Advertisement

Guidelines for the Use of Protein Domains in Acidic Phospholipid Imaging

  • Matthieu Pierre Platre
  • Yvon JaillaisEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1376)

Abstract

Acidic phospholipids are minor membrane lipids but critically important for signaling events. The main acidic phospholipids are phosphatidylinositol phosphates (PIPs also known as phosphoinositides), phosphatidylserine (PS), and phosphatidic acid (PA). Acidic phospholipids are precursors of second messengers of key signaling cascades or are second messengers themselves. They regulate the localization and activation of many proteins, and are involved in virtually all membrane trafficking events. As such, it is crucial to understand the subcellular localization and dynamics of each of these lipids within the cell. Over the years, several techniques have emerged in either fixed or live cells to analyze the subcellular localization and dynamics of acidic phospholipids. In this chapter, we review one of them: the use of genetically encoded biosensors that are based on the expression of specific lipid binding domains (LBDs) fused to fluorescent proteins. We discuss how to design such sensors, including the criteria for selecting the lipid binding domains of interest and to validate them. We also emphasize the care that must be taken during data analysis as well as the main limitations and advantages of this approach.

Key words

Biosensor Phosphatidylinositol phosphate Phosphatidic acid Phosphatidylserine Genetically encoded probes Lipid binding domain Live imaging PtdIns Lipid signaling Phospholipase 

Notes

Acknowledgement

We thank Mathilde Simon, Marie-Cécile Caillaud, and Marlene Dreux for commenting the manuscript. Y.J. has received funding from the European Research Council—ERC Grant Agreement no. [3363360-APPL] and from the Marie Curie Action—CIG Grant Agreement no. [PCIG-GA-2011-303601] under the European Union’s Seventh Framework Programme (FP/2007-2013).

References

  1. 1.
    Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9(2):99–111. doi: 10.1038/nrm2328 PubMedCrossRefGoogle Scholar
  2. 2.
    McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438(7068):605–611. doi: 10.1038/nature04398 PubMedCrossRefGoogle Scholar
  3. 3.
    Jean S, Kiger AA (2012) Coordination between RAB GTPase and phosphoinositide regulation and functions. Nat Rev Mol Cell Biol 13(7):463–470. doi: 10.1038/nrm3379 PubMedCrossRefGoogle Scholar
  4. 4.
    Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93(3):1019–1137. doi: 10.1152/physrev.00028.2012 PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Kay JG, Grinstein S (2013) Phosphatidylserine-mediated cellular signaling. Adv Exp Med Biol 991:177–193. doi: 10.1007/978-94-007-6331-9_10 PubMedCrossRefGoogle Scholar
  6. 6.
    Kay JG, Koivusalo M, Ma X, Wohland T, Grinstein S (2012) Phosphatidylserine dynamics in cellular membranes. Mol Biol Cell 23(11):2198–2212. doi: 10.1091/mbc.E11-11-0936 PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Hankins HM, Baldridge RD, Xu P, Graham TR (2015) Role of flippases, scramblases and transfer proteins in phosphatidylserine subcellular distribution. Traffic 16(1):35–47. doi: 10.1111/tra.12233 PubMedCrossRefGoogle Scholar
  8. 8.
    Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, Grinstein S (2008) Membrane phosphatidylserine regulates surface charge and protein localization. Science 319(5860):210–213. doi: 10.1126/science.1152066 PubMedCrossRefGoogle Scholar
  9. 9.
    Fairn GD, Schieber NL, Ariotti N, Murphy S, Kuerschner L, Webb RI, Grinstein S, Parton RG (2011) High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine. J Cell Biol 194(2):257–275. doi: 10.1083/jcb.201012028 PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9(2):112–124. doi: 10.1038/nrm2330 PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Athenstaedt K, Daum G (1999) Phosphatidic acid, a key intermediate in lipid metabolism. Eur J Biochem 266(1):1–16PubMedCrossRefGoogle Scholar
  12. 12.
    Cazzolli R, Shemon AN, Fang MQ, Hughes WE (2006) Phospholipid signalling through phospholipase D and phosphatidic acid. IUBMB Life 58(8):457–461. doi: 10.1080/15216540600871142 PubMedCrossRefGoogle Scholar
  13. 13.
    Horchani H, de Saint-Jean M, Barelli H, 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(11):e113484. doi: 10.1371/journal.pone.0113484 PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Bigay J, Antonny B (2012) Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev Cell 23(5):886–895. doi: 10.1016/j.devcel.2012.10.009 PubMedCrossRefGoogle Scholar
  15. 15.
    Kay JG, Grinstein S (2011) Sensing phosphatidylserine in cellular membranes. Sensors (Basel) 11(2):1744–1755. doi: 10.3390/s110201744 CrossRefGoogle Scholar
  16. 16.
    Leventis PA, Grinstein S (2010) The distribution and function of phosphatidylserine in cellular membranes. Annu Rev Biophys 39:407–427. doi: 10.1146/annurev.biophys.093008.131234 PubMedCrossRefGoogle Scholar
  17. 17.
    Dall’Armi C, Devereaux KA, Di Paolo G (2013) The role of lipids in the control of autophagy. Curr Biol 23(1):R33–R45. doi: 10.1016/j.cub.2012.10.041 PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182(4):685–701. doi: 10.1083/jcb.200803137 PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Hammond GR, Schiavo G, Irvine RF (2009) Immunocytochemical techniques reveal multiple, distinct cellular pools of PtdIns4P and PtdIns(4,5)P(2). Biochem J 422(1):23–35. doi: 10.1042/BJ20090428 PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Hammond GR, Machner MP, Balla T (2014) A novel probe for phosphatidylinositol 4-phosphate reveals multiple pools beyond the Golgi. J Cell Biol 205(1):113–126. doi: 10.1083/jcb.201312072 PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Levine TP, Munro S (2002) Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr Biol 12(9):695–704PubMedCrossRefGoogle Scholar
  22. 22.
    Cruz-Garcia D, Ortega-Bellido M, Scarpa M, Villeneuve J, Jovic M, Porzner M, Balla T, Seufferlein T, Malhotra V (2013) Recruitment of arfaptins to the trans-Golgi network by PI(4)P and their involvement in cargo export. EMBO J 32(12):1717–1729. doi: 10.1038/emboj.2013.116 PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Szentpetery Z, Varnai P, Balla T (2010) Acute manipulation of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc Natl Acad Sci U S A 107(18):8225–8230. doi: 10.1073/pnas.1000157107 PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Daboussi L, Costaguta G, Payne GS (2012) Phosphoinositide-mediated clathrin adaptor progression at the trans-Golgi network. Nat Cell Biol 14(3):239–248. doi: 10.1038/ncb2427 PubMedCrossRefGoogle Scholar
  25. 25.
    Hammond GR, Fischer MJ, Anderson KE, Holdich J, Koteci A, Balla T, Irvine RF (2012) PI4P and PI(4,5)P2 are essential but independent lipid determinants of membrane identity. Science 337(6095):727–730. doi: 10.1126/science.1222483 PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Stefan CJ, Manford AG, Emr SD (2013) ER-PM connections: sites of information transfer and inter-organelle communication. Curr Opin Cell Biol 25(4):434–442. doi: 10.1016/j.ceb.2013.02.020 PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Manford AG, Stefan CJ, Yuan HL, Macgurn JA, Emr SD (2012) ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev Cell 23(6):1129–1140. doi: 10.1016/j.devcel.2012.11.004 PubMedCrossRefGoogle Scholar
  28. 28.
    Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD (2011) Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144(3):389–401. doi: 10.1016/j.cell.2010.12.034 PubMedCrossRefGoogle Scholar
  29. 29.
    Ling Y, Stefan CJ, Macgurn JA, Audhya A, Emr SD (2012) The dual PH domain protein Opy1 functions as a sensor and modulator of PtdIns(4,5)P(2) synthesis. EMBO J 31(13):2882–2894. doi: 10.1038/emboj.2012.127 PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Gozani O, Karuman P, Jones DR, Ivanov D, Cha J, Lugovskoy AA, Baird CL, Zhu H, Field SJ, Lessnick SL, Villasenor J, Mehrotra B, Chen J, Rao VR, Brugge JS, Ferguson CG, Payrastre B, Myszka DG, Cantley LC, Wagner G, Divecha N, Prestwich GD, Yuan J (2003) The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114(1):99–111PubMedCrossRefGoogle Scholar
  31. 31.
    Viaud J, Lagarrigue F, Ramel D, Allart S, Chicanne G, Ceccato L, Courilleau D, Xuereb JM, Pertz O, Payrastre B, Gaits-Iacovoni F (2014) Phosphatidylinositol 5-phosphate regulates invasion through binding and activation of Tiam1. Nat Commun 5:4080. doi: 10.1038/ncomms5080 PubMedCrossRefGoogle Scholar
  32. 32.
    Viaud J, Boal F, Tronchere H, Gaits-Iacovoni F, Payrastre B (2014) Phosphatidylinositol 5-phosphate: a nuclear stress lipid and a tuner of membranes and cytoskeleton dynamics. Bioessays 36(3):260–272. doi: 10.1002/bies.201300132 PubMedCrossRefGoogle Scholar
  33. 33.
    Ramel D, Lagarrigue F, Pons V, Mounier J, Dupuis-Coronas S, Chicanne G, Sansonetti PJ, Gaits-Iacovoni F, Tronchere H, Payrastre B (2011) Shigella flexneri infection generates the lipid PI5P to alter endocytosis and prevent termination of EGFR signaling. Sci Signal 4(191):ra61. doi: 10.1126/scisignal.2001619 PubMedCrossRefGoogle Scholar
  34. 34.
    Guittard G, Gerard A, Dupuis-Coronas S, Tronchere H, Mortier E, Favre C, Olive D, Zimmermann P, Payrastre B, Nunes JA (2009) Cutting edge: Dok-1 and Dok-2 adaptor molecules are regulated by phosphatidylinositol 5-phosphate production in T cells. J Immunol 182(7):3974–3978. doi: 10.4049/jimmunol.0804172 PubMedCrossRefGoogle Scholar
  35. 35.
    Vicinanza M, Korolchuk VI, Ashkenazi A, Puri C, Menzies FM, Clarke JH, Rubinsztein DC (2015) PI(5)P Regulates Autophagosome Biogenesis. Mol Cell 57(2):219–234. doi: 10.1016/j.molcel.2014.12.007 PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Eugster A, Pecheur EI, Michel F, Winsor B, Letourneur F, Friant S (2004) Ent5p is required with Ent3p and Vps27p for ubiquitin-dependent protein sorting into the multivesicular body. Mol Biol Cell 15(7):3031–3041. doi: 10.1091/mbc.E03-11-0793 PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Friant S, Pecheur EI, Eugster A, Michel F, Lefkir Y, Nourrisson D, Letourneur F (2003) Ent3p Is a PtdIns(3,5)P2 effector required for protein sorting to the multivesicular body. Dev Cell 5(3):499–511PubMedCrossRefGoogle Scholar
  38. 38.
    Li X, Wang X, Zhang X, Zhao M, Tsang WL, Zhang Y, Yau RG, Weisman LS, Xu H (2013) Genetically encoded fluorescent probe to visualize intracellular phosphatidylinositol 3,5-bisphosphate localization and dynamics. Proc Natl Acad Sci U S A 110(52):21165–21170. doi: 10.1073/pnas.1311864110 PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Zoncu R, Perera RM, Sebastian R, Nakatsu F, Chen H, Balla T, Ayala G, Toomre D, De Camilli PV (2007) Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proc Natl Acad Sci U S A 104(10):3793–3798. doi: 10.1073/pnas.0611733104 PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Simon ML, Platre MP, Assil S, van Wijk R, Chen WY, Chory J, Dreux M, Munnik T, Jaillais Y (2014) A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis. Plant J 77(2):322–337. doi: 10.1111/tpj.12358 PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Schmid SL, Mettlen M (2013) Cell biology: lipid switches and traffic control. Nature 499(7457):161–162. doi: 10.1038/nature12408 PubMedCrossRefGoogle Scholar
  42. 42.
    Suh BC, Inoue T, Meyer T, Hille B (2006) Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels. Science 314(5804):1454–1457. doi: 10.1126/science.1131163 PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Posor Y, Eichhorn-Gruenig M, Puchkov D, Schoneberg J, Ullrich A, Lampe A, Muller R, Zarbakhsh S, Gulluni F, Hirsch E, Krauss M, Schultz C, Schmoranzer J, Noe F, Haucke V (2013) Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499(7457):233–237. doi: 10.1038/nature12360 PubMedCrossRefGoogle Scholar
  44. 44.
    Uchida Y, Hasegawa J, Chinnapen D, Inoue T, Okazaki S, Kato R, Wakatsuki S, Misaki R, Koike M, Uchiyama Y, Iemura S, Natsume T, Kuwahara R, Nakagawa T, Nishikawa K, Mukai K, Miyoshi E, Taniguchi N, Sheff D, Lencer WI, Taguchi T, Arai H (2011) Intracellular phosphatidylserine is essential for retrograde membrane traffic through endosomes. Proc Natl Acad Sci U S A 108(38):15846–15851. doi: 10.1073/pnas.1109101108 PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Varnai P, Balla T (2006) Live cell imaging of phosphoinositide dynamics with fluorescent protein domains. Biochim Biophys Acta 1761(8):957–967. doi: 10.1016/j.bbalip.2006.03.019 PubMedCrossRefGoogle Scholar
  46. 46.
    Kutateladze TG (2010) Translation of the phosphoinositide code by PI effectors. Nat Chem Biol 6(7):507–513. doi: 10.1038/nchembio.390 PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Moravcevic K, Mendrola JM, Schmitz KR, Wang YH, Slochower D, Janmey PA, Lemmon MA (2010) Kinase associated-1 domains drive MARK/PAR1 kinases to membrane targets by binding acidic phospholipids. Cell 143(6):966–977. doi: 10.1016/j.cell.2010.11.028 PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Nishioka T, Frohman MA, Matsuda M, Kiyokawa E (2010) Heterogeneity of phosphatidic acid levels and distribution at the plasma membrane in living cells as visualized by a Foster resonance energy transfer (FRET) biosensor. J Biol Chem 285(46):35979–35987. doi: 10.1074/jbc.M110.153007 PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Cicchetti G, Biernacki M, Farquharson J, Allen PG (2004) A ratiometric expressible FRET sensor for phosphoinositides displays a signal change in highly dynamic membrane structures in fibroblasts. Biochemistry 43(7):1939–1949. doi: 10.1021/bi035480w PubMedCrossRefGoogle Scholar
  50. 50.
    van der Wal J, Habets R, Varnai P, Balla T, Jalink K (2001) Monitoring agonist-induced phospholipase C activation in live cells by fluorescence resonance energy transfer. J Biol Chem 276(18):15337–15344. doi: 10.1074/jbc.M007194200 PubMedCrossRefGoogle Scholar
  51. 51.
    Sato M, Ueda Y, Takagi T, Umezawa Y (2003) Production of PtdInsP3 at endomembranes is triggered by receptor endocytosis. Nat Cell Biol 5(11):1016–1022. doi: 10.1038/ncb1054 PubMedCrossRefGoogle Scholar
  52. 52.
    Niu Y, Zhang C, Sun Z, Hong Z, Li K, Sun D, Yang Y, Tian C, Gong W, Liu JJ (2013) PtdIns(4)P regulates retromer-motor interaction to facilitate dynein-cargo dissociation at the trans-Golgi network. Nat Cell Biol 15(4):417–429. doi: 10.1038/ncb2710 PubMedCrossRefGoogle Scholar
  53. 53.
    Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 19(17):4577–4588. doi: 10.1093/emboj/19.17.4577 PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Yu JW, Mendrola JM, Audhya A, Singh S, Keleti D, DeWald DB, Murray D, Emr SD, Lemmon MA (2004) Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol Cell 13(5):677–688PubMedCrossRefGoogle Scholar
  55. 55.
    Toth DJ, Toth JT, Gulyas G, Balla A, Balla T, Hunyady L, Varnai P (2012) Acute depletion of plasma membrane phosphatidylinositol 4,5-bisphosphate impairs specific steps in endocytosis of the G-protein-coupled receptor. J Cell Sci 125(Pt 9):2185–2197. doi: 10.1242/jcs.097279 PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006) PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314(5804):1458–1461. doi: 10.1126/science.1134389 PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, Milosevic I, Gracheva EO, Bagriantsev SN, Borgese N, De Camilli P (2013) PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153(7):1494–1509. doi: 10.1016/j.cell.2013.05.026 PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Idevall-Hagren O, Dickson EJ, Hille B, Toomre DK, De Camilli P (2012) Optogenetic control of phosphoinositide metabolism. Proc Natl Acad Sci U S A 109(35):E2316–E2323. doi: 10.1073/pnas.1211305109 PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Hammond GR (2012) Membrane biology: making light work of lipids. Curr Biol 22(20):R869–R871. doi: 10.1016/j.cub.2012.09.005 PubMedCrossRefGoogle Scholar
  60. 60.
    Kanai F, Liu H, Field SJ, Akbary H, Matsuo T, Brown GE, Cantley LC, Yaffe MB (2001) The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat Cell Biol 3(7):675–678. doi: 10.1038/35083070 PubMedCrossRefGoogle Scholar
  61. 61.
    Ellson CD, Gobert-Gosse S, Anderson KE, Davidson K, Erdjument-Bromage H, Tempst P, Thuring JW, Cooper MA, Lim ZY, Holmes AB, Gaffney PR, Coadwell J, Chilvers ER, Hawkins PT, Stephens LR (2001) PtdIns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of p40(phox). Nat Cell Biol 3(7):679–682. doi: 10.1038/35083076 PubMedCrossRefGoogle Scholar
  62. 62.
    Safi A, Vandromme M, Caussanel S, Valdacci L, Baas D, Vidal M, Brun G, Schaeffer L, Goillot E (2004) Role for the pleckstrin homology domain-containing protein CKIP-1 in phosphatidylinositol 3-kinase-regulated muscle differentiation. Mol Cell Biol 24(3):1245–1255PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Maffucci T, Brancaccio A, Piccolo E, Stein RC, Falasca M (2003) Insulin induces phosphatidylinositol-3-phosphate formation through TC10 activation. EMBO J 22(16):4178–4189. doi: 10.1093/emboj/cdg402 PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Roy A, Levine TP (2004) Multiple pools of phosphatidylinositol 4-phosphate detected using the pleckstrin homology domain of Osh2p. J Biol Chem 279(43):44683–44689. doi: 10.1074/jbc.M401583200 PubMedCrossRefGoogle Scholar
  65. 65.
    Sarkes D, Rameh LE (2010) A novel HPLC-based approach makes possible the spatial characterization of cellular PtdIns5P and other phosphoinositides. Biochem J 428(3):375–384. doi: 10.1042/BJ20100129 PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Varnai P, Balla T (1998) Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J Cell Biol 143(2):501–510PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Ben El Kadhi K, Roubinet C, Solinet S, Emery G, Carreno S (2011) The inositol 5-phosphatase dOCRL controls PI(4,5)P2 homeostasis and is necessary for cytokinesis. Curr Biol 21(12):1074–1079. doi: 10.1016/j.cub.2011.05.030 PubMedCrossRefGoogle Scholar
  68. 68.
    Szentpetery Z, Balla A, Kim YJ, Lemmon MA, Balla T (2009) Live cell imaging with protein domains capable of recognizing phosphatidylinositol 4,5-bisphosphate; a comparative study. BMC Cell Biol 10:67. doi: 10.1186/1471-2121-10-67 PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Santagata S, Boggon TJ, Baird CL, Gomez CA, Zhao J, Shan WS, Myszka DG, Shapiro L (2001) G-protein signaling through tubby proteins. Science 292(5524):2041–2050. doi: 10.1126/science.1061233 PubMedCrossRefGoogle Scholar
  70. 70.
    Dove SK, Piper RC, McEwen RK, Yu JW, King MC, Hughes DC, Thuring J, Holmes AB, Cooke FT, Michell RH, Parker PJ, Lemmon MA (2004) Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors. EMBO J 23(9):1922–1933. doi: 10.1038/sj.emboj.7600203 PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Dowler S, Currie RA, Campbell DG, Deak M, Kular G, Downes CP, Alessi DR (2000) Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities. Biochem J 351(Pt 1):19–31PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Marshall AJ, Krahn AK, Ma K, Duronio V, Hou S (2002) TAPP1 and TAPP2 are targets of phosphatidylinositol 3-kinase signaling in B cells: sustained plasma membrane recruitment triggered by the B-cell antigen receptor. Mol Cell Biol 22(15):5479–5491PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Varnai P, Rother KI, Balla T (1999) Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton’s tyrosine kinase pleckstrin homology domain visualized in single living cells. J Biol Chem 274(16):10983–10989PubMedCrossRefGoogle Scholar
  74. 74.
    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(12):1424–1430. doi: 10.1038/ncb2351 PubMedCrossRefGoogle Scholar
  75. 75.
    Yeung T, Heit B, Dubuisson JF, Fairn GD, Chiu B, Inman R, Kapus A, Swanson M, Grinstein S (2009) Contribution of phosphatidylserine to membrane surface charge and protein targeting during phagosome maturation. J Cell Biol 185(5):917–928. doi: 10.1083/jcb.200903020 PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Kassas N, Tryoen-Toth P, Corrotte M, Thahouly T, Bader MF, Grant NJ, Vitale N (2012) Genetically encoded probes for phosphatidic acid. Methods Cell Biol 108:445–459. doi: 10.1016/B978-0-12-386487-1.00020-1 PubMedCrossRefGoogle Scholar
  77. 77.
    Zhang F, Wang Z, Lu M, Yonekubo Y, Liang X, Zhang Y, Wu P, Zhou Y, Grinstein S, Hancock JF, Du G (2014) Temporal production of the signaling lipid phosphatidic acid by phospholipase D2 determines the output of extracellular signal-regulated kinase signaling in cancer cells. Mol Cell Biol 34(1):84–95. doi: 10.1128/MCB.00987-13 PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Bohdanowicz M, Schlam D, Hermansson M, Rizzuti D, Fairn GD, Ueyama T, Somerharju P, Du G, Grinstein S (2013) Phosphatidic acid is required for the constitutive ruffling and macropinocytosis of phagocytes. Mol Biol Cell 24(11):1700–1712. doi: 10.1091/mbc.E12-11-0789, S1701-1707PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Antonescu CN, Aguet F, Danuser G, Schmid SL (2011) Phosphatidylinositol-(4,5)-bisphosphate regulates clathrin-coated pit initiation, stabilization, and size. Mol Biol Cell 22(14):2588–2600. doi: 10.1091/mbc.E11-04-0362 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Laboratoire de Reproduction et Développement des Plantes, CNRS, INRA, ENS Lyon, UCBLUniversité de LyonLyon Cedex 07France

Personalised recommendations