Phosphatidylserine-mediated cellular signaling

Advances in Experimental Medicine and Biology

Volumn 991, Issue , 2013, Pages 177-193

  Kay, Jason G ^a   Grinstein, Sergio ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Lipid dynamics; Membrane signaling; Phosphatidylserine; Phosphatidylserine detection; Protein lipid binding

Indexed keywords

PHOSPHATIDYLSERINE; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2;

APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE; CELL SURFACE; CELLULAR DISTRIBUTION; ENDOSOME; GOLGI COMPLEX; HEMOSTASIS; INTRACELLULAR SIGNALING; LIPID DEGRADATION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION;

EUKARYOTA;

EID: 84885006979     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-6331-9_10     Document Type: Article

References (178)

1. Ajiro K, Bortner CD, Westmoreland J, Cidlowski JA (2008) An endogenous calcium-dependent, caspase-independent intranuclear degradation pathway in thymocyte nuclei: antagonism by physiological concentrations of K(+) ions. Exp Cell Res 314:1237-1249
2. Aleshin A, Finn RS (2010) SRC: a century of science brought to the clinic. Neoplasia 12:599-607
3. Andersen MH, Graversen H, Fedosov SN et al (2000) Functional analyses of two cellular binding domains of bovine lactadherin. Biochemistry 39: 6200-6206
4. Anderson HA, Maylock CA, Williams JA et al (2003) Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat Immunol 4:87-91
5. Andree HA, Reutelingsperger CP, Hauptmann R et al (1990) Binding of vascular anticoagulant alpha (VAC alpha) to planar phospholipid bilayers. J Biol Chem 265:4923-4928
6. Angelillo-Scherrer A, Burnier L, Lambrechts D et al (2008) Role of Gas6 in erythropoiesis and anemia in mice. J Clin Invest 118:583-596
7. Aoki J, Nagai Y, Hosono H et al (2002) Structure and function of phosphatidylserine-speci fi c phospholipase A1. Biochim Biophys Acta 1582:26-32
8. Arikketh D, Nelson R, Vance JE (2008) De fi ning the importance of phosphatidylserine synthase-1 (PSS1): unexpected viability of PSS1-de fi cient mice. J Biol Chem 283:12888-12897
9. Atkinson K, Fogel S, Henry SA (1980) Yeast mutant defective in phosphatidylserine synthesis. J Biol Chem 255:6653-6661
10. Augereau O, Rossignol R, DeGiorgi F et al (2004) Apoptotic-like mitochondrial events associated to phosphatidylserine exposure in blood platelets induced by local anaesthetics. Thromb Haemost 92:104-113
11. Bai J, Wang P, Chapman ER (2002) C2A activates a cryptic Ca(2+)-triggered membrane penetration activity within the C2B domain of synaptotagmin I. Proc Natl Acad Sci U S A 99:1665-1670
12. Bakowski MA, Braun V, Lam GY et al (2010) The phosphoinositide phosphatase SopB manipulates membrane surface charge and traf fi cking of the Salmonella-containing vacuole. Cell Host Microbe 7:453-462
13. Balasubramanian K, Mirnikjoo B, Schroit AJ (2007) Regulated externalization of phosphatidylserine at the cell surface: implications for apoptosis. J Biol Chem 282:18357-18364
14. Bayascas JR (2008) Dissecting the role of the 3-phosphoinositide- dependent protein kinase-1 (PDK1) signalling pathways. Cell Cycle 7:2978-2982
15. Bellini F, Bruni A (1993) Role of a serum phospholipase A1 in the phosphatidylserine-induced T cell inhibition. FEBS Lett 316:1-4
16. Bergo MO, Gavino BJ, Steenbergen R et al (2002) De fi ning the importance of phosphatidylserine synthase 2 in mice. J Biol Chem 277:47701-47708
17. Bevers EM, Comfurius P, van Rijn JL et al (1982) Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur J Biochem 122:429-436
18. Bevers EM, Wiedmer T, Comfurius P et al (1992) Defective Ca(2+)-induced microvesiculation and de fi cient expression of procoagulant activity in erythrocytes from a patient with a bleeding disorder: a study of the red blood cells of Scott syndrome. Blood 79:380-388
19. Bevers EM, Williamson PL (2010) Phospholipid scramblase: an update. FEBS Lett 584:2724-2730
20. Béguin S, Kumar R (1997) Thrombin, fi brin and platelets: a resonance loop in which von Willebrand factor is a necessary link. Thromb Haemost 78: 590-594
21. Boehning D, Patterson RL, Sedaghat L et al (2003) Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol 5:1051-1061
22. Bollen IC, Higgins JA (1980) Phospholipid asymmetry in rough-and smooth-endoplasmic-reticulum membranes of untreated and phenobarbital-treated rat liver. Biochem J 189:475-480
23. Boon JM, Smith BD (2002) Chemical control of phospholipid distribution across bilayer membranes. Med Res Rev 22:251-281
24. Borisenko GG, Matsura T, Liu S-X et al (2003) Macrophage recognition of externalized phosphatidylserine and phagocytosis of apoptotic Jurkat cells-existence of a threshold. Arch Biochem Biophys 413:41-52
25. Bradshaw JM (2010) The Src, Syk, and Tec family kinases: distinct types of molecular switches. Cell Signal 22:1175-1184
26. Brose N, Petrenko AG, Sudhof TC, Jahn R (1992) Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256:1021-1025
27. Calderon F, Kim H-Y (2008) Detection of intracellular phosphatidylserine in living cells. J Neurochem 104:1271-1279
28. Castoldi E, Collins PW, Williamson PL, Bevers EM (2011) Compound heterozygosity for 2 novel TMEM16F mutations in a patient with Scott syndrome. Blood 117:4399-4400
29. Chattopadhyay A, London E (1987) Parallax method for direct measurement of membrane penetration depth utilizing fl uorescence quenching by spinlabeled phospholipids. Biochemistry 26:39-45
30. Chattopadhyay A, London E (1988) Spectroscopic and ionization properties of N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)-labeled lipids in model membranes. Biochim Biophys Acta 938:24-34
31. Chen CY, Ingram MF, Rosal PH, Graham TR (1999) Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J Cell Biol 147:1223-1236
32. Cosemans JMEM, Van Kruchten R, Olieslagers S et al (2010) Potentiating role of Gas6 and Tyro3, Axl and Mer (TAM) receptors in human and murine platelet activation and thrombus stabilization. J Thromb Haemost 8:1797-1808
33. Dachary-Prigent J, Pasquet JM, Freyssinet JM, Nurden AT (1995) Calcium involvement in aminophospholipid exposure and microparticle formation during platelet activation: a study using Ca2 + ?ATPase inhibitors. Biochemistry 34:11625-11634
34. Daleke DL (2006) Phospholipid fl ippases. J Biol Chem 282:821-825
35. Daleke DL (2003) Regulation of transbilayer plasma membrane phospholipid asymmetry. J Lipid Res 44:233-242
36. Darland-Ransom M, Wang X, Sun C-L et al (2008) Role of C. elegans TAT-1 protein in maintaining plasma membrane phosphatidylserine asymmetry. Science 320:528-531
37. Dasgupta SK, Abdel-Monem H, Niravath P et al (2009) Lactadherin and clearance of platelet-derived microvesicles. Blood 113:1332-1339
38. Epand RM, Stevenson C, Bruins R et al (1998) The chirality of phosphatidylserine and the activation of protein kinase C. Biochemistry 37:12068-12073
39. Estaquier J, Vallette F, Vayssiere J-L, Mignotte B (2012) The mitochondrial pathways of apoptosis. Adv Exp Med Biol 942:157-183
40. Fadok VA, Voelker DR, Campbell PA et al (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers speci fi c recognition and removal by macrophages. J Immunol 148:2207-2216
41. Fairn GD, Hermansson M, Somerharju P, Grinstein S (2011) Phosphatidylserine is polarized and required for proper Cdc42 localization and for development of cell polarity. Nat Cell Biol 13:1424-1430
42. Fairn GD, Schieber NL, Ariotti N et al (2011) Highresolution mapping reveals topologically distinct cellular pools of phosphatidylserine. J Cell Biol 194:257-275
43. Finkielstein CV, Overduin M, Capelluto DGS (2006) Cell migration and signaling speci fi city is determined by the phosphatidylserine recognition motif of Rac1. J Biol Chem 281:27317-27326
44. Frasch SC, Berry KZ, Fernandez-Boyanapalli R et al (2008) NADPH oxidase-dependent generation of lysophosphatidylserine enhances clearance of activated and dying neutrophils via G2A. J Biol Chem 283:33736-33749
45. Frasch SC, Bratton DL (2012) Emerging roles for lysophosphatidylserine in resolution of in fl ammation. Prog Lipid Res 51:199-207
46. Freyssinet J-M, Toti F (2010) Formation of procoagulant microparticles and properties. Thromb Res 125(Suppl 1):S46-S48
47. Ghosh S, Strum JC, Sciorra VA et al (1996) Raf-1 kinase possesses distinct binding domains for phosphatidylserine and phosphatidic acid. Phosphatidic acid regulates the translocation of Raf-1 in 12-O- tetradecanoylphorbol-13-acetate-stimulated Madin-Darby canine kidney cells. J Biol Chem 271:8472-8480
48. Ghosh S, Xie WQ, Quest AF et al (1994) The cysteine-rich region of raf-1 kinase contains zinc, translocates to liposomes, and is adjacent to a segment that binds GTP-ras. J Biol Chem 269: 10000-10007
49. Gilbert GE, Furie BC, Furie B (1990) Binding of human factor VIII to phospholipid vesicles. J Biol Chem 265:815-822
50. Gilbert GE, Kaufman RJ, Arena AA et al (2002) Four hydrophobic amino acids of the factor VIII C2 domain are constituents of both the membranebinding and von Willebrand factor-binding motifs. J Biol Chem 277:6374-6381
51. Graham TR (2004) Flippases and vesicle-mediated protein transport. Trends Cell Biol 14:670-677
52. Greenberg ME, Sun M, Zhang R et al (2006) Oxidized phosphatidylserine- CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J Exp Med 203:2613-2625
53. Hampton MB, Vanags DM, Pörn-Ares MI, Orrenius S (1996) Involvement of extracellular calcium in phosphatidylserine exposure during apoptosis. FEBS Lett 399:277-282
54. Hanayama R, Tanaka M, Miwa K et al (2002) Identi fi cation of a factor that links apoptotic cells to phagocytes. Nature 417:182-187
55. Hancock JF, Magee AI, Childs JE, Marshall CJ (1989) All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57:1167-1177
56. Hancock JF, Paterson H, Marshall CJ (1990) A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 63:133-139
57. Heemskerk JW, Siljander P, Vuist WM et al (1999) Function of glycoprotein VI and integrin alpha2beta1 in the procoagulant response of single, collagenadherent platelets. Thromb Haemost 81:782-792
58. Heemskerk JWM, Bevers EM, Lindhout T (2002) Platelet activation and blood coagulation. Thromb Haemost 88:186-193
59. Hekman M, Hamm H, Villar AV et al (2002) Associations of B-and C-Raf with cholesterol, phosphatidylserine, and lipid second messengers: preferential binding of Raf to arti fi cial lipid rafts. J Biol Chem 277:24090-24102
60. Hicks AM, DeLong CJ, Thomas MJ et al (2006) Unique molecular signatures of glycerophospholipid species in different rat tissues analyzed by tandem mass spectrometry. Biochim Biophys Acta 1761: 1022-1029
61. Higgins JA, Dawson RM (1977) Asymmetry of the phospholipid bilayer of rat liver endoplasmic reticulum. Biochim Biophys Acta 470:342-356
62. Hla T (2004) Prostaglandins & other lipid mediators: a new phase, a new team. Prostaglandins Other Lipid Mediat 73:1-2
63. Hobson JP, Rosenfeldt HM, Barak LS et al (2001) Role of the sphingosine-1-phosphate receptor EDG-1 in PDGF-induced cell motility. Science 291:1800-1803
64. Hoppe AD, Swanson JA (2004) Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis. Mol Biol Cell 15:3509-3519
65. Hosono H, Aoki J, Nagai Y et al (2001) Phosphatidylserine-speci fi c phospholipase A1 stimulates histamine release from rat peritoneal mast cells through production of 2-acyl-1-lysophosphatidylserine. J Biol Chem 276:29664-29670
66. Hua Z, Fatheddin P, Graham TR (2002) An essential subfamily of Drs2p-related P-type ATPases is required for protein traf fi cking between Golgi complex and endosomal/vacuolar system. Mol Biol Cell 13:3162-3177
67. Huang BX, Akbar M, Kevala K, Kim H-Y (2011) Phosphatidylserine is a critical modulator for Akt activation. J Cell Biol 192:979-992
68. Huang M, Rigby AC, Morelli X et al (2003) Structural basis of membrane binding by Gla domains of vitamin K-dependent proteins. Nat Struct Biol 10:751-756
69. Jacquemin MG, Desqueper BG, Benhida A et al (1998) Mechanism and kinetics of factor VIII inactivation: study with an IgG4 monoclonal antibody derived from a hemophilia A patient with inhibitor. Blood 92:496-506
70. Jo D-G, Jun J-I, Chang J-W et al (2004) Calcium binding of ARC mediates regulation of caspase 8 and cell death. Mol Cell Biol 24:9763-9770
71. Johnson KR, Becker KP, Facchinetti MM et al (2002) PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane. Extracellular release of sphingosine-1-phosphate induced by phorbol 12-myristate 13-acetate (PMA). J Biol Chem 277:35257-35262
72. Johnson LM, James KM, Chamberlain MD, Anderson DH (2005) Identi fi cation of key residues in the A-Raf kinase important for phosphoinositide lipid binding specificity. Biochemistry 44:3432-3440
73. Jung EM, Lee T-J, Park J-W et al (2008) The novel phospholipase C activator, m-3M3FBS, induces apoptosis in tumor cells through caspase activation, down-regulation of XIAP and intracellular calcium signaling. Apoptosis 13:133-145
74. Kay JG, Koivusalo M, Ma X et al (2012) Phosphatidylserine dynamics in cellular membranes. Mol Biol Cell 23:2198-2212
75. Kim H-Y (2007) Novel metabolism of docosahexaenoic acid in neural cells. J Biol Chem 282:18661-18665
76. Kim SW, Quinn-Allen MA, Camp JT et al (2000) Identi fi cation of functionally important amino acid residues within the C2-domain of human factor V using alanine-scanning mutagenesis. Biochemistry 39:1951-1958
77. Knight CG, Morton LF, Onley DJ et al (1999) Collagen-platelet interaction: Gly-Pro-Hyp is uniquely speci fi c for platelet Gp VI and mediates platelet activation by collagen. Cardiovasc Res 41:450-457
78. Knight JD, Falke JJ (2009) Single-molecule fl uorescence studies of a PH domain: new insights into the membrane docking reaction. Biophys J 96:566-582
79. Kobayashi N, Karisola P, Peña-Cruz V et al (2007) TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity 27:927-940
80. Koopman G, Reutelingsperger CP, Kuijten GA et al (1994) Annexin V for fl ow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84:1415-1420
81. Laude AJ, Prior IA (2008) Palmitoylation and localisation of RAS isoforms are modulated by the hypervariable linker domain. J Cell Sci 121:421-427
82. Lee MJ, Thangada S, Claffey KP et al (1999) Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell 99:301-312
83. Lemke G, Burstyn-Cohen T (2010) TAM receptors and the clearance of apoptotic cells. Ann N Y Acad Sci 1209:23-29
84. Leventis PA, Grinstein S (2010) The distribution and function of phosphatidylserine in cellular membranes. Annu Rev Biophys 39:407-427
85. Lhermusier T, Chap H, Payrastre B (2011) Platelet membrane phospholipid asymmetry: from the characterization of a scramblase activity to the identi fi cation of an essential protein mutated in Scott syndrome. J Thromb Haemost 9:1883-1891
86. Lin L, Huai Q, Huang M et al (2007) Crystal structure of the bovine lactadherin C2 domain, a membrane binding motif, shows similarity to the C2 domains of factor V and factor VIII. J Mol Biol 371:717-724
87. Lucas N, Cho W (2011) Phosphatidylserine binding is essential for plasma membrane recruitment and signaling function of 3-phosphoinositide dependent kinase-1. J Biol Chem 286(48):41265-41272
88. Macedo-Ribeiro S, Bode W, Huber R et al (1999) Crystal structures of the membrane-binding C2 domain of human coagulation factor V. Nature 402:434-439
89. Mackler JM, Drummond JA, Loewen CA et al (2002) The C(2)B Ca(2+)-binding motif of synaptotagmin is required for synaptic transmission in vivo . Nature 418:340-344
90. Makide K, Kitamura H, Sato Y et al (2009) Emerging lysophospholipid mediators, lysophosphatidylserine, lysophosphatidylthreonine, lysophosphatidylethanolamine and lysophosphatidylglycerol. Prostaglandins Other Lipid Mediat 89:135-139
91. Mapes J, Chen Y-Z, Kim A et al (2012) CED-1, CED-7, and TTR-52 regulate surface phosphatidylserine expression on apoptotic and phagocytic cells. Curr Biol 22(14):1267-1275
92. Marinetti G, Love R (1976) Differential reaction of cell membrane phospholipids and proteins with chemical probes. Chem Phys Lipids 16:239-254
93. Martin OC, Pagano RE (1987) Transbilayer movement of fl uorescent analogs of phosphatidylserine and phosphatidylethanolamine at the plasma membrane of cultured cells. Evidence for a proteinmediated and ATP-dependent process(es). J Biol Chem 262:5890-5898
94. Martin SJ, Finucane DM, Amarante-Mendes GP et al (1996) Phosphatidylserine externalization during CD95-induced apoptosis of cells and cytoplasts requires ICE/CED-3 protease activity. J Biol Chem 271:28753-28756
95. Martin TW, Lagunoff D (1979) Interactions of lysophospholipids and mast cells. Nature 279:250-252
96. Mattson MP, Chan SL (2003) Calcium orchestrates apoptosis. Nat Cell Biol 5:1041-1043
97. McPherson RA, Harding A, Roy S et al (1999) Interactions of c-Raf-1 with phosphatidylserine and 14-3-3. Oncogene 18:3862-3869
98. Meers P, Mealy T (1993) Calcium-dependent annexin V binding to phospholipids: stoichiometry, speci fi city, and the role of negative charge. Biochemistry 32:11711-11721
99. Meers P, Mealy T (1994) Phospholipid determinants for annexin V binding sites and the role of tryptophan. Biochemistry 33:5829-5837
100. Michaelson D, Silletti J, Murphy G et al (2001) Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol 152:111-126
101. Mirnikjoo B, Balasubramanian K, Schroit AJ (2008) Mobilization of lysosomal calcium regulates the externalization of phosphatidylserine during apoptosis. J Biol Chem 284:6918-6923
102. Mirnikjoo B, Balasubramanian K, Schroit AJ (2009) Suicidal membrane repair regulates phosphatidylserine externalization during apoptosis. J Biol Chem 284:22512-22516
103. Mott HR, Carpenter JW, Zhong S et al (1996) The solution structure of the Raf-1 cysteine-rich domain: a novel ras and phospholipid binding site. Proc Natl Acad Sci U S A 93:8312-8317
104. Mukherjee S, Chattopadhyay A, Samanta A, Soujanya T (1994) Dipole moment change of NBD group upon excitation studied using solvatochromic and quantum chemical approaches: implications in membrane research. J Phys Chem 98:2809-2812
105. Muñoz-Pinedo C (2012) Signaling pathways that regulate life and cell death: evolution of apoptosis in the context of self-defense. Adv Exp Med Biol 738:124-143
106. Murata-Kamiya N, Kikuchi K, Hayashi T et al (2010) Helicobacter pylori exploits host membrane phosphatidylserine for delivery, localization, and pathophysiological action of the CagA oncoprotein. Cell Host Microbe 7:399-411
107. Nagata S, Hanayama R, Kawane K (2010) Autoimmunity and the clearance of dead cells. Cell 140:619-630
108. Nakano T, Ishimoto Y, Kishino J et al (1997) Cell adhesion to phosphatidylserine mediated by a product of growth arrest-speci fi c gene 6. J Biol Chem 272:29411-29414
109. Natarajan P, Wang J, Hua Z, Graham TR (2004) Drs2p-coupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc Natl Acad Sci U S A 101:10614-10619
110. Navarro-Lérida I, Sánchez-Perales S, Calvo M et al (2012) A palmitoylation switch mechanism regulates Rac1 function and membrane organization. EMBO J 31:534-551
111. Needham D, Zhelev DV (1995) Lysolipid exchange with lipid vesicle membranes. Ann Biomed Eng 23:287-298
112. Nikawa JI, Yamashita S (1981) Characterization of phosphatidylserine synthase from Saccharomyces cerevisiae and a mutant defective in the enzyme. Biochim Biophys Acta 665:420-426
113. Okeley NM, Gelb MH (2004) A designed probe for acidic phospholipids reveals the unique enriched anionic character of the cytosolic face of the mammalian plasma membrane. J Biol Chem 279:21833-21840
114. Padilla-López S, Langager D, Chan C-H, Pearce DA (2012) BTN1, the Saccharomyces cerevisiae homolog to the human Batten disease gene, is involved in phospholipid distribution. Dis Model Mech 5:191-199
115. Park D, Tosello-Trampont A-C, Elliott MR et al (2007) BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 450:430-434
116. Park KS, Lee H-Y, Kim M-K et al (2006) Lysophosphatidylserine stimulates L2071 mouse fi broblast chemotactic migration via a process involving pertussis toxin-sensitive trimeric G-proteins. Mol Pharmacol 69:1066-1073
117. Park S-Y, Jung M-Y, Kim H-J et al (2008) Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ 15: 192-201
118. Park S-Y, Kim S-Y, Jung M-Y et al (2008) Epidermal growth factor-like domain repeat of stabilin-2 recognizes phosphatidylserine during cell corpse clearance. Mol Cell Biol 28:5288-5298
119. Paulusma CC, Elferink RPJO (2010) P4 ATPases-the physiological relevance of lipid fl ipping transporters. FEBS Lett 584:2708-2716
120. Pitson SM, Moretti PAB, Zebol JR et al (2003) Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J 22:5491-5500
121. Pomorski T, Lombardi R, Riezman H et al (2003) Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol Biol Cell 14:1240-1254
122. Pratt KP, Shen BW, Takeshima K et al (1999) Structure of the C2 domain of human factor VIII at 1.5 A resolution. Nature 402:439-442
123. Ravichandran KS (2011) Beginnings of a good apoptotic meal: the fi nd-me and eat-me signaling pathways. Immunity 35:445-455
124. Reverter JC, Béguin S, Kessels H et al (1996) Inhibition of platelet-mediated, tissue factor-induced thrombin generation by the mouse/human chimeric 7E3 antibody. Potential implications for the effect of c7E3 Fab treatment on acute thrombosis and "clinical restenosis". J Clin Invest 98:863-874
125. Rosing J, Bevers EM, Comfurius P et al (1985) Impaired factor X and prothrombin activation associated with decreased phospholipid exposure in platelets from a patient with a bleeding disorder. Blood 65:1557-1561
126. Rosing J, Tans G, Govers-Riemslag JW et al (1980) The role of phospholipids and factor Va in the prothrombinase complex. J Biol Chem 255:274-283
127. Rosse C, Linch M, Kermorgant S et al (2010) PKC and the control of localized signal dynamics. Nat Rev Mol Cell Biol 11:103-112
128. Sahu SK, Gummadi SN, Manoj N, Aradhyam GK (2007) Phospholipid scramblases: an overview. Arch Biochem Biophys 462:103-114
129. Saito K, Nishijima M, Kuge O (1998) Genetic evidence that phosphatidylserine synthase II catalyzes the conversion of phosphatidylethanolamine to phosphatidylserine in Chinese hamster ovary cells. J Biol Chem 273:17199-17205
130. Santiago C, Ballesteros A, Martínez-Muñoz L et al (2007) Structures of T cell immunoglobulin mucin protein 4 show a metal-Ion-dependent ligand binding site where phosphatidylserine binds. Immunity 27:941-951
131. Sato T, Aoki J, Nagai Y et al (1997) Serine phospholipid-speci fi c phospholipase A that is secreted from activated platelets. A new member of the lipase family. J Biol Chem 272:2192-2198
132. Schick PK, Kurica KB, Chacko GK (1976) Location of phosphatidylethanolamine and phosphatidylserine in the human platelet plasma membrane. J Clin Invest 57:1221-1226
133. Schoenwaelder SM, Yuan Y, Josefsson EC et al (2009) Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 114:663-666
134. Sebastian TT, Baldridge RD, Xu P, Graham TR (2011) Phospholipid fl ippases: building asymmetric membranes and transport vesicles. Biochim Biophys Acta 1821(8):1068-1077
135. Seigneuret M, Devaux PF (1984) ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc Natl Acad Sci U S A 81:3751-3755
136. Shao C, Novakovic VA, Head JF et al (2008) Crystal structure of lactadherin C2 domain at 1.7A resolution with mutational and computational analyses of its membrane-binding motif. J Biol Chem 283: 7230-7241
137. Shi J, Gilbert GE (2003) Lactadherin inhibits enzyme complexes of blood coagulation by competing for phospholipid-binding sites. Blood 101:2628-2636
138. Shi J, Heegaard CW, Rasmussen JT, Gilbert GE (2004) Lactadherin binds selectively to membranes containing phosphatidyl-L-serine and increased curvature. Biochim Biophys Acta 1667:82-90
139. Shi J, Shi Y, Waehrens LN et al (2006) Lactadherin detects early phosphatidylserine exposure on immortalized leukemia cells undergoing programmed cell death. Cytometry 69:1193-1201
140. Shiao YJ, Balcerzak B, Vance JE (1998) A mitochondrial membrane protein is required for translocation of phosphatidylserine from mitochondria-associated membranes to mitochondria. Biochem J 331 (Pt 1): 217-223
141. Sigal CT, Zhou W, Buser CA et al (1994) Aminoterminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids. Proc Natl Acad Sci U S A 91: 12253-12257
142. Smith GA, Hesketh TR, Plumb RW, Metcalfe JC (1979) The exogenous lipid requirement for histamine release from rat peritoneal mast cells stimulated by concanavalin A. FEBS Lett 105:58-62
143. Sperka-Gottlieb CD, Hermetter A, Paltauf F, Daum G (1988) Lipid topology and physical properties of the outer mitochondrial membrane of the yeast, Saccharomyces cerevisiae . Biochim Biophys Acta 946:227-234
144. Stahelin RV, Hwang JH, Kim J-H et al (2005) The mechanism of membrane targeting of human sphingosine kinase 1. J Biol Chem 280:43030-43038
145. Steenbergen R, Nanowski TS, Beigneux A et al (2005) Disruption of the phosphatidylserine decarboxylase gene in mice causes embryonic lethality and mitochondrial defects. J Biol Chem 280: 40032-40040
146. Stein A, Radhakrishnan A, Riedel D et al (2007) Synaptotagmin activates membrane fusion through a Ca2+?dependent trans interaction with phospholipids. Nat Struct Mol Biol 14:904-911
147. Stevens CF, Sullivan JM (2003) The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39:299-308
148. Sutton RB, Sprang SR (1998) Structure of the protein kinase Cbeta phospholipid-binding C2 domain complexed with Ca2+. Structure 6:1395-1405
149. Suzuki J, Umeda M, Sims PJ, Nagata S (2010) Calcium-dependent phospholipid scrambling by TMEM16F. Nature 468:834-838
150. Südhof TC (2002) Synaptotagmins: why so many? J Biol Chem 277:7629-7632
151. Swairjo MA, Concha NO, Kaetzel MA et al (1995) Ca(2+)-bridging mechanism and phospholipid head group recognition in the membrane-binding protein annexin V. Nat Struct Biol 2:968-974
152. Takai Y, Kishimoto A, Iwasa Y et al (1979) Calciumdependent activation of a multifunctional protein kinase by membrane phospholipids. J Biol Chem 254:3692-3695
153. Takai Y, Kishimoto A, Kikkawa U et al (1979) Unsaturated diacylglycerol as a possible messenger for the activation of calcium-activated, phospholipiddependent protein kinase system. Biochem Biophys Res Commun 91:1218-1224
154. Tang X, Halleck MS, Schlegel RA, Williamson P (1996) A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 272:1495-1497
155. Tyurin VA, Tyurina YY, Kochanek PM et al (2008) Oxidative lipidomics of programmed cell death. Methods Enzymol 442:375-393
156. Uchida Y, Hasegawa J, Chinnapen D et al (2011) Intracellular phosphatidylserine is essential for retrograde membrane traf fi c through endosomes. Proc Natl Acad Sci U S A 108:15846-15851
157. Udell CM, Rajakulendran T, Sicheri F, Therrien M (2011) Mechanistic principles of RAF kinase signaling. Cell Mol Life Sci 68:553-565
158. Vale MG (1977) Localization of the amino phospholipids in sarcoplasmic reticulum membranes revealed by trinitrobenzenesulfonate and fl uorodinitrobenzene. Biochim Biophys Acta 471:39-48
159. van de Waart P, Bruls H, Hemker HC, Lindhout T (1983) Interaction of bovine blood clotting factor Va and its subunits with phospholipid vesicles. Biochemistry 22:2427-2432
160. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112-124
161. Vance JE (2008) Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids. J Lipid Res 49:1377-1387
162. Vance JE (2003) Molecular and cell biology of phosphatidylserine and phosphatidylethanolamine metabolism. Prog Nucleic Acid Res Mol Biol 75:69-111
163. Vance JE, Steenbergen R (2005) Metabolism and functions of phosphatidylserine. Prog Lipid Res 44:207-234
164. Verdaguer N, Corbalan-Garcia S, Ochoa WF et al (1999) Ca(2+) bridges the C2 membrane-binding domain of protein kinase Calpha directly to phosphatidylserine. EMBO J 18:6329-6338
165. Weiss HJ, Vicic WJ, Lages BA, Rogers J (1979) Isolated de fi ciency of platelet procoagulant activity. Am J Med 67:206-213
166. Wennerberg K, Rossman KL, Der CJ (2005) The Ras superfamily at a glance. J Cell Sci 118: 843-846
167. Williamson P, Bevers EM, Smeets EF et al (1995) Continuous analysis of the mechanism of activated transbilayer lipid movement in platelets. Biochemistry 34:10448-10455
168. Williamson P, Christie A, Kohlin T et al (2001) Phospholipid scramblase activation pathways in lymphocytes. Biochemistry 40:8065-8072
169. Williamson P, Schlegel RA (2002) Transbilayer phospholipid movement and the clearance of apoptotic cells. Biochim Biophys Acta 1585:53-63
170. Yamaguchi H, Takagi J, Miyamae T et al (2008) Milk fat globule EGF factor 8 in the serum of human patients of systemic lupus erythematosus. J Leukoc Biol 83:1300-1307
171. Yáñez M, Gil-Longo J, Campos-Toimil M (2012) Calcium binding proteins. Adv Exp Med Biol 740:461-482
172. Yeung T, Gilbert GE, Shi J et al (2008) Membrane phosphatidylserine regulates surface charge and protein localization. Science 319:210-213
173. Yeung T, Heit B, Dubuisson J-F et al (2009) Contribution of phosphatidylserine to membrane surface charge and protein targeting during phagosome maturation. J Cell Biol 185:917-928
174. Yeung T, Terebiznik M, Yu L et al (2006) Receptor activation alters inner surface potential during phagocytosis. Science 313:347-351
175. Zhang Z, Hui E, Chapman ER, Jackson MB (2009) Phosphatidylserine regulation of Ca2+?triggered exocytosis and fusion pores in PC12 cells. Mol Biol Cell 20:5086-5095
176. Züllig S, Neukomm LJ, Jovanovic M et al (2007) Aminophospholipid translocase TAT-1 promotes phosphatidylserine exposure during C. elegans apoptosis. Curr Biol 17:994-999
177. Zwaal RF, Comfurius P, van Deenen LL (1977) Membrane asymmetry and blood coagulation. Nature 268:358-360
178. Zwaal RFA, Comfurius P, Bevers EM (2005) Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 62:971-988