 57-68 (1998)

"Assessment of painful episode frequency in patients with sickle cell disease" M P Westerman, K Bailey, S Freels,  R Schlegel, and P Williamson, Amer Jour Hematol,  54: 183-188 (1997)

“Multiple systems for recognition of apoptotic lymphocytes by macrophages” D Pradhan, S Krahling, P Williamson, and R A Schlegel, Mol Biol Cell, 8: 767-778 (1997)

"A Subfamily of P-type ATPases with Aminophospholipid Transporting Activity" X. Tang, R A Schlegel, M. Halleck, and P Williamson, Science 272: 1495-1497 (1996)

“Mechanisms for Recognition and Phagocytosis of Apoptotic Lymphocytes by Macrophages”, R A Schlegel, M Callahan, S Krahling and P Williamson, in
Lymphocyte Activation and Immune Regulation VI.  Cell Cycle and Programmed
Cell Death in the Immune System.  J.J. Cohen, T. Hunter, S.Gupta and W. E.
Paul, eds. Plenum, New York, p. 21-28 (1996).

"Reconstitution of phospholipid scramblase from human blood platelets" P Comfurius, P Williamson, E F Smeets, R A Schlegel, E M Bevers, and R F A Zwaal, Biochem 35: 7631-7634 (1996)

"Continuous Analysis of the Mechanism of Activated Transbilayer Lipid Movement in Platelets" P Williamson, E M Bevers, E F Smeets, P Comfurius, R A Schlegel, and R F A Zwaal. Biochem 34: 10448-10455 (1995)

"The Complex of Phosphatidylinositol 4,5-Bisphosphate and Calcium Ions is not responsible for Ca2+-induced loss of Phospholipid asymmetry in the human erythrocyte: A study in Scott Syndrome, a disorder of Calcium-induced phospholipid scrambling" E M Bevers, R Wiedmer, P Comfurius, J Zhao, E F Smeets, R A Schlegel, A J Schroit, H J Weiss, P Williamson, R F A Zwaal, and Peter J Sims, Blood 86: 1983-1991 (1995)

"Mechanism of Phosphatidylserine Exposure,  A Phagocyte Recognition Signal, on Apoptotic T Lymphocytes". B Verhoven, R A Schlegel, and P Williamson. J Exp Med 182: 1597-1601 (1995)

"Phosphatidylserine Vesicles Inhibit Phagocytosis of Erythrocytes with a Symmetric Transbilayer distribution of phospholipids". D Pradhan, P Williamson, and R A Schlegel, Mol Memb Biol. 11: 181-188 (1994)

"Back and Forth: the regulation and function of transbilayer phospholipid movement in eukaryotic cells (Review)" P Williamson and R A Schlegel. Mol Memb Biol 11: 199-216 (1994)

"Intracellular Ca++-containing vesicles in sickle cell disorders", M P Westerman, E Puchulu, R A Schlegel, M Salameh, and P Williamson, J Lab Clin Med, 124: 416-420 (1994)

"Plasma membrane lipid packing and LFA-1-dependent aggregation of lymphocytes", D M Smith, P L Williamson, and R A Schlegel,  J Cell. Physiol. 156: 182-188 (1993)

"Altered lipid packing identifies apoptotic thymocytes", R A Schlegel, M Stevens, K Lumley-Sapanski, and P L Williamson,  Imm Lett, 36: 283-288 (1993)

"Asymmetry in trans-bilayer lateral pressure may drive expansion of the secretion fusion pore" A Bogdanov, B Verhoven, R A Schlegel, and P Williamson  Biochem Soc Trans 21: 271-275 (1993)

"Lipid asymmetry in erythrocytes is rapidly lost and regained", B M Verhoven, R A Schlegel, and P Williamson, Biochim Biophys Acta 1104: 15-23 (1992)

"Single cell analysis of factors increasing the survival of resealed erythrocytes in the circulation of mice" R A Schlegel, K Lumley-Sapanski, and P Williamson, Proc 4th Internatl Meeting for the Use of Resealed Erythrocytes as Carriers and Bioreactors M. Magnani and J. deLoach, eds, pp. 133-138 (1992)

"Ca2+ accumulation and loss by aberrant endocytic vesicles in sickle erythrocytes", P Williamson, E Puchulu, J Penniston, M P Westerman, and R A Schlegel,  J Cell Physiol 152: 1-9 (1992)

"Binding of perforin to membranes is sensitive to lipid spacing and not headgroup", R Antia, R A Schlegel and P Williamson,  Immun Lett 32: 153-158 (1992)  Winner: EFIS Prize for best article, 1992

"Ca++ induces transbilayer redistribution of all major phospholipids in human erythryocytes", P Williamson, A Kulick, A Zachowski, R A Schlegel, and P F Devaux,  Biochem 31: 6355-6360 (1992)

"Altered erythrocyte protein kinase C activity and membrane protein phosphorylation in chronic myelogenous leukemia"  M Kundu, J Basu, M Fujimagari, P Williamson, R A Schlegel, and P Chakrabarti,  Biochem Biophys Acta 1096: 205-208 (1991)

"Monozygotic twins with sickle cell anemia and discordant clinical courses: Clinical and laboratory studies" B R Amin, R M Bauersachs, H J Meiselman, N Mohandas, R P Hebbel, P E Bowen, R A Schlegel, P Williamson, and M P Westerman,  Hemoglobin 15: 247-256 (1991)

"Bilayer/cytoskeleton interactions in lipid-symmetric erythrocytes assessed by a photoactivatable phospholipid analogue" D Pradhan, P Williamson, and R A Schlegel,
Biochemistry 30: 7754-7758 (1991)

"A Quantitative model of the humoral immune system suggests that immune memory is just the colocalization of specific B and T cells" R Antia, B Levin, and P Williamson,  J Theoret Biol 153: 371-384 (1991)

"Ca2+-dependent membrane-binding proteins in normal erythrocytes and erythrocytes from patients with chronic myelogenous leukemia, M Fujimagari, P L Williamson, and R A Schlegel, Blood 75: 1337-1235 (1990)

"Peroxidation-induced perturbations of erythrocyte lipid organization" D Pradhan, M Weiser, K Lumley-Sapanski, D Frazier, P Williamson, and R A Schlegel,  Biochim Biophys Acta 1023: 398-404 (1990)

"Signals for recognition of resealed erythrocytes by reticuloendothelial cells", R A Schlegel and P Williamson, Adv Biosciences 81: 195-198 (1990)

"Functional and pathological significance of phospholipid asymmetry in erythrocyte membranes", R A Schlegel, S Kemper, and P Williamson, J Biosci 15: 197-192 (1990)

"Erythrocyte membrane abnormalities in sickle cell disease", P. Williamson, E Puchulu, M Westerman, and R A Schlegel,  Biotechnol and Appl Biochem 12: 523-8 (1990)

"A photoactivatable phospholipid analog that specifically labels membrane cytoskeletal proteins of intact erythrocytes", D Pradhan, P Williamson, and R A Schlegel,  Biochemistry 28: 6943-6949 (1989)

"Effect of transbilayer phospholipid distribution on erythrocyte fusion", E K Tullius, P Williamson, and R A Schlegel, Biosciences Rep,  9: 623-633 (1989)

"Plasma membrane lipid organization and the adherence of differentiating lymphocytes to macrophages", B J Del Buono, S M White, P L Williamson, and R A Schlegel,  J Cell Physiol 138: 61-69 (1989)

"Role of phospholipid asymmetry in cellular membrane fusion"  R A Schlegel and P Williamson in  Molecular Mechanisms of Membrane Fusion  Sohki,D Doyle, T D Flanagan, S W Hui, and E Mayhew, eds, Plenum, pp. 289-301 (1988)

"Relation between the organization of spectrin and of membrane lipids in lymphocytes", B J Del Buono, P L Williamson, and R A Schlegel, J Cell Biol,  106: 697-703 (1988)

"Merocyanine 540 as a flow cytometric probe of membrane lipid organization in Leukocytes", L McEvoy, R A Schlegel, P Williamson, and B J del Buono,  J Leuk Biol 44: 337-344 (1988)

"Phosphatidylserine as a determinant for reticuloendothelial recognition of liposome models of the erythrocyte surface", T M Allen, P Williamson, and R A Schlegel,  Proc Nat Acad Sci, US 85: 8067-71 (1988)

"A fluorescent dye which recognizes mature peripheral erythrocytes of myeloproliferative disorders", J A Reed, R Green, Y Yamada, R H Kough, P Williamson, and R A Schlegel, Cell Biol Int Rep 11: 55-62 (1987)

"Membrane phospholipid organization as a determinant of blood cell-reticuloendothelial cell interactions", R A Schlegel and P Williamson,  J Cell Physiol 132: 381-384 (1987)

"Phospholipid organization as a determinant of red cell recognition by the reticuloendothelial system", R A Schlegel, L McEvoy, M Weiser, and P Williamson, Adv Biosci 67: 173-181 (1987)

"Maintenance of membrane phospholipid asymmetry: lipid - cytoskeletal interactions or lipid pump?" P Williamson, R Antia, and R A Schlegel, FEBS Letters 219: 316-20 (1987).

"Alterations in plasma membrane lipid organization during lymphocyte differentiation", B J del Buono, P L Williamson, and R A Schlegel,  J Cell Physiol 126: 379-388 (1986).

"Membrane phospholipid asymmetry as a determinant of erythrocyte recognition by macrophages", L McEvoy, P Williamson, and R A Schlegel, Proc Nat Acad Sci 83: 3311-3315 (1986)

"Phospholipid Asymmetry in Loaded Red Cells", R A Schlegel, J A Reed, L McEvoy, L Algarin, and P Williamson  Meth Enzymol 149: 281-293 (1986)

"Alteration of Plasma Membrane Organization in Sickle Cell   Anemia", H-R Choe, R A Schlegel, E Rubin, P Williamson, and M   P Westerman,  Brit Jour Haematol 63: 761-773, (1986)

"Endocytosis in Sickle Red Cells: A Mechanism for Elevated Intracellular Ca2+ Levels" E Rubin, R A Schlegel, and P Williamson,  J Cell Physiol 126: 53-59 (1986)

"Changes in the organization of the lipid bilayer of the plasma membrane during spermatogenesis and epididymal maturation",  R A Schlegel, R Hammerstedt, G P Cofer, K Kozarsky, D Friedus, and P Williamson, Biology of Reproduction 34: 379-391 (1986)

"Erythrocyte Membrane Phospholipid Asymmetry as a Factor in Erythrocyte-Endothelial Cell Interactions", R A Schlegel, T W Prendergast, and P Williamson.  J Cell Physiol 123: 215-218 (1985)

"Insertion of Lipid Domains into Plasma Membranes by Fusion with  Erythrocytes", R A Schlegel, K Lumley-Sapanski, and P Williamson.  Biochim Biophys Acta 846: 234-41 (1985)

"Membrane Phospholipid Asymmetry and the Adherence of Loaded   Red Blood Cells", R A Schlegel, L. McEvoy, and P Williamson,   Biblthca. Haemat. 51: 150-156 (1985).

"Disruption of Phospholipid Asymmetry in Erythrocyte Vesicles Deficient in Spectrin", H-R Choe, P Williamson, E Rubin, and R A Schlegel,  Cell Biol Internat Rep 9: 597-606, (1985)

"RNA Synthesis in Male Pronuclei of the Sea Urchin", D Poccia, R Wolff, S Kragh and P Williamson, Biochim Biophys Acta 824: 349-356 (1985)

"Merocyanine 540 recognizes membrane abnormalities of erythrocytes in chronic myelogenous leukemia", J A Reed, R H Kough, P L Williamson, and R A Schlegel,  Cell Biol Internat Reports 9: 43-49 (1985)

"Phospholipid Asymmetry in Human Erythrocyte Ghosts",  P Williamson, L Algarin, J Bateman, H-R Choe, and R A Schlegel. J Cell Physiol 123: 209-214 (1985).

"Alteration of Lipid Organization following Fertilization of Sea Urchin Eggs"; D J Freidus, R A Schlegel, and P Williamson.   Biochim Biophys Acta 803: 191-196 (1984).

"Maintenance of phospholipid asymmetry and its role in erythrocyte pathology", P Williamson and R A Schlegel Erythrocyte Membranes 3: Recent clinical and Experimental Advances) (W.C. Kruckeberg, J. W. Eaton, J. Aster, and G.J. Brewer, eds) Alan R Liss N. Y. pp. 123-136 (1984).

"Plasma Membrane Lipid Order of Leukemic and Normal Immature  Avian Erythroid Cells", G P Cofer, P Williamson, and R A Schlegel Exp Cell Res 153: 32-38 (1984).

"Merocyanine 540: a fluorescent probe sensitive to lipid packing", P Williamson, K Mattocks, and R A Schlegel.  Biochim Biophys Acta 732: 387-393 (1983).

"Lectin-induced Rearrangement of an Immature Hematopoietic Cell Surface Marker", B M Phelps, P Williamson, and R A Schlegel. J Cell Physiol  110: 245-248 (1982).

"Enucleation eliminates a Differentiation-Specific Marker from Normal and Leukemic Murine Erythroid Cells". R A Schlegel, B M Phelps, G P Cofer, and P Williamson. Expt Cell Res 139: 321-325 (1982)

"Involvement of Spectrin in the Maintenance of Membrane Phase State  Asymmetry", P Williamson, J Bateman, K Kozarsky, K Mattocks, N Hermanowicz, H-R Choe, and R A Schlegel.  Cell 30: 725-733 (1982).

"Membrane Phase State and the Rearrangement of Hematopoietic Cell Surface Receptors", P Williamson, W Massey, B M Phelps, and R A Schlegel,  Mol Cell Biol  1: 128-135 (1981).

"Alterations in Chromatin Structure during Early Sea Urchin Embryogenesis", A Savic, P Richman, P Williamson, and D Poccia,  Proc Nat Acad Sci  78: 3706-3710 (1981).

"A Hybridization Method of Autoradiographic Visualization of   Small Unique Sequence Fragments Resolved on Polyacrylamide   Gels", P Williamson,  Anal Biochem  109: 309-316 (1980).

"Binding of Merocyanine 540 to Normal and Leukemic Erythroid Cells", R Schlegel, B Phelps, A Waggoner, L Terada, and P Williamson, Cell  20: 321-328 (1980).

"DNA Folding and Histone Organization in Chromatin", G Felsenfeld, D Camerini-Otero, R Simon, B Sollner-Webb, P Williamson, and M Zasloff,  Proc Miami Winter Sympos, Acad Pr, New York, 235-249 (1979).

"The Internal Organization of the Nucleosome", G Felsenfeld, J McGhee, B Sollner-Webb, and P Williamson,  Proc ICN-UCLA Symp Mol Biol pp. 541-549 (1979).

"Transcription of histone covered T7 DNA by E. Coli RNA Polymerase", P Williamson and G Felsenfeld, Biochemistry  17: 5695-5705 (1978).

 "The Heterogeneous Nuclear RNA of Chicken Erythroblasts", P Williamson and A J Tobin,  Biochim Biophys Acta  475: 366-382 (1977).

"DNA Structure, Nucleosome Folding, and Gene Activity", R D Camerini-Otero, B Sollner-Webb, R H Simon, P Williamson, M Zasloff, and G Felsenfeld,  Cold Spring Harbor Symp Quant Biol 42: 57-75 (1977).

"The Heterogeneous Nuclear RNA of Chicken Erythroblasts", P Williamson and A J Tobin, Proc ICN-UCLA Symposium on Devel Biol; ed. by D MacMahon and C F Fox, pp 497-507 (1975).

"Analysis of Data from DNA-DNA and DNA-RNA Hybridization Experiments", P Williamson in Eukaryotes at the Subcellular Level , ed. by J.A. Last, Marcel-Dekker, New York, pp. 125-160, (1975).

"Studies on globin mRNA and its metabolism in chickens", Ph.D. Thesis, Harvard University (1974).

"Binding of a-Bungarotoxin to Acetylcholine Receptors in Mammalian Muscle", D Berg, R B Kelly, P B Sargent, P Williamson, and Z Hall Proc Nat Acad Sci 69: 147-151 (1972).

"Purification of Ile-tRNA synthetase from E. coli", P Williamson, Quarterly Report, Laboratory of Chemical Biodynamics, Berkeley, Calif Fall (1969).


Lipid Asymmetry Model

Courtesy of Peggy Halleck (Penn State University)