Phosphatidylserine in the brain: Metabolism and function

Progress in Lipid Research

Volumn 56, Issue 1, 2014, Pages 1-18

  Kim, Hee Yong ^a   Huang, Bill X ^a   Spector, Arthur A ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Cognition; Docosahexaenoic acid; Membranes; Neuron; Serine; Signal transduction

Indexed keywords

ALCOHOL; AMINOPHOSPHOLIPID TRANSLOCASE; CARRIER PROTEIN; DOCOSAHEXAENOIC ACID; ETHER DERIVATIVE; LYSOPHOSPHATIDYLSERINE; MEMBRANE PROTEIN; N ACYLPHOSPHATIDYLSERINE; N ACYLSERINE; NEUROTRANSMITTER; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLSERINE; PHOSPHATIDYLSERINE ALKYL ETHER DERIVATIVE; PHOSPHATIDYLSERINE DECARBOXYLASE; PHOSPHATIDYLSERINE SYNTHASE; PHOSPHATIDYLSERINE SYNTHASE 1; PHOSPHATIDYLSERINE SYNTHASE 2; PLASMALOGEN; PROTEIN KINASE B; PROTEIN KINASE C; RAF PROTEIN; RAS PROTEIN; SERINC PROTEIN; SERINE; SERINE DERIVATIVE; UNCLASSIFIED DRUG; ALKYL ETHER; BASP1 PROTEIN; CANNABINOID 2 RECEPTOR; DIACYLGLYCEROL KINASE; EVECTIN 2; GLYCEROPHOSPHOLIPID; LACTADHERIN; N PALMITOYLSERINE; N STEAROYLSERINE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN KINASE C ALPHA; SPHINGOSINE KINASE 1; SYNAPSIN I; TAU PROTEIN;

ABSENCE OF SIDE EFFECTS; ALCOHOL CONSUMPTION; BRAIN FUNCTION; CELL MEMBRANE; CELL SURVIVAL; CLINICAL TRIAL (TOPIC); COGNITIVE DEFECT; CONTROLLED CLINICAL TRIAL (TOPIC); CYTOPLASM; DIET SUPPLEMENTATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; EVIDENCE BASED MEDICINE; EXOCYTOSIS; GENE DELETION; HUMAN; INTRACELLULAR TRANSPORT; LIPID BRAIN LEVEL; LIPID COMPOSITION; MEMORY; MEMORY DISORDER; MENTAL STRESS; NERVE CELL DIFFERENTIATION; NERVE CELL MEMBRANE; NEUROPROTECTION; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOSPHOLIPID METABOLISM; PHOSPHOLIPID TRANSFER; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LIPID INTERACTION; REVIEW; SIGNAL TRANSDUCTION; WORD RECOGNITION; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; BRAIN; CELL DIFFERENTIATION; CYTOLOGY; METABOLISM; NERVE CELL; ASTROCYTE; CELL TRANSPORT; LIPOGENESIS; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

ANIMALS; BIOSYNTHETIC PATHWAYS; BRAIN; CELL DIFFERENTIATION; CELL SURVIVAL; DOCOSAHEXAENOIC ACIDS; HUMANS; MODELS, BIOLOGICAL; NEURONS; PHOSPHATIDYLSERINES;

EID: 84904974702     PISSN: 01637827     EISSN: 18732194     Source Type: Journal    
DOI: 10.1016/j.plipres.2014.06.002     Document Type: Review

References (200)

1. L. Svennerholm Distribution and fatty acid composition of normal human brain J Lipid Res 9 1968 570 579
2. M. Akbar, F. Calderon, Z. Wen, and H.Y. Kim Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal surv (Pubitemid 41105957)
3. B.X. Huang, M. Akbar, K. Kevala, and H.Y. Kim Phosphatidylserine is a critical modulator for Akt activation J Cell Biol 192 2011 979 992
4. H.Y. Kim, M. Akbar, A. Lau, and L. Edsall Inhibition of neuronal apoptosis by docosahexaenoic acid (22:6n-3): role of phosphatidylserine in antiapoptotic effect J Biol Chem 275 2000 35215 35223
5. H.Y. Kim Novel metabolism of docosahexaenoic acid in neural cells J Biol Chem 282 2007 18661 18665
6. H.Y. Kim, M. Akbar, and Y.S. Kim Phosphatidylserine-dependent neuroprotective signaling promoted by docosahexaenoic acid Prostaglandins Leukot Essent Fatty Acids 82 2010 165 172
7. A.C. Newton, and L.M. Keranen Phosphatidyl-l-serine is necessary for protein kinase C's high-affinity interaction with diacylglycerol-containing membranes Biochemistry 33 1994 6651 6658 (Pubitemid 24189380)
8. N. Brose, A.G. Petrenko, T.C. Sudhof, and R. Jahn Synaptotagmin: a calcium sensor on the synaptic vesicle surface necessary for protein kinase C's high-affinity interaction with diacylglycerol-containing membranes Science 256 1994 1021 1025
9. G.J. Augustine How does calcium trigger neurotransmitter release? Curr Opin Neurobiol 11 2001 320 326 (Pubitemid 32524097)
10. 2+-regulated membrane fusion by synaptotagmin and SNAREs Science 304 2004 435 438 (Pubitemid 38495938)
11. S.M. Dennison, M.E. Bowen, A.T. Brunger, and B.R. Lentz Neuronal SNAREs do not trigger fusion between synthetic membranes but do promote PGE-mediated membrane fusion Biophys J 90 2006 1661 1675
12. M. Baudry, G. Massicotti, and S. Hauge Phosphatidylserine increases the affinity of the AMPA/quasqualate receptor in rat brain membranes Behav Neural Biol 55 1991 137 140
13. J. Murray, L. Cuccia, A. Ianoul, J.J. Cheetham, and L.J. Johnston Imaging the selective binding of synapsin to anionic membrane domains ChemBioChem 5 2004 1489 1494 (Pubitemid 39531661)
14. T.B. Shea Phospholipids alter tau conformation, phosphorylation, proteolysis, and association with microtubules: implication for tau function under normal and degenerative conditions J Neurosci Res 50 1997 114 122 (Pubitemid 27433358)
15. M.L. Bader Lange, G. Cenini, M. Piroddi, H.M. Abdul, R. Sultana, and F. Galli et al. Loss of phospholipid asymmetry and elevated brain apoptotic protein levels in subjects with amnestic mild cognitive impairment and Alzheimer disease Neurobiol Dis 29 2008 456 463
16. R. Mozzi, S. Buratta, and G. Goracci Metabolism and function of phosphatidylserine in mammalian brain Neurochem Res 28 2003 195 214 (Pubitemid 36207345)
17. J.E. Vance Molecular and cell biology of phosphatidylserine and phosphatidylethanolamine metabolism Prog Nucleic Acid Res Mol Biol 75 2003 69 111 (Pubitemid 137639555)
18. O. Kuge, and M. Nishijima Biosynthetic regulation and intracellular transport of phosphatidylserine in mammalian cells J Biochem 133 2003 397 403 (Pubitemid 36604683)
19. J.E. Vance, and D.E. Vance Phospholipid biosynthesis in mammalian cells Biochem Cell Biol 82 2004 113 128 (Pubitemid 38580878)
20. J.E. Vance Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids J Lipid Res 49 2008 1377 1387
21. D.E. Vance, and J.E. Vance Physiological consequences of disruption of mammalian phospholipid biosynthetic genes J Lipid Res 50 2009 S132 S137
22. J.E. Vance, and G. Tasseva Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells Biochem Biophy Acta 18312 2013 543 554
23. P.A. Leventis, and S. Grinstein The distribution and function of phosphatidylserine in cellular membranes Annu Rev Biophys 39 2010 407 427
24. J.E. Vance Phospholipid synthesis in a membrane fraction associated with mitochondria J Biol Chem 265 1990 7248 7256
25. B. Sturbois-Balcerzak, S.J. Stone, A. Sreenivas, and J.E. Vance Structure and expression of the murine phosphatidylserine synthase-1 gene J Biol Chem 276 2001 8205 8212
26. S. Buratta, M. Felicetti, and R. Mozzi Synthesis of phosphatidylserine by base exchange in Triton-insoluble floating fractions from rat cerebellum J Neurochem 103 2007 942 951 (Pubitemid 47568712)
27. S. Buratta, G. Ferrera, and R. Mozzi Presence of phosphatidylserine synthesizing enzymes in the triton insoluble floating fractions from cerebrocortical plasma membranes. Do phosphatidylserine synthesizing enzymes in plasma membrane microdomains play a role in signal transduction? Neurochem Res 36 2011 774 782
28. I.S. Mikhaevitch, I.N. Singh, G. Sorrentino, R. Massarelli, and J.N. Kanfer Modulation of phosphatidylserine synthesis by a muscarinic receptor occupancy in human neuroblastoma cell line LA-N-1 Biochem J 299 1994 375 380 (Pubitemid 24114128)
29. M. Brunetti, A. Gaiti, and G. Porcellati Synthesis of phosphatidylcholine and phosphatidylethanolamine at different ages in the rat brain in vitro Lipids 11 1979 925 931 (Pubitemid 10141960)
30. J.M. Carter, K.A. Waite, R.B. Campenot, J.E. Vance, and D.E. Vance Enhanced expression and activation of CTP:phosphocholine cytidylyltransferase β2 during neurite outgrowth J Biol Chem 278 2003 44988 44994 (Pubitemid 37377258)
31. H. Marcucci, L. Paoletti, S. Jackowski, and C. Banchio Phosphatidylcholine biosynthesis during neuronal differentiation and its role in cell fate determination J Biol Chem 285 2010 25382 25393
32. C.J. Pynn, N.G. Henderson, H. Clark, G. Kostner, W. Bernhard, and A.D. Postle Specificity and rate of human and mouse liver and plasma phosphatidylcholine synthesis analyzed in vivo J Lipid Res 52 2011 399 407
33. R. Mozzi, and G. Porcellati Conversion of phosphatidylethanolamine to phosphatidylcholine in rat brain by the methylation pathway FEBS Lett 100 1979 363 366 (Pubitemid 9174911)
34. J.K. Blusztajn, S.H. Zeisel, and R.J. Wurtman Synthesis of lecithin (phosphatidylcholine) from phosphatidylethanolamine in bovine brain Brain Res 179 1979 319 329
35. J.E. Vance, D. Pau, R.B. Campenot, M. Bussière, and D.E. Vance Evidence that the major membrane lipids except cholesterol, are made in axons of cultured rat sympathetic neurons J Neurochem 62 1994 329 337
36. D.E. Vance Phospholipid methylation in mammals: from biochemistry to physiological function Biochim Biophys Acta 1838 2014 1477 1487
37. K.A. da Costa, K.S. Rai, C.N. Cracinescu, K. Parikh, M.G. Mehedint, and L.M. Sanders et al. Dietary docosahexaenoic acid supplementation modulates hippocampal development in the Pemt-/- mouse J Biol Chem 285 2010 1008 1015
38. R. Steenbergen, T.S. Nanowski, R. Nelson, S.G. Young, and J.E. Vance Phospholipid homeostasis in phosphatidylserine synthase-2-deficient mice Biochim Biophys Acta 1761 2006 313 323
39. G. Tasseva, L. Cole, and J.E. Vance N-Myc and Sp regulate phosphatidylserine synthase-1 expression in brain and glial cells J Biol Chem 286 2011 1061 1073
40. H.Y. Kim, J. Bigelow, and J.H. Kevala Substrate preference in phosphatidylserine biosynthesis for docosahexaenoic acid containing species Biochemistry 43 2004 1030 1036 (Pubitemid 38141502)
41. Y. Sugiura, Y. Konishi, N. Zaima, S. Kajihara, H. Nakanishi, and R. Taguchi et al. Visualization of the cell-selective distribution of PUFA-containing phosphatidylcholines in mouse brain by imaging mass spectrometry J Lipid Res 50 2009 1766 1788
42. O. Kuge, K. Hasegawa, T. Ohsawa, K. Saito, and M. Nishijima Purification and characterization of Chinese hamster phosphatidylserine synthase 2 J Biol Chem 278 2003 42692 42698 (Pubitemid 37310544)
43. S. Tomohiro, A. Kawaguti, Y. Kawabe, S. Kitada, and O. Kuge Purification and characterization of human phosphatidylserine synthases 1 and 2 Biochem J 418 2009 421 429
44. A.K. Kimura, and H.Y. Kim Phosphatidylserine synthase 2: high efficiency for synthesizing phosphatidylserine containing docosahexaenoic acid J Lipid Res 54 2013 214 222
45. D. Arikketh, R. Nelson, and J.E. Vance Defining the importance of phosphatidylserine synthase-1 (PSS1): unexpected viability of PSS1-deficient mice J Biol Chem 283 2008 12888 12897
46. M.O. Bergo, B.J. Gavino, R. Steenbergen, B. Sturbois, A.F. Parlow, and D.A. Sanan et al. Defining the importance of phosphatidylserine synthase 2 in mice J Biol Chem 277 2002 47701 47708 (Pubitemid 36159293)
47. C.W. Cotman, M.L. Blank, A. Moehl, and F. Snyder Lipid composition of synaptic plasma membranes isolated from rat brain by zonal centrifugation Biochemistry 8 1969 4606 4612
48. W.C. Breckenridge, G. Gombos, and I.G. Morgan The lipid composition of adult rat brain synaptosomal plasma membranes Biochim Biophys Acta 266 1972 695 707
49. M. Murthy, J. Hamilton, R.S. Greiner, T. Moriguchi, N. Salem Jr, and H.Y. Kim Differential effects of n-3 fatty acid deficiency on phospholipid molecular species composition in the rat hippocampus J Lipid Res 43 2002 611 617
50. J. Hamilton, R. Greiner, N. Salem Jr, and H.Y. Kim N-3 fatty acid deficiency decreases phosphatidylserine accumulation selectively in neuronal tissues Lipids 35 2000 863 869
51. J.S. O'Brien, D.L. Fillerup, and J.F. Mead Quantification and fatty acid and fatty aldehyde composition of the ethanolamine, choline, and serine glycerophosphatides in human cerebral grey and white matter J Lipid Res 5 1964 329 338
52. H. Yabuuchi, and J.S. O'Brien Positional distribution of fatty acids in glycerophosphatides of bovine gray matter J Lipid Res 9 1968 65 67
53. E. Yavin, and B.P. Zeigler Regulation of phospholipid metabolism in differentiating cells from rat brain cerebral hemispheres in culture. Serine incorporation into serine phosphoglycerides: base exchange and decarboxylation patterns J Biol Chem 252 1977 260 267 (Pubitemid 8020636)
54. M. Butler, and P. Morell The role of phosphatidylserine decarboxylase in brain phospholipid metabolism J Neurochem 41 1983 1445 1454 (Pubitemid 14227460)
55. L.A. Horrocks The alk-1-enyl group content of mammalian myelin phosphoglycerides by quantitative two-dimensional thin-layer chromatography J Lipid Res 9 1968 469 472
56. J.M. Deeley, M.C. Thomas, R.J.W. Truscott, T.W. Mitchell, and S.J. Blanksby Identification of abundant alkyl ether glycerophospholipids in the human lens by tandem mass spectrometry techniques Anal Chem 81 2009 1920 1930
57. K. Nagy, V.V. Brahmbhatt, O. Berdeaux, L. Bretillon, F. Destaillats, and N. Acar Comparative study of serine plasmalogens in human retina and optic nerve: identification of atypical species with odd carbon chains J Lipid Res 53 2012 776 783
58. W.H. Stein, and S. Moore The free amino acids of human blood plasma J Biol Chem 211 1954 915 926
59. +-dependent neutral amino acid transporters A, ASC, and N of the blood-brain barrier: mechanisms for neutral amino acid removal Am J Physiol 287 2004 E622 E629
60. Y. Hirabayashi, and S. Furuya Roles of l-serine and sphingolipid synthesis in brain development and neuronal survival Prog Lipid Res 47 2008 188 203
61. G.B. Phillips, and G.T. Dodge Composition of phospholipids and of phospholipid fatty acids of human plasma J Lipid Res 8 1967 676 681
62. S. Méresse, C. Delbart, J.C. Fruchart, and R. Cecchelli Low-density lipoprotein receptor on endothelium of brain capillaries J Neurochem 53 1989 340 345 (Pubitemid 19186064)
63. H.E. De Vries, B. Breedveld, J. Kuiper, A.G. De Boer, T.J.C. Van Berkel, and D.D. Breimer High-density lipoprotein and cerebral endothelial cells in vitro: interactions and transport Biochem Pharmacol 50 1995 271 273
64. B. Dehouck, L. Fenart, M.P. Dehouck, A. Pierce, G. Torpier, and R. Cecchelli A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier J Cell Biol 138 1997 877 889 (Pubitemid 27365049)
65. J.M. Dietschy, and S.D. Turley Cholesterol metabolism in the central nervous system during early development and in the mature animal J Lipid Res 45 2004 1375 1397 (Pubitemid 39022664)
66. M. Inuzuka, M. Hayakawa, and T. Ingi Serinc, an activity-regulated protein family, incorporates serine into membrane lipid synthesis J Biol Chem 280 2005 35776 35783 (Pubitemid 41532771)
67. C. Vargas-Lopes, C. Madeira, S.A. Kahn, I. Albino do Couto, P. Bado, and J.C. Houzel Protein kinase C activity regulates d-serine availability in the brain J Neurochem 116 2011 281 290
68. A.R. Rutter, R.L. Fradley, E.M. Garrett, K.L. Chapman, J.M. Lawrence, and T.W. Rosahl et al. Evidence from gene knockout studies implicates Asc-1 as the primary transporter mediating d-serine uptake in the mouse CNS Eur J Neurosci 25 2007 1757 1766 (Pubitemid 46550015)
69. L. Pollegioni, and S. Sacchi Metabolism of the neuromodulator d-serine Cell Mol Life Sci 67 2010 2387-14
70. T. Omori, H. Mihara, T. Kurihara, and N. Esaki Occurrence of phosphatidyl-d-serine in the rat cerebrum Biochem Biophys Res Commun 382 2009 415 418
71. T. Omori, H. Mihara, T. Kurihara, and N. Esaki The distribution of phosphatidyl-d-serine in the rat Biosci Biotechnol Biochem 74 2010 1953 1955
72. J.H. Yang, A. Wada, K. Yoshida, Y. Miyoshi, T. Sayano, and K. Esaki et al. Brain-specific Phgdh deletion reveals a pivotal role for l-serine biosynthesis in controlling the level of d-serine, an N-methyl-d-aspartate receptor co-agonist, in adult brain J Biol Chem 285 2010 41380 41390
73. L.P. Diniz, J.C. Almeida, V. Tortelli, C.V. Lopes, P. Setti-Perdigão, and J. Stipurski et al. Astrocyte-induced synaptogenesis is mediated by transforming growth factor β signaling through modulation of d-serine levels in cerebral cortex neurons J Biol Chem 287 2012 41432 41445
74. M. Thompson, J.C. Marecki, S. Marinesco, V. Labrie, J.C. Roder, and S.W. Barger et al. Paradoxical roles of serine racemase and d-serine in the G93A mSOD1 mouse model of amyotrophic lateral sclerosis J Neurochem 120 2012 598 610
75. D.R. Voelker Reconstitution of phosphatidylserine import into rat liver mitochondria J Biol Chem 264 1989 8019 8025 (Pubitemid 19137283)
76. Y. Uchida, J. Hasegawa, D. Chinnapen, T. Inoue, S. Okazaki, and R. Kato et al. Intracellular phosphatidylserine is essential for retrograde membrane traffic through endosomes Proc Natl Acad Sci USA 108 2011 15846 15851
77. K.J. Cho, J.H. Park, A.M. Piggott, A.A. Salim, A.A. Gorfe, and R.G. Parton et al. Staurosporines disrupt phosphatidylserine trafficking and mislocalize Ras proteins J Biol Chem 287 2012 43573 43584
78. K. Maeda, K. Anand, A. Chiapparino, A. Kumar, M. Poletto, and M. Kaksonen et al. Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins Nature 501 2013 257 261
79. J.A. Coleman, M.C.M. Kwok, and R.S. Molday Localization, purification, and functional reconstitution of the P4-ATPase Atp8a2, a phosphatidylserine flippase in photoreceptor disc membranes J Biol Chem 284 2009 32670 32679
80. R.D. Baldridge, and T.R. Graham Identification of residues defining phospholipid flippase substrate specificity of type IV ATPqases Proc Nat Acad Sci USA 109 2012 E290 E298
81. V.A. Fadok, D.R. Voelker, P.A. Campbell, J.J. Cohen, D.L. Brantton, and P.M. Henson Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages J Immunol 148 1992 2207 2216
82. E.M. Bevers, P. Comfurius, J.L. van Rijn, H.C. Hemker, and R.F. Zwaal Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets Eur J Biochem 122 1982 429 436 (Pubitemid 12152078)
83. C. Cusulin, E. Monni, H. Ahlenius, J. Wood, J.C. Brune, and O. Lindvall et al. Embryonic stem cell-derived neural stem cells fuse with microglia and mature neurons Stem Cells 30 2012 2657 2671
84. F. Calderon, and H.Y. Kim Detection of intracellular phosphatidylserine in living cells J Neurochem 104 2008 1271 1279 (Pubitemid 351293340)
85. T. Yeung, G.E. Gilbert, J. Shi, A. Kapus, and S. Grinstein Membrane phosphatidylserine regulates surface charge and protein localization Science 319 2008 210 213
86. D.L. Daleke Phospholipid flippases J Biol Chem. 282 2007 821 825 (Pubitemid 47076513)
87. D.L. Daleke Regulation of transbilayer plasma membrane phospholipid asymmetry J Lipid Res 44 2003 233 242 (Pubitemid 37303867)
88. J. Ding, Z. Wu, B.P. Crider, Y. Ma, X. Li, and C. Slaughter et al. Identification and functional expression of four isoforms of ATPase II, the putative aminophospholipid translocase: effect of isoform variation of the ATPase activity and phospholipid selectivity J Biol Chem 275 2000 23378 23386 (Pubitemid 30646241)
89. M. Meguro, A. Kashigawi, K. Mitsuya, M. Nakao, I. Kondo, and S. Saitoh et al. A novel maternally expressed gene, ATP10C, encodes a putative aminophospholipid translocase associated with Angelman syndrome Nat Genet 28 2001 19 20 (Pubitemid 32405810)
90. K. Levano, V. Punia, M. Raghunath, P.R. Debata, G.M. Curcio, and A. Mogha et al. Atp8a1 deficiency is associated with phosphatidylserine externalization in the hippocampus and delayed hippocampus-dependent learning J Neurochem 120 2012 302 313
91. X. Zhu, R.T. Libby, W.N. de Vries, R.S. Smith, D.L. Wright, and R.T. Bronson Mutations of a P-type ATPase gene cause axonal degeneration PLoS Genet 8 8 2012 e1002853
92. J.A. Coleman, X. Zhu, H.R. Djajadi, L.L. Molday, R.S. Smith, and R.T. Libby et al. Phospholipid flippase ATP8A2 is required for normal visual and auditory function and photoreceptor and spiral ganglion cell survival J Cell Sci 127 2014 1138 1149
93. D.R. Voelker, and J.L. Frazier Isolation and characterization of a Chinese hamster ovary cell line requiring ethanolamine or phosphatidylserine for growth and exhibiting defective phosphatidylserine synthase activity J Biol Chem 261 1986 1002 1008 (Pubitemid 16144756)
94. L.F. Borkenhagen, E.P. Kennedy, and L. Fielding Enzymatic formation and decarboxylation of phosphatidylserine J Biol Chem 236 1961 PC28 PC30
95. A. Ikemoto, T. Kobayashi, K. Emoto, M. Umeda, S. Watanabe, and H. Okuyama Effects of docosahexaenoic and arachidonic acids on the synthesis and distribution of aminophospholipids during neuronal differentiation of PC12 cells Arch Biochem Biophys 364 1999 67 74 (Pubitemid 29394292)
96. V.M. Gohil, and M.L. Greenberg Mitochondrial membrane biogenesis: phospholipids and proteins go hand in hand J Cell Biol 184 2009 469 472
97. S.E. Horvath, L. Böttinger, F.N. Vögtle, N. Wiedemann, C. Meisinger, and T. Becker et al. Processing and topology of the yeast mitochondrial phosphatidylserine decarboxylase 1 J Biol Chem 287 2012 36744 36755
98. J.H. Kevala, and H.Y. Kim Determination of substrate preference in phosphatidylserine decarboxylation by liquid chromatography-electrospray ionization mass spectrometry Anal Biochem 292 2001 130 138 (Pubitemid 32417731)
99. O.B. Bleijerveld, J.F.H.M. Brouwers, A.B. Vaandrager, J.B. Helms, and M. Houweling The CDP-ethanolamine pathway and phosphatidylserine decarboxylation generate different phosphatidylethanolamine molecular species J Biol Chem 282 2007 28362 28372 (Pubitemid 47606037)
100. O. Camici, and L. Corazzi Import of phosphatidylethanolamine for the assembly of rat brain mitochondrial membranes J Membr Biol 148 1995 169 176
101. D.R. Voelker Disruption of phosphatidylserine translocation to the mitochondria in baby hamster kidney cells J Biol Chem 260 1985 14671 14676 (Pubitemid 16210997)
102. D.R. Voelker Phosphatidylserine functions as the major precursor of phosphatidylethanolamine in cultured BHK-21 cells Proc Natl Acad Sci USA 81 1984 2669 2673 (Pubitemid 14109321)
103. O. Kuge, M. Nishijima, and Y. Akamatsu Phosphatidylserine-dependent neuroprotective signaling promoted by docosahexaenoic acid Proc Natl Acad Sci USA 82 1985 1926 1930
104. O. Kuge, M. Nishijima, and Y. Akamatsu Phosphatidylserine biosynthesis in cultured Chinese hamster ovary cells. II. Isolation and characterization of phosphatidylserine auxotrophs J Biol Chem 261 1986 5790 5794 (Pubitemid 17207405)
105. R. Leonardi, M.W. Frank, P.D. Jackson, C.O. Rock, and S. Jackowski Elimination of the CDP-ethanolamine pathway disrupts hepatic lipid homeostasis J Biol Chem 284 2009 27077 27089
106. P.G. Bradford, G.V. Marinetti, and L.G. Abood Stimulation of phospholipase A2 and secretion of catecholamines from brain synaptosomes by potassium and A23187 J Neurochem 41 1983 1684 1693 (Pubitemid 14208190)
107. J.A. Kelleher, and G.Y. Sun Enzymic hydrolysis of arachidonoyl- phospholipids by rat brain synaptosomes Neurochem Int 7 1985 825 831 (Pubitemid 15017334)
108. J. Cao, D. Shan, T. Revett, D. Li, L. Wu, and W. Liu et al. Molecular identification of a novel mammalian brain isoform of acyl-CoA:lysophospholipid acyltransferase with prominent ethanolamine lysophospholipid acylating activity, LPEAT J Biol Chem 283 2008 19049 19057
109. B.M. Ross, and S.J. Kish Characterization of lysophospholipid metabolizing enzymes in human brain J Neurochem 63 1994 1839 1848 (Pubitemid 24326228)
110. O.A. James, G. MacDonald, and W. Thompson Acylation of lysophosphatidylserine by rat brain microsomes J Neurochem 33 1979 1061 1066 (Pubitemid 10188737)
111. P.G. Rhodes, Z.Y. Hu, and G.Y. Sun Lysophosphatidylserine enhances the transfer of 22:6n3 to lysophosphatidic acid in rat brain microsomes Life Sci 49 1991 225 232
112. K.K. Vaswani, and R.W. Ledeen Purified rat brain myelin contains measurable acyl-CoA:lysophospholipid acyltransferase(s) but little, if any, glycerol-3-phosphate acyltransferase J Neurochem 52 1989 69 74 (Pubitemid 19023351)
113. J.L. Blankman, J.Z. Long, S.A. Trauger, G. Siuzdak, and B.F. Cravatt ABHD12 controls brain lysophosphatidylserine pathways that are deregulated in a murine model of the neurodegenerative disease PHARC Proc Natl Acad Sci USA 110 2013 1500 1505
114. K. Makide, H. Kitamura, Y. Sato, M. Okutani, and J. Aoki Emerging lysophospholipid mediators, lysophosphatidylserine, lysophosphatidylthreonine, lysophosphatidylethanolamine and lysophosphatidylglycerol Prostaglandins Other Lipid Mediat 89 2009 135 139
115. S.C. Frasch, and D.L. Bratton Emerging role for lysophosphatidylserine in resolution of inflammation Prog Lipid Res 51 2012 199 207
116. Z. Guan, S. Li, D.C. Smith, W.A. Shaw, and C.R.H. Raetz Identification of N-acylphosphatidylserine molecules in eukaryotic cells Biochemistry 46 2007 14500 14513 (Pubitemid 350276356)
117. H.H.O. Schmid, P.C. Schmid, and V. Natarajan N-acylated glycerophospholipids and their derivatives Prog Lipid Res 29 1990 1 43 (Pubitemid 120036504)
118. H. Cadas, E. di Tomaso, and D. Piomelli Occurrence and biosynthesis of endogenous cannabinoid precursor, N-arachidonoyl phosphatidylethanolamine, in rat brain J Neurosci 17 1997 1226 1242 (Pubitemid 27073726)
119. A. Guiffrida, L.H. Parsons, T.M. Kerr, F. Rodríguez de Fonseca, M. Navarro, and D. Piomelli Dopamine activation of endogenous cannabinoid signaling in dorsal striatum Nat Neurosci 2 1999 358 363 (Pubitemid 30491279)
120. P. Pacher, S. Bátkai, and G. Kunos The endocannabinoid system as an emerging target of pharmacotherapy Pharmacol Rev 58 2006 389 462 (Pubitemid 44394908)
121. V. DeMarzo, A. Fontana, H. Cadas, S. Schinelli, G. Cimino, and J.C. Schwartz et al. Formation and inactivation of endogenous cannabinoid anandamide in central neurons Nature 372 1994 686 691
122. Y. Okamoto, J. Morishita, K. Tsuboi, T. Tonai, and N. Ueda Molecular characterization of a phospholipase D generating anandamide and its congeners J Biol Chem 279 2004 5298 5305 (Pubitemid 38220550)
123. J. Liu, L. Wang, J. Harvey-White, D. Osei-Hyiaman, R. Razdan, and Q. Gong et al. A biosynthetic pathway for anandamide Proc Natl Acad Sci USA 103 2006 13345 13350 (Pubitemid 44380110)
124. G.M. Simon, and B.F. Cravatt Anandamide biosynthesis catalyzed by the phosphodiesterase GDE1 and detection of the glycerophospho N-acyl ethanolamine precursors in mouse brain J Biol Chem 283 2008 9341 9349
125. B. Tan, D.K. O'Dell, Y.W. Yu, M.F. Monn, H.V. Hughes, and S. Burstein et al. Identification of endogenous acyl amino acids based on a targeted lipidomics approach J Lipid Res 51 2010 112 119
126. 2+ channels in sympathetic neurons J Neurophysiol 100 2008 1147 1151
127. G. Milman, Y. Maor, S. Abu-Lafi, M. Horowitz, R. Gallily, and S. Batkai et al. N-arachidonoyl l-serine, an endocannabinoid-like brain constituent with vasodilatory properties Proc Natl Acad Sci USA 103 2006 2428 2433 (Pubitemid 43271686)
128. + channels J Pharmacol Exp Ther 328 2009 351 361
129. X. Zhang, Y. Maor, J.F. Wang, G. Kunos, and J.E. Groopman Endocannabinoid-like N-arachidonoyl serine is a novel pro-angiogenic mediator Br J Pharmacol 160 2010 1583 1594
130. R. Smoum, A. Bar, B. Tan, G. Milman, M. Attar-Namdar, and O. Ofek et al. Oleoyl serine, an endogenous N-acyl amide, modulates bone remodeling Proc Natl Acad Sci USA 107 2010 17710 17715
131. A.C. Newton Protein kinase C: poised to signal Am J Physiol Endocrinol Metab 298 2010 E395 E402
132. M. Medkova, and W. Cho Mutagenesis of the C2 domain of protein kinase C-α J Biol Chem 273 1998 17544 17552
133. D. Murray, and B. Honig Electrostatic control of the membrane targeting of C2 domains Mol Cell 9 2002 145 154 (Pubitemid 34127778)
134. 2 J Biol Chem 278 2003 12452 12460 (Pubitemid 36800232)
135. 2+ bridges the C2 membrane-binding domain of protein kinase C directly to phosphatidylserine EMBO J 18 1999 6329 6338 (Pubitemid 29533237)
136. B. Ananthanarayanan, S. Das, S.G. Rhee, D. Murray, and W. Cho Membrane targeting of C2 domains of phospholipase C-δ isoforms J Biol Chem 277 2002 3568 3575 (Pubitemid 34953228)
137. 2+-bridging mechanism and phospholipid head group recognition in the membrane-binding protein annexin V Nat Struct Biol 2 1995 968 974
138. 2+signaling to membrane dynamics Mol Cell Biol 6 2005 449 461 (Pubitemid 40780557)
139. R. Huber, J. Romisch, and E.-P. Paques The crystal and molecular structure of human annexin V, an anticoagulant protein that binds to calcium and membranes EMBO J 9 1990 3867 3874
140. N. Lucas, and W. Cho Phosphatidylserine binding is essential for plasma membrane recruitment and signaling function of 3-phosphoinositide-dependent kinase 1 J Biol Chem 286 2011 41265 41272
141. T. Improta-Brears, S. Ghosh, and R.M. Bell Mutational analysis of Raf-1 cysteine rich domain: requirement for a cluster of basic aminoacids for interaction with phosphatidylserine Mol Cell Biochem 198 1999 171 178 (Pubitemid 29414537)
142. S. Macedo-Ribeiro, W. Bode, R. Huber, M.A. Quinn-Allen, S.W. Kim, and T.L. Ortel et al. Crystal structures of the membrane-binding C2 domain of human coagulation factor V Nature 402 1999 434 439 (Pubitemid 129544834)
143. J. Shi, C.W. Heegaard, J.T. Rasmussen, and G.E. Gilbert Lactadherin binds selectively to membranes containing phosphatidyl-l-serine and increased curvature Biochim Biophys Acta 1667 2004 80 90
144. J.E. Johnson, J. Giorgione, and A.C. Newton The C1 and C2 domains of protein kinase C are independent membrane targeting modules, with specificity for phosphatidylserine conferred by the C1 domain Biochemistry 39 2000 11360 11369
145. D.P. Brazil, and B.A. Hemmings Ten years of protein kinase B signaling: a hard Akt to follow Trends Biochem Sci 26 2001 657 664 (Pubitemid 33042488)
146. M. Andjelkovic, D.R. Alessi, R. Meier, A. Fermandez, N.J.C. Lamb, and M. Frech et al. Role of translocation in the activation and function of protein kinase B J Biol Chem 272 1997 31515 31524 (Pubitemid 28013293)
147. O. Kuge, K. Hasegawa, K. Saito, and M. Nishijima Control of phosphatidylserine biosynthesis through phosphatidylserine-mediated inhibition of phosphatidylserine synthase I in Chinese hamster ovary cells Proc Natl Acad Sci USA 95 1998 4199 4203
148. D.R. Alessi, S.R. James, C.P. Downes, A.B. Holmes, P.R.J. Gaffney, and C.B. Reese et al. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα Curr Biol 7 1997 261 269 (Pubitemid 27176852)
149. L. Stephens, K. Anderson, D. Stokoe, H. Erdjument-Bromage, A.B. Holmes, and P.R.J. Gaffney et al. Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B Science 279 1998 710 714 (Pubitemid 28144551)
150. S.J. Leevers, H.F. Paterson, and C.J. Marshall Requirement for Ras in Raf activation is overcome by targeting Raf to the plasma membrane Nature 369 1994 411 414 (Pubitemid 24184056)
151. M. Levi de Stein, J.H. Medina, and E. De Robertis In vivo and in vitro modulation of central type benzodiazepine receptors by phosphatidylserine Mol Brain Res 5 1989 9 15 (Pubitemid 19011049)
152. T. Kimura, A.A. Yeliseev, K. Vukoti, S.D. Rhodes, K. Cheng, and K.C. Rice et al. Recombinant cannabinoid type 2 receptor in liposome model activates G protein in response to anionic lipid constituents J Biol Chem 287 2012 4076 4087
153. T.C. Südhof Neurotransmitter release: the last millisecond in the life of a synaptic vesicle Neuron 80 2013 675 690
154. 2+ concentrations to SNARE-mediated membrane fusions Mol Biol Cell 16 2005 4755 4764 (Pubitemid 41416458)
155. E. Hui, C.P. Johnson, J. Yao, F.M. Dunning, and E.R. Chapman Synaptotagmin-mediated bending of the target membrane is a critical step in Ca(2+)-regulated fusion Cell 138 2009 709 721
156. S. Takamori, M. Holt, K. Stenius, E.A. Lemke, M. Grønborg, and D. Riedel et al. Molecular anatomy of a trafficking organelle Cell 127 2006 831 846 (Pubitemid 44716256)
157. J.W. Deutsch, and R.B. Kelly Lipids of synaptic vesicles: relevance to the mechanism of membrane fusion Biochemistry 20 1981 378 385
158. Z. Wang, H. Liu, Y. Gu, and E.R. Chapman Reconstituted synaptotagmin I mediates vesicle docking, priming, and fusion J Cell Biol 195 2011 1159 1170
159. Y. Watanabe, M. Nishio, S. Hamaji, Y. Hagashi, Y. Hu, and H. Hidaka Neuronal nitric oxide synthase-membrane phospholipid interactions Arch Biochem Biophys 358 1998 68 73 (Pubitemid 28471375)
160. O.S. Ostroumova, L.V. Schagima, M.I. Mosevitsky, and V.V. Zakharov Ion channel activity of brain abundant protein BASP1 in planar lipid bilayers FEBS J 278 2011 461 469
161. H. Yamamoto, Y. Kida, and M. Sakaguchi Phosphatidylserine-binding protein lactadherin inhibits protein translocation across ER membrane Biochem Biophys Res Commun 434 2013 620 626
162. 2 domain of MFG-E8 and insights into its molecular recognition with phosphatidylserine Biochim Biophys Acta 1828 2013 1083 1093
163. R.V. Stahelin, J.H. Hwang, J.H. Kim, Z.Y. Park, K.R. Johnson, and L.M. Obeid et al. The mechanism of membrane targeting of human sphingosine kinase 1 J Biol Chem 280 2005 43030 43038 (Pubitemid 43049268)
164. 2 isoform J Biol Chem 287 2012 38824 38834
165. B. Tu-sekine, and D.M. Rabin Dual regulation of diacylglycerol kinase (DGK)-θ. Polybasic protein promote activation by phospholipids and increase substrate affinity J Biol Chem 287 2012 41619 41627
166. 2 domain binding to lipid membranes Proc Natl Acad Sci USA 110 2013 111 116
167. C.L. Lai, A. Srivastava, C. Pilling, A.R. Chase, J.J. Falke, and G.A. Voth Molecular mechanism of membrane searching of the GRP1 PH domain J Mol Biol 425 2013 3073 3090
168. N.K. Mishra, Y. Peleg, E. Cirri, T. Belogus, Y. Lifshitz, and D.R. Voelker et al. FXYD proteins stabilize Na, K-ATPase: amplification of specific phosphatidylserine-protein interactions J Biol Chem 286 2011 9699 9712
169. E. Kapri-Pardes, A. Katz, H. Havlv, Y. Mahmmoud, M. Ilan, and I. Khalfin-Penigel et al. Stabilization of the α2 isoform of Na, K-ATPase by mutations in a phospholipid binding pocket J Biol Chem 286 2011 42888 42899
170. A. Orlowski, M. Gryzbck, A. Bunker, M. Pasenliewicz-Gierula, I. Vattulainen, and P.T. Mannisto et al. Strong preference for dopamine and L-dopa towards lipid head group: importance for lipid composition and implications for neurotransmitter metabolism J Neurochem 122 2012 681 690
171. C. Wang, F. Ye, G.F. Velardez, G.H. Peters, and P. Westh Affinity of four polar neurotransmitters for lipid bilayer membranes J Phys Chem B 115 2011 196 203
172. K. Hamazaki, K.H. Choi, and H.Y. Kim Phospholipid profile in the postmortem hippocampus of patients with schizophrenia and bipolar disorder: no changes in docosahexaenoic acid species J Psychiatr Res 44 2010 688 693
173. M. Eto, H. Shindou, and T. Shimizu A novel lysophosphatidic acid acyltransferase enzyme (LPAAT4) with a possible role for incorporating docosahexaenoic acid into brain glycerophospholipids Biochem Biophys Res Commun 443 2014 718 724
174. F. Calderon, and H.Y. Kim Docosahexaenoic acid promotes neurite growth in hippocampal neurons J Neurochem 90 2004 979 988 (Pubitemid 39099980)
175. D. Cao, R. Xue, J. Xu, and Z. Liu Effects of docosahexaenoic acid on the survival and neurite outgrowth of rat cortical neurons in primary cultures J Nutr Biochem 16 2004 538 546
176. E. Kawakita, M. Hashimoto, and O. Shido Docosahexaenoic acid promotes neurogenesis in vitro and in vivo Neuroscience 139 2006 991 997
177. H.Y. Kim, H.S. Moon, D. Cao, J. Lee, K. Kevala, and S.B. Jun et al. N-docosylhexaenoylethanolamide promotes development of hippocampal neurons Biochem J 435 2011 327 336
178. M.A. Rashid, M. Katakura, G. Khavebava, and H.Y. Kim N- docosylhexaenoylethanolamine is a potent neurogenic factor for neural stem cell differentiation J. Neurochem 125 2013 869 884
179. H.Y. Kim, M. Akbar, and A. Lau Effects of docosapentaenoic acid on neuronal apoptosis Lipids 38 2003 453 457 (Pubitemid 36724305)
180. M. Guo, L. Stockert, M. Akbar, and H.Y. Kim Neuronal specific increase of phosphatidylserine by docosahexaenoic acid J Mol Neurosci 33 2007 67 73 (Pubitemid 47574960)
181. O. Tam, and S.M. Innis Dietary polyunsaturated fatty acids in gestation alter fetal cortical phospholipids, Fatty acids and phosphatidylserine synthesis Dev Neurosci 28 2006 222 229
182. M. Akbar, J. Baick, F. Calderon, Z. Wen, and H.Y. Kim Ethanol promotes neuronal apoptosis by inhibiting phosphatidylserine accumulation J Neurosci Res 83 2006 432 440 (Pubitemid 43184406)
183. Z. Wen, and H.Y. Kim Inhibition of phosphatidylserine biosynthesis by ethanol in developing rat brain J Neurosci Res 85 2007 1568 1578 (Pubitemid 46724400)
184. M.P. Carrasco, J.M. Jiménez-López, J.L. Segovia, and C. Marco Effects of ethanol on the remodeling of neutral lipids and phospholipids in brain mitochondria and microsomes Neurochem Int 50 2007 858 865 (Pubitemid 46710197)
185. A.L. Petursdottir, S.A. Farr, J.E. Morley, W.A. Banks, and G.V. Skuladottir Lipid peroxidation in brain during aging in the senescence- accelerated mouse (SAM) Neurobiol Aging 28 2007 1170 1178 (Pubitemid 46810060)
186. S.C. Cunnane, J.A. Schneider, C. Tangney, J. Tremblay-Mercier, M. Fortier, and D.A. Bennett et al. Plasma and brain fatty acid profiles in mild cognitive impairment and Alzheimer's disease J Alzheimer's Dis 29 2012 691 697
187. L. Ullman, V. Mimouni, S. Roxx, R. Porsolt, and J.P. Poisson Brain and hippocampus fatty acid composition in the phospholipid classes of age-related cognitive deficit rats Prostaglandins Leukot Essent Fatty Acids 64 2001 189 195 (Pubitemid 32896820)
188. F. Drago, P.L. Canonico, and U. Scapagini Behavioral effects of phosphatidylserine in aged rats Neurobiol Aging 2 1981 209 213 (Pubitemid 12166169)
189. J. Corwin, R.L. Dean III, R.T. Bartus, J. Rotrosen, and D.L. Watkins Behavioral effects of phosphatidylserine in the aged Fischer 344 rats: amelioration of passive avoidance deficits without changes in psychomotor task performance Neurobiol Aging 6 1985 11 15 (Pubitemid 15105367)
190. B. Lee, B.J. Sur, J.J. Han, I. Shim, S. Her, and H.J. Lee et al. Krill phosphatidylserine improves learning and memory in Morris water maze in aged rats Prog Neuropsychopharmacol Biol Psychiatry 34 2010 1085 1093
191. H.J. Park, H.S. Shim, K.S. Kim, J.J. Han, J.S. Kim, and A.R. Yu et al. Enhanced learning and memory of normal young rats by repeated oral administration of Krill phosphatidylserine Nutr Neurosci 16 2012 47 53
192. P.J. Delwaide, A.M. Gyselynck-Mambourg, A. Hurlet, and M. Ylieff Double blind randomized controlled study of phosphatidylserine in senile demented patients Acta Neurol Scand 73 1986 136 140 (Pubitemid 16124005)
193. J. Baumeister, T. Barthel, K.R. Geiss, and M. Weiss Influence of phosphatidylserine on cognitive performance and cortical activity after induced stress Nutr Neurosci 11 2008 103 110
194. B.L. Jorissen, F. Brorens, M.P.J. Van Boxtel, and W.J. Riedel Safety of soy-derived phosphatidylserine in elderly people Nutr Neurosci 5 2002 337 343 (Pubitemid 35174633)
195. Y. Richter, Y. Herzog, T. Cohen, and Y. Steinhart The effect of phosphatidylserine-containin omega-3 fatty acids on memory abilities in subjects with subjective memory complaints; a pilot study Clin Interv Aging 5 2010 313 316
196. V. Vakhapova, T. Cohen, Y. Richter, Y. Herzog, and A.D. Korczyn Phosphatidylserine containing ω-3 fatty acids may improve memory abilities in non-demented elderly with memory complaints: a double-blind placebo-controlled trial Dement Geriatr Cogn Disord 29 2010 467 474
197. A. Kato-Kataoka, M. Sakai, R. Ebina, and C. Nonaka Soybean derived phosphatidylserine improves memory function of the elderly Japanese subjects with memory complaints J Clin Biochem Nutr 47 2010 246 255
198. A. Leon, D. Benvegnú, G. Toffano, P. Orlando, and P. Massari Effect of brain cortex phospholipids on adenylate-cyclase activity in mouse brain J Neurochem 30 1978 23 26 (Pubitemid 8266271)
199. F. Casamenti, P. Mantovani, L. Amaducci, and G. Papeu Effect of phosphatidylserine on acetylcholine output from the cerebral cortex of rats J Neurochem 32 1979 529 533 (Pubitemid 9131960)
200. F. Casamenti, C. Scali, and G. Papeu Phosphatidylserine reverses the age-dependent decrease in cortical acetylcholine release: a microdialysis study Eur J Pharmacol 194 1991 11 16