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Phosphatidic acid - a simple phospholipid with multiple faces

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Phosphatidic acid (PA) is the simplest glycerophospholipid naturally occurring in living organisms, and even though its content among other cellular lipids is minor, it is drawing more and more attention due to its multiple biological functions. PA is a precursor for other phospholipids, acts as a lipid second messenger and, due to its structural properties, is also a modulator of membrane shape. Although much is known about interaction of PA with its effectors, the molecular mechanisms remain unresolved to a large degree. Throughout many of the well-characterized PA cellular sensors, no conserved binding domain can be recognized. Moreover, not much is known about the cellular dynamics of PA and how it is distributed among subcellular compartments. Remarkably, PA can play distinct roles within each of these compartments. For example, in the nucleus it behaves as a mitogen, influencing gene expression regulation, and in the Golgi membrane it plays a role in membrane trafficking. Here, we discuss how a biophysical experimental approach enabled PA behavior to be described in the context of a lipid bilayer and to what extent various physicochemical conditions may modulate the functional properties of this lipid. Understanding these aspects would help to unravel specific mechanisms of PA-driven membrane transformations and protein recruitment and thus would lead to a clearer picture of the biological role of PA.

Physical description
  • Laboratory of Cytobiochemistry, Faculty of Biotechnology, University of Wrocław, Wrocław, Poland
  • Laboratory of Cytobiochemistry, Faculty of Biotechnology, University of Wrocław, Wrocław, Poland
  • Laboratory of Cytobiochemistry, Faculty of Biotechnology, University of Wrocław, Wrocław, Poland
  • Laboratory of Cytobiochemistry, Faculty of Biotechnology, University of Wrocław, Wrocław, Poland
  • Ammar MR, Kassas N, Bader MF, Vitale N (2014) Phosphatidic acid in neuronal development: A node for membrane and cytoskeleton rearrangements. Biochimie 107: 51-57.doi: 10.1016/j.biochi.2014.07.026.
  • Boughriet A, Ladjadj M, Bicknell-Brown E (1988) Calcium-induced condensation-reorganization phenomena in multilamellar vesicles of phosphatidic acid. pH potentiometric and 31P-NMR, Raman and ESR spectroscopic studies. Biochim Biophys Acta 939: 523-532.doi: 10.1016/0005-2736(88)90099-5.
  • Broemstrup T, Reuter N (2010) Molecular Dynamics Simulations of Mixed Acidic/Zwitterionic Phospholipid Bilayers. Biophys J 99: 825-833.doi: 10.1016/j.bpj.2010.04.064.
  • Buckland AG, Wilton DC (2000) Anionic phospholipids, interfacial binding and the regulation of cell functions. Biochim Biophys Acta 1483: 199-216.doi: 10.1016/S1388-1981(99)00188-2.
  • Burger KN, Demel RA, Schmid SL, De Kruijff B (2000) Dynamin is membrane-active: Lipid insertion is induced by phosphoinositides and phosphatidic acid. Biochemistry 39: 12485-12493.doi: 10.1021/bi000971r.
  • Cambrea LR, Hovis JS (2007) Formation of three-dimensional structures in supported lipid bilayers. Biophys J 92: 3587-3594.doi: 10.1529/biophysj.106.101139.
  • Carman GM, Henry SA (2013) Phosphatidic acid plays a central role in the transcriptional regulation of glycerophospholipid synthesis in Saccharomyces cerevisiae. J Biol Chem 282: 37293-37297.doi: 10.1074/jbc.R700038200.
  • Carruthers A, Melchior DL (1983) Study of the relationship between bilayer water permeability and bilayer physical state. Biochemistry 22: 5797-5807.doi: 10.1021/bi00294a018
  • Chernomordik LV, Kozlov MM (2003) Protein-lipid interplay in fusion and fission of biological membranes. Annu Rev Biochem 72: 175-207.doi: 10.1146/annurev.biochem.72.121801.161504.
  • Choi SY, Huang P, Jenkins GM, Chan DC, Schiller J, Frohman MA (2006) A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat Cell Biol 8: 1255-1262.doi: 10.1038/ncb1487.
  • Coleman RA, Lee DP (2004) Enzymes of triacylglycerol synthesis and their regulation. Prog Lipid Res 43: 134-176.doi: 10.1016/S0163-7827(03)00051-1.
  • Connerth M, Tatsuta T, Haag M, Klecker T, Westermann B, Langer T (2012) Intramitochondrial transport of phosphatidic acid in yeast by a lipid transfer protein. Science 338: 815-818.doi: 10.1126/science.1225625.
  • Contreras FX, Ernst AM, Haberkant P, Björkholm P, Lindahl E, Gönen B, Tischer C, Elofsson A, Von Heijne G, Thiele C, Pepperkok R, Wieland F, Brügger B (2012) Molecular recognition of a single sphingolipid species by a protein's transmembrane domain. Nature 481: 525-529.doi: 10.1038/nature10742.
  • Cullis PR, Hope MJ, Tilcock CP (1986) Lipid polymorphism and the roles of lipids in membranes. Chem Phys Lipids 40: 127-144.doi: 10.1016/0009-3084(86)90067-8.
  • Cullis PR, de Kruijff B, Verkleij AJ, Hope MJ (1986) Lipid polymorphism and membrane fusion. Biochem Soc Trans 14: 242-245.doi: 10.1042/bst0140242.
  • daCosta CJ, Wagg ID, McKay ME, Baenziger JE (2004) Phosphatidic acid and phosphatidylserine have distinct structural and functional interactions with the nicotinic acetylcholine receptor. J Biol Chem 279: 14967-14974.doi: 10.1074/jbc.M310037200.
  • van Dijck PWM, de Kruijff B, Verkleij AJ, van Deenen LLM, de Gier J (1978) Comparative studies on the effects of pH and Ca2+ on bilayers of various negatively charged phospholipids and their mixtures with phosphatidylcholine. Biochim Biophys Acta 512: 84-96.doi: 10.1016/0005-2736(78)90219-5
  • Eaton JM, Mullins GR, Brindley DN, Harris TE (2013) Phosphorylation of lipin 1 and charge on the phosphatidic acid head group control its phosphatidic acid phosphatase activity and membrane association. J Biol Chem 288: 9933-9945.doi: 10.1074/jbc.M112.441493.
  • Escribá PV, Ozaita A, Ribas C, Miralles A, Fodor E, Farkas T, García-Sevilla JA (1997) Role of lipid polymorphism in G protein-membrane interactions: Nonlamellar-prone phospholipids and peripheral protein binding to membranes. Proc Natl Acad Sci 94: 11375-11380.doi: 10.1073/pnas.94.21.11375.
  • Estrela-Lopis I, Brezesinski G, Möhwald H (2004) Miscibility of DPPC and DPPA in monolayers at the air/water interface. Chem Phys Lipids 131: 71-80.doi: 10.1016/j.chemphyslip.2004.04.005.
  • Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen J (2001) Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294: 1942-1945.doi: 10.1126/science.1066015.
  • Farren SB, Hope MJ, Cullis PR (1983) Polymorphic phase preferences of phosphatidic acid: A 31P and 2H NMR study. Biochem Biophys Res Commun 111: 675-682.doi: 10.1016/0006-291X(83)90359-5.
  • Foster DA (2013) Phosphatidic acid and lipid-sensing by mTOR. Trends Endocrinol Metab 24: 272-278.doi: 10.1016/j.tem.2013.02.003.
  • Freyberg Z, Sweeney D, Siddhanta a, Bourgoin S, Frohman M, Shields D (2001) Intracellular localization of phospholipase D1 in mammalian cells. Mol Biol Cell 12: 943-955,doi: 10.1091/mbc.12.4.943.
  • Frohman MA, Morris AJ (1999) Phospholipase D structure and regulation. Chem Phys Lipids 98: 127-140.doi: 10.1016/S0009-3084(99)00025-0.
  • Garidel P, Johann C, Blume A (1997a) Nonideal mixing and phase separation in phosphatidylcholine-phosphatidic acid mixtures as a function of acyl chain length and pH. Biophys J 72: 2196–2210.doi: 10.1016/S0006-3495(97)78863-5.
  • Garidel P, Johann C, Mennicke L, Blume A (1997b) The mixing behavior of pseudobinary phosphatidylcholine-phosphatidylglycerol mixtures as a function of pH and chain length. Eur Biophys J 26: 447–459.doi: 10.1007/s002490050099
  • Ghosh S, Bell RM (1997) Regulation of raf-1 kinase by interaction with the lipid second messenger, phosphatidic acid. Biochem Soc Trans 25: 561-565.doi: 10.1042/bst0250561.
  • Ghosh S, Moore S, Bell RM, Dush M (2003) Functional analysis of a phosphatidic acid binding domain in human Raf-1 kinase: Mutations in the phosphatidate binding domain lead to tail and trunk abnormalities in developing zebrafish embryos. J Biol Chem 278: 45690-45696.doi: 10.1074/jbc.M302933200.
  • Gonzalez-Baro MR, Coleman RA (2017) Mitochondrial acyltransferases and glycerophospholipid metabolism. Biochim Biophys Acta 1862: 49-55.doi: 10.1016/j.bbalip.2016.06.023.
  • Hajra AK (1997) Dihydroxyacetone phosphate acyltransferase. Biochim Biophys Acta 1348: 27-34.doi: 10.1016/S0005-2760(97)00120-3.
  • Han GS, Carman GM (2010) Characterization of the human LPIN1-encoded phosphatidate phosphatase isoforms. J Biol Chem 285: 14628-14638.doi: 10.1074/jbc.M110.117747.
  • Horchani H, De Saint-Jean M, Barelli HL, Antonny B (2014) Interaction of the Spo20 membrane-sensor motif with phosphatidic acid and other anionic lipids, and influence of the membrane environment. PLoS One 9: e113484.doi: 10.1371/journal.pone.0113484.
  • Huang J, Feigenson GW (1999) A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys J 76: 2142-2157.doi: 10.1016/S0006-3495(99)77369-8.
  • Huang P, Altshuller YM, Hou JC, Pessin JE, Frohman MA (2005) Insulin-stimulated plasma membrane fusion of Glut4 glucose transporter-containing vesicles is regulated by phospholipase D1. Mol Biol Cell 16: 2614-2623.doi: 10.1091/mbc.e04-12-1124.
  • Jang JH, Lee CS, Hwang D, Ryu SH (2012) Understanding of the roles of phospholipase D and phosphatidic acid through their binding partners. Prog Lipid Res 51: 71-81.doi: 10.1016/j.plipres.2011.12.003.
  • Jouhet J (2013) Importance of the hexagonal lipid phase in biological membrane organization. Front Plant Sci 4: 494.doi: 10.3389/fpls.2013.00494.
  • Kassas N, Tanguy E, Thahouly T, Fouillen L, Heintz D, Chasserot-Golaz S, Bader MF, Grant NJ, Vitale N (2017) Comparative characterization of phosphatidic acid sensors and their localization during frustrated phagocytosis. J Biol Chem 292: 4266-4279.doi: 10.1074/jbc.M116.742346.
  • Kim YJ, Guzman-Hernandez ML, Wisniewski E, Echeverria N, Balla T (2016) Phosphatidylinositol and phosphatidic acid transport between the ER and plasma membrane during PLC activation requires the Nir2 protein. Biochem Soc Trans 44: 197-201.doi: 10.1042/BST20150187.
  • Kobayashi S, Hirakawa K, Horiuchi H, Fukuda R, Ohta A (2013) Phosphatidic acid and phosphoinositides facilitate liposome association of Yas3p and potentiate derepression of ARE1 (alkane-responsive element one)-mediated transcription control. Fungal Genet Biol 61: 100-110.doi: 10.1016/j.fgb.2013.09.008.
  • Kolesnikov YS, Nokhrina KP, Kretynin S V, Volotovski ID, Martinec J, Romanov G a, Kravets VS (2012) Molecular structure of phospholipase D and regulatory mechanisms of its activity in plant and animal cells. Biochemistry (Mosc) 77: 1-14.doi: 10.1134/S0006297912010014.
  • Kooijman EE, Burger KN (2009) Biophysics and function of phosphatidic acid: A molecular perspective. Biochim Biophys Acta 1791: 881-888.doi: 10.1016/j.bbalip.2009.04.001.
  • Kooijman EE, Carter KM, Van Laar EG, Chupin V, Burger KN, De Kruijff B (2005a) What makes the bioactive lipids phosphatidic acid and lysophosphatidic acid so special? Biochemistry 44: 17007-17015.doi: 10.1021/bi0518794.
  • Kooijman EE, Chupin V, Fuller NL, Kozlov MM, De Kruijff B, Burger KN, Rand PR (2005b) Spontaneous curvature of phosphatidic acid and lysophosphatidic acid. Biochemistry 44: 2097-2102.doi: 10.1021/bi0478502.
  • Kooijman EE, Chupin V, de Kruijff B, Burger KN (2003) Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic 4: 162-174.doi: 10.1034/j.1600-0854.2003.00086.x.
  • Kooijman EE, Tieleman DP, Testerink C, Munnik T, Rijkers DT, Burger KN, De Kruijff B (2007) An electrostatic/hydrogen bond switch as the basis for the specific interaction of phosphatidic acid with proteins. J Biol Chem 282: 11356-11364.doi: 10.1074/jbc.M609737200.
  • Kouaouci R, Silvius JR, Graham I, Pezolet M (1985) Calcium-induced lateral phase separations in phosphatidylcholine-phosphatidic acid mixtures. a raman spectroscopic study. Biochemistry 24: 7132-7140.doi: 10.1021/bi00346a017.
  • Kwolek U, Kulig W, Wydro P, Nowakowska M, Róg T, Kepczynski M (2015) Effect of phosphatidic acid on biomembrane: experimental and molecular dynamics simulations study. J Phys Chem B 119: 10042-10051.doi: 10.1021/acs.jpcb.5b03604.
  • Langner M, Kubica K (1999) The electrostatics of lipid surfaces. Chem Phys Lipids 101: 3-35.doi: 10.1016/S0009-3084(99)00052-3.
  • Laplante M, Sabatini DM (2012) MTOR signaling in growth control and disease. Cell 149: 274-293.doi: 10.1016/j.cell.2012.03.017.
  • Liao MJ, Prestegard JH (1981) Structural properties of a Ca2+-phosphatidic acid complex Small angle x-ray scattering and calorimetric results. Biochim Biophys Acta 645: 149-156.doi: 10.1016/0005-2736(81)90523-X.
  • Liscovitch M, Czarny M, Fiucci G, Tang X (2000) Phospholipase D: molecular and cell biology of a novel gene family. Biochem J 345 Pt 3: 401-415.doi: 10.1016/j.bbamem.2013.10.003.
  • Liu Y, Su Y, Wang X (2013) Phosphatidic Acid-Mediated Signaling. In Lipid-Mediated Protein Signaling, D.G.S. Capelluto ed, pp. 159-176. Dordrecht: Springer Netherlands.
  • Loewen CJ, Gaspar ML, Jesch SA, Delon NT (2004) Phospholipid metabolism regulated by a transcription factor sensing phosphatidic acid. Science 304: 1644-1647.doi: 10.1126/science.1096083.
  • Mouritsen OG (2011) Lipids, curvature, and nano-medicine. Eur J Lipid Sci Technol 113: 1174-1187.doi: 10.1002/ejlt.201100050.
  • Nadler A, Reither G, Feng S, Stein F, Reither S, Müller R, Schultz C (2013) The fatty acid composition of diacylglycerols determines local signaling patterns. Angew Chem Int Ed Engl 52: 6330-6334.doi: 10.1002/anie.201301716.
  • Nakanishi H, de los Santos P, Neiman AM (2004) Positive and negative regulation of a SNARE protein by control of intracellular localization. Mol Biol Cell 15: 1802-1815.doi: 10.1091/mbc.e03-11-0798.
  • Ogawa R, Nagao K, Taniuchi K, Tsuchiya M, Kato U, Hara Y, Inaba T, Kobayashi T, Sasaki Y, Akiyoshi K, Watanabe-Takahashi M, Nishikawa K, Umeda M (2015) Development of a novel tetravalent synthetic peptide that binds to phosphatidic acid. PLoS One 10: e0131668.doi: 10.1371/journal.pone.0131668.
  • Oh WJ, Jacinto E (2011) mTOR complex 2 signaling and functions. Cell Cycle 10: 2305-2316.doi: 10.4161/cc.10.14.16586.
  • Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651-657.doi: 10.1038/nature05185.
  • Pascher I, Sundell S (1985) Interactions and space requirements of the phosphate head group in membrane lipids. The Crystal structure of disodium lysophosphatidate dihydrate. Chem Phys Lipids 37: 241-250.doi: 10.1016/0009-3084(85)90012-X.
  • Pleskot R, Li J, Žárský V, Potocký M, Staiger CJ (2013) Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid. Trends Plant Sci 18: 496-504.doi: 10.1016/j.tplants.2013.04.005.
  • Pomorski TG, Nylander T, Cárdenas M (2014) Model cell membranes: Discerning lipid and protein contributions in shaping the cell. Adv Colloid Interface Sci 205: 207-220.doi: 10.1016/j.cis.2013.10.028.
  • Putta P, Rankenberg J, Korver RA, van Wijk R, Munnik T, Testerink C, Kooijman EE (2016) Phosphatidic acid binding proteins display differential binding as a function of membrane curvature stress and chemical properties. Biochim Biophys Acta 1858: 2709-2716.doi: 10.1016/j.bbamem.2016.07.014.
  • Santos HA, Vila-Viçosa D, Teixeira VH, Baptista AM, Machuqueiro M (2015) Constant-pH MD Simulations of DMPA/DMPC Lipid Bilayers. J Chem Theory Comput 11: 5973-5979.doi: 10.1021/acs.jctc.5b00956.
  • van Schooten B, Testerink C, Munnik T (2006) Signalling diacylglycerol pyrophosphate, a new phosphatidic acid metabolite. Biochim Biophys Acta 1761: 151-159.doi: 10.1016/j.bbalip.2005.12.010.
  • Selvy EP, Lavieri RR, Lindsley WC, Brown HA (2011) Phospholipase D: enzymology, functionality, and chemical modulation. Chem Rev 111: 6064-6119.doi: 10.1109/TMI.2012.2196707.
  • Shulga YV, Topham MK, Epand RM (2011) Regulation and functions of diacylglycerol kinases. Chem Rev 111: 6186-6208.doi: 10.1021/cr1004106.
  • Stace CL, Ktistakis NT (2006) Phosphatidic acid- and phosphatidylserine-binding proteins. Biochim Biophys Acta 1761: 913-926.doi: 10.1016/j.bbalip.2006.03.006.
  • Sung TC, Altshuller YM, Morris AJ, Frohman MA (1999a) Molecular analysis of mammalian phospholipase D2. J Biol Chem 274: 494-502.doi: 10.1074/jbc.274.1.494.
  • Sung TC, Zhang Y, Morris AJ, Frohman MA (1999b) Structural analysis of human phospholipase D1. J Biol Chem 274: 3659-3666.doi: 10.1074/jbc.274.6.3659.
  • Takahashi H, Yasue T, Ohki K, Hatta I (1995) Structural and thermotropic properties of calcium-dimyristoylphosphatidic acid complexes at acidic and neutral pH conditions. Biophys J 69: 1464-1472.doi: 10.1016/S0006-3495(95)80016-0.
  • Testerink C, Munnik T (2005) Phosphatidic acid: A multifunctional stress signaling lipid in plants. Trends Plant Sci 10: 368-375.doi: 10.1016/j.tplants.2005.06.002.
  • Toschi A, Lee E, Xu L, Garcia A, Gadir N, Foster DA (2009) Regulation of mTORC1 and mTORC2 Complex Assembly by Phosphatidic Acid: Competition with Rapamycin. Mol Cell Biol 29: 1411-1420.doi: 10.1128/MCB.00782-08.
  • Träuble H, Eibl H (1974) Electrostatic effects on lipid phase transitions: membrane structure and ionic environment. Proc Natl Acad Sci U S A 71: 214-219.doi: 10.1073/pnas.71.1.214.
  • Tritarelli A, Oricchio E, Ciciarello M, Mangiacasale R, Palena A, Lavia P, Soddu S, Cundari E (2004) p53 Localization at centrosomes during mitosis and postmitotic checkpoint are ATM-dependent and require serine 15 phosphorylation. Mol Biol Cell 15: 3751-3737.doi: 10.1091/mbc.e03-12-0900.
  • Vance JE, Vance DE (2004) Phospholipid biosynthesis in mammalian cells. Biochem Cell Biol 82: 113-128.doi: 10.1139/o03-073.
  • Vaz WL (1994) Diffusion and chemical reactions in phase-separated membranes. Biophys Chem 50: 139-145.doi: 10.1016/0301-4622(94)85026-7.
  • Verkleij AJ, de Maagd R, Leunissen-Bijvelt J, de Kruijff B (1982) Divalent cations and chlorpromazine can induce non-bilayer structures in phosphatidic acid-containing model membranes. Biochim Biophys Acta 684: 255-262.doi: 10.1016/0005-2736(82)90014-1.
  • Veverka V, Crabbe T, Bird I, Lennie G, Muskett FW, Taylor RJ, Carr MD (2008) Structural characterization of the interaction of mTOR with phosphatidic acid and a novel class of inhibitor: compelling evidence for a central role of the FRB domain in small molecule-mediated regulation of mTOR. Oncogene 27: 585-595.doi: 10.1038/sj.onc.1210693.
  • Vila-Vicosa D, Teixeira VH, Santos HA, Baptista AM, Machuqueiro M (2014) Treatment of ionic strength in biomolecular simulations of charged lipid bilayers. J Chem Theory Comput 10: 5483-5492.doi: 10.1021/ct500680q.
  • Watanabe Y, Tamura Y, Kawano S, Endo T (2015) Structural and mechanistic insights into phospholipid transfer by Ups1-Mdm35 in mitochondria. Nat Commun 6: 7922.doi: 10.1038/ncomms8922.
  • Wendel AA, Lewin TM, Coleman RA (2009) Glycerol-3-phosphate acyltransferases: Rate limiting enzymes of triacylglycerol biosynthesis. Biochim Biophys Acta 1791: 501-506.doi: 10.1016/j.bbalip.2008.10.010.
  • Wissing JB, Behrbohm H (1993) Diacylglycerol pyrophosphate, a novel phospholipid compound. FEBS Lett 315: 95-99.doi: 10.1016/0014-5793(93)81141-L.
  • Yamashita T, Eguchi K, Saitoh N, von Gersdorff H, Takahashi T (2010) Developmental shift to a mechanism of synaptic vesicle endocytosis requiring nanodomain Ca2+. Nat Neurosci 13: 838-844.doi: 10.1038/nn.2576.
  • Yang CY, Frohman MA (2012) Mitochondria: Signaling with phosphatidic acid. Int J Biochem Cell Biol 44: 1346-1350.doi: 10.1016/j.biocel.2012.05.006.
  • Yang JS, Gad H, Lee SY, Mironov A, Zhang L, Beznoussenko GV, Valente C, Turacchio G, Bonsra AN, Du G, Baldanzi G, Graziani A, Bourgoin S, Frohman MA, Luini A, Hsu VW (2008) A role for phosphatidic acid in COPI vesicle fission yields insights into Golgi maintenance. Nat Cell Biol 10: 1146-1153.doi: 10.1038/ncb1774.
  • Yao CK, Lin YQ, Ly CV, Ohyama T, Haueter CM, Moiseenkova-Bell VY, Wensel TG, Bellen HJ (2009) A synaptic vesicle-associated Ca2+ channel promotes endocytosis and couples exocytosis to endocytosis. Cell 138: 947-960.doi: 10.1016/j.cell.2009.06.033.
  • Young BP, Shin JJ, Orij R, Chao JT, Li SC, Guan XL, Khong A, Jan E, Wenk MR, Prinz WA, Smits GJ, Loewen CJ (2010) Phosphatidic acid is a pH biosensor that links membrane biogenesis to metabolism. Science 329: 1085-1088.doi: 10.1126/science.1191026.
  • Zhang C, Wendel AA, Keogh MR, Harris TE, Chen J, Coleman RA (2012) Glycerolipid signals alter mTOR complex 2 (mTORC2) to diminish insulin signaling. Proc Natl Acad Sci U S A 109: 1667-1672.doi: 10.1073/pnas.1110730109.
  • Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7: 9-19.doi: 10.1038/nrm1784.
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