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Cellular and Molecular Life Sciences

, Volume 67, Issue 23, pp 3927–3946 | Cite as

One lipid, multiple functions: how various pools of PI(4,5)P2 are created in the plasma membrane

  • Katarzyna KwiatkowskaEmail author
Review

Abstract

Phosphatidylinositol 4,5-bisphosphate [PI(4,5)P2] is a minor lipid of the inner leaflet of the plasma membrane that controls the activity of numerous proteins and serves as a source of second messengers. This multifunctionality of PI(4,5)P2 relies on mechanisms ensuring transient appearance of PI(4,5)P2 clusters in the plasma membrane. One such mechanism involves phosphorylation of PI(4)P to PI(4,5)P2 by the type I phosphatidylinositol-4-phosphate 5-kinases (PIP5KI) at discrete membrane locations coupled with PI(4)P delivery/synthesis at the plasma membrane. Simultaneously, both PI(4)P and PI(4,5)P2 participate in anchoring PIP5KI at the plasma membrane via electrostatic bonds. PIP5KI isoforms are also selectively recruited and activated at the plasma membrane by Rac1, talin, or AP-2 to generate PI(4,5)P2 in ruffles and lamellipodia, focal contacts, and clathrin-coated pits. In addition, PI(4,5)P2 can accumulate at sphingolipid/cholesterol-based rafts following activation of distinct membrane receptors or be sequestered in a reversible manner due to electrostatic constrains posed by proteins like MARCKS.

Keywords

Plasma membrane Phosphatidylinositol 4,5-bisphosphate Type I phosphatidylinositol-4-phosphate 5-kinases Rac1 Talin AP-2 Lipid rafts 

Abbreviations

FERM

Band 4.1-ezrin-radixin-moesin homology

BTK

Bruton’s tyrosine kinase

DAG

Diacylglycerol

DAGK

Diacylglycerol kinase

EGF

Epidermal growth factor

IP3

Inositol trisphosphate

MDCK

Madin-Darby kidney cells

MARCKS

Myristoylated alanine-rich C kinase substrate

GAP43

Growth-associated protein 43

OCRL1

Oculocerebrorenal syndrome of Lowe 1 phosphatase

OSBP

Oxysterol-binding protein

PTEN

Phosphatase and tensin homologue on chromosome 10

PA

Phosphatidic acid

PI

Phosphatidylinositol

PIPK

Phosphatidylinositol phosphate kinase

PI3K

Phosphatidylinositol 3-kinase

PI4K

Phosphatidylinositol 4-kinase

PI(3)P

Phosphatidylinositol 3-monophosphate

PI(4)P

Phosphatidylinositol 4-monophosphate

PI(5)P

Phosphatidylinositol 5-monophosphate

PI(4,5)P2

Phosphatidylinositol 4,5-bishosphate

PI(3,4,5)P3

Phosphatidylinositol 3,4,5-trisphosphate

Fapp

Phosphatidylinositol-4-phosphate adaptor protein

IPP 5-Ptase

Inositol polyphosphate 5-phosphatase

PLC

Phospholipase C

PLD

Phospholipase D

PTB

Phosphotyrosine-binding

PH

Pleckstrin homology

PIP5KI

Type I phosphatidylinositol-4-phosphate 5-kinase

PIP4KII

Type II phosphatidylinositol-5-phosphate 4-kinase

OSH2

Yeast oxysterol-binding protein homologue

Notes

Acknowledgments

I gratefully thank Prof. Andrzej Sobota, Nencki Institute of Experimental Biology, Warsaw, for support and excellent discussion. I also thank Prof. Jan Fronk, Warsaw University, for valuable comments on the manuscript.

References

  1. 1.
    Hokin MR, Hokin LE (1953) Enzyme secretion and the incorporation of P32 into phospholipides of pancreas slices. J Biol Chem 203:967–977PubMedGoogle Scholar
  2. 2.
    Yin HL, Janmey PA (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65:761–789PubMedGoogle Scholar
  3. 3.
    Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657PubMedGoogle Scholar
  4. 4.
    Rameh LE, Cantley LC (1999) The role of phosphoinositide 3-kinase lipid products in cell function. J Biol Chem 274:8347–8350PubMedGoogle Scholar
  5. 5.
    Maehama T, Dixon JE (1998) The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 273:13375–13378PubMedGoogle Scholar
  6. 6.
    McPherson PS, Garcia EP, Slepnev VI, David C, Zhang X, Grabs D, Sossin WS, Bauerfeind R, Nemoto Y, De Camilli P (1996) A presynaptic inositol-5-phosphatase. Nature 379:353–357PubMedGoogle Scholar
  7. 7.
    Nemoto Y, Arribas M, Haffner C, DeCamilli P (1997) Synaptojanin 2, a novel synaptojanin isoform with a distinct targeting domain and expression pattern. J Biol Chem 272:30817–30821PubMedGoogle Scholar
  8. 8.
    Lowe M (2005) Structure and function of the Lowe syndrome protein OCRL. Traffic 6:711–719PubMedGoogle Scholar
  9. 9.
    Ungewickell A, Hugge C, Kisseleva M, Chang SC, Zou J, Feng Y, Galyov EE, Wilson M, Majerus PW (2005) The identification and characterization of two phosphatidylinositol-4,5-bisphosphate 4-phosphatases. Proc Natl Acad Sci USA 102:18854–18859PubMedGoogle Scholar
  10. 10.
    Lowe CU, Terrey M, MacLachlan EA (1952) Organic-aciduria, decreased renal ammonia production, hydrophthalmos, and mental retardation; a clinical entity. AMA Am J Dis Child 83:164–184PubMedGoogle Scholar
  11. 11.
    Leahey AM, Charnas LR, Nussbaum RL (1993) Nonsense mutations in the OCRL-1 gene in patients with the oculocerebrorenal syndrome of Lowe. Hum Mol Genet 2:461–463PubMedGoogle Scholar
  12. 12.
    Cremona O, Di Paolo G, Wenk MR, Lüthi A, Kim WT, Takei K, Daniell L, Nemoto Y, Shears SB, Flavell RA, McCormick DA, De Camilli P (1999) Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99:179–188PubMedGoogle Scholar
  13. 13.
    Voronov SV, Frere SG, Giovedi S, Pollina EA, Borel C, Zhang H, Schmidt C, Akeson EC, Wenk MR, Cimasoni L, Arancio O, Davisson MT, Antonarakis SE, Gardiner K, De Camilli P, Di Paolo G (2008) Synaptojanin 1-linked phosphoinositide dyshomeostasis and cognitive deficits in mouse models of Down’s syndrome. Proc Natl Acad Sci USA 105:9415–9420PubMedGoogle Scholar
  14. 14.
    Zou J, Marjanovic J, Kisseleva MV, Wilson M, Majerus PW (2007) Type I phosphatidylinositol-4,5-bisphosphate 4-phosphatase regulates stress-induced apoptosis. Proc Natl Acad Sci USA 104:16834–16839PubMedGoogle Scholar
  15. 15.
    Dove SK, Dong K, Kobayashi T, Williams FK, Michell RH (2009) Phosphatidylinositol 3,5-bisphosphate and Fab1p/PIKfyve underPPIn endo-lysosome function. Biochem J 419:1–13PubMedGoogle Scholar
  16. 16.
    Sbrissa D, Ikonomov OC, Deeb R, Shisheva A (2002) Phosphatidylinositol 5-phosphate biosynthesis is linked to PIKfyve and is involved in osmotic response pathway in mammalian cells. J Biol Chem 277:47276–47284PubMedGoogle Scholar
  17. 17.
    Coronas S, Lagarrigue F, Ramel D, Chicanne G, Delsol G, Payrastre B, Tronchere H (2008) Elevated levels of PtdIns5P in NPM-ALK transformed cells: implication of PIKfyve. Biochem Biophys Res Commun 372:351–355PubMedGoogle Scholar
  18. 18.
    Shisheva A (2008) PIKfyve: partners, significance, debates, paradoxes. Cell Biol Int 32:591–604PubMedGoogle Scholar
  19. 19.
    Tolias KF, Rameh LE, Ishihara H, Shibasaki Y, Chen J, Prestwich GD, Cantley LC, Carpenter C (1998) Type I phosphatidylinositol-4-phosphate 5-kinases synthesize the novel lipids phosphatidylinositol 3,5-bisphosphate and phosphatidylinositol 5-phosphate. J Biol Chem 273:18040–18046PubMedGoogle Scholar
  20. 20.
    Ikonomov OC, Sbrissa D, Mlak K, Kanzaki M, Pessin J, Shisheva A (2002) Functional dissection of lipid and protein kinase signals of PIKfyve reveals the role of PtdIns 3,5-P2 production for endomembrane integrity. J Biol Chem 277:9206–9211PubMedGoogle Scholar
  21. 21.
    Ishihara H, Shibasaki Y, Kizuki N, Katagiri H, Yazaki Y, Asano T, Oka Y (1996) Cloning of cDNAs encoding two isoforms of 68-kDa type I phosphatidylinositol-4-phosphate 5-kinase. J Biol Chem 271:23611–23614PubMedGoogle Scholar
  22. 22.
    Loijens JC, Anderson RA (1996) Type I phosphatidylinositol-4-phosphate 5-kinases are distinct members of this novel lipid kinase family. J Biol Chem 271:32937–32943PubMedGoogle Scholar
  23. 23.
    Ishihara H, Shibasaki Y, Kizuki N, Wada T, Yazaki Y, Asano T, Oka Y (1998) Type I phosphatidylinositol-4-phosphate 5-kinases. Cloning of the third isoform and deletion/substitution analysis of members of this novel lipid kinase family. J Biol Chem 273:8741–8748PubMedGoogle Scholar
  24. 24.
    Giudici ML, Emson PC, Irvine RF (2004) A novel neuronal-specific splice variant of type I phosphatidylinositol 4-phosphate 5-kinase isoform γ. Biochem J 379:489–496PubMedGoogle Scholar
  25. 25.
    Di Paolo G, Moskowitz HS, Gipson K, Wenk MR, Voronov S, Obayashi M, Flavell R, Fitzsimonds RM, Ryan TA, De Camilli P (2004) Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature 431:415–422PubMedGoogle Scholar
  26. 26.
    Jenkins GH, Fisette PL, Anderson RA (1994) Type I phosphatidylinositol 4-phosphate 5-kinase isoforms are specifically stimulated by phosphatidic acid. J Biol Chem 269:11547–11554PubMedGoogle Scholar
  27. 27.
    Itoh T, Ishihara H, Shibasaki Y, Oka Y, Takenawa T (2000) Autophosphorylation of type I phosphatidylinositol phosphate kinase regulates its lipid kinase activity. J Biol Chem 275:19389–19394PubMedGoogle Scholar
  28. 28.
    Park SJ, Itoh T, Takenawa T (2001) Phosphatidylinositol 4-phosphate 5-kinase type I is regulated through phosphorylation response by extracellular stimuli. J Biol Chem 276:4781–4787PubMedGoogle Scholar
  29. 29.
    Di Paolo G, Pellegrini L, Letinic K, Cestra G, Zoncu R, Voronov S, Chang S, Guo J, Wenk MR, De Camilli P (2002) Recruitment and regulation of phosphatidylinositol phosphate kinase type 1γ by the FERM domain of talin. Nature 420:85–89PubMedGoogle Scholar
  30. 30.
    Ling K, Doughman RL, Firestone AJ, Bunce MW, Anderson RA (2002) Type Iγ phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420:89–93PubMedGoogle Scholar
  31. 31.
    Mellman DL, Gonzales ML, Song C, Barlow CA, Wang P, Kendziorski C, Anderson RA (2008) A PtdIns(4,5)P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature 451:1013–1017PubMedGoogle Scholar
  32. 32.
    Chang JD, Field SJ, Rameh LE, Carpenter CL, Cantley LC (2004) Identification and characterization of a phosphoinositide phosphate kinase homolog. J Biol Chem 279:11672–11679PubMedGoogle Scholar
  33. 33.
    Tolias KF, Hartwig JH, Ishihara H, Shibasaki Y, Cantley LC, Carpenter CL (2000) Type Iα phosphatidylinositol-4-phosphate 5-kinase mediates Rac-dependent actin assembly. Curr Biol 10:153–156PubMedGoogle Scholar
  34. 34.
    Yamamoto M, Chen MZ, Wang YJ, Sun HQ, Wei Y, Martinez M, Yin HL (2006) Hypertonic stress increases phosphatidylinositol 4,5-bisphosphate levels by activating PIP5KIβ. J Biol Chem 281:32630–32638PubMedGoogle Scholar
  35. 35.
    Wang Y, Litvinov RI, Chen X, Bach TL, Lian L, Petrich BG, Monkley SJ, Kanaho Y, Critchley DR, Sasaki T, Birnbaum MJ, Weisel JW, Hartwig J, Abrams CS (2008) Loss of PIP5KIγ, unlike other PIP5KI isoforms, impairs the integrity of the membrane cytoskeleton in murinsmegakaryocytes. J Clin Invest 118:812–881PubMedGoogle Scholar
  36. 36.
    Wang Y, Chen X, Lian L, Tang T, Stalker TJ, Sasaki T, Kanaho Y, Brass LF, Choi JK, Hartwig JH, Abrams CS (2008) Loss of PIP5KIβ demonstrates that PIP5KI isoform-specific PIP2 synthesis is required for IP3 formation. Proc Natl Acad Sci USA 105:14064–14069PubMedGoogle Scholar
  37. 37.
    Mao YS, Yamaga M, Zhu X, Wei Y, Sun H, Wang J, Yun M, Wang Y, Di Paolo G, Bennett M, Mellman I, Abrams CS, De Camilli P, Lu CY, Yin HL (2009) Essential and unique roles of PIP5K-γ and -α in Fcγ receptor-mediated phagocytosis. J Cell Biol 184:281–296PubMedGoogle Scholar
  38. 38.
    Coppolino MG, Dierckman R, Loijens J, Collins RF, Pouladi M, Jongstra-Bilen J, Schreiber AD, Trimble WS, Anderson R, Grinstein S (2002) Inhibition of phosphatidylinositol-4-phosphate 5-kinase Iα impairs localized actin remodeling and suppresses phagocytosis. J Biol Chem 277:43849–43857PubMedGoogle Scholar
  39. 39.
    Doughman RL, Firestone AJ, Wojtasiak ML, Bunce MW, Anderson RA (2003) Membrane ruffling requires coordination between type Iα phosphatidylinositol phosphate kinase and Rac signaling. J Biol Chem 278:23036–23045PubMedGoogle Scholar
  40. 40.
    Kisseleva M, Feng Y, Ward M, Song C, Anderson RA, Longmore GD (2005) The LIM protein Ajuba regulates phosphatidylinositol 4,5-bisphosphate levels in migrating cells through an interaction with and activation of PIPKIα. Mol Cell Biol 25:3956–3966PubMedGoogle Scholar
  41. 41.
    Chen MZ, Zhu X, Sun HQ, Mao YS, Wei Y, Yamamoto M, Yin HL (2009) Oxidative stress decreases phosphatidylinositol 4,5-bisphosphate levels by deactivating phosphatidylinositol-4-phosphate 5-kinase β in a Syk-dependent manner. J Biol Chem 284:23743–23753PubMedGoogle Scholar
  42. 42.
    Tolias KF, Couvillon AD, Cantley LC, Carpenter CL (1998) Characterization of a Rac1- and RhoGDI-associated lipid kinase signaling complex. Mol Cell Biol 18:762–770PubMedGoogle Scholar
  43. 43.
    Szymanska E, Korzeniowski M, Raynal P, Sobota A, Kwiatkowska K (2009) Contribution of PIP-5 kinase Iα to raft-based FcγRIIA signaling. Exp Cell Res 315:981–995PubMedGoogle Scholar
  44. 44.
    Shibasaki Y, Ishihara H, Kizuki N, Asano T, Oka Y, Yazaki Y (1997) Massive actin polymerization induced by phosphatidylinositol-4-phosphate 5-kinase in vivo. J Biol Chem 272:7578–7581PubMedGoogle Scholar
  45. 45.
    Rozelle AL, Machesky LM, Yamamoto M, Driessens MH, Insall RH, Roth MG, Luby-Phelps K, Marriott G, Hall A, Yin HL (2000) Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr Biol 10:311–320PubMedGoogle Scholar
  46. 46.
    Yamamoto M, Hilgemann DH, Feng S, Bito H, Ishihara H, Shibasaki Y, Yin HL (2001) Phosphatidylinositol 4,5-bisphosphate induces actin stress-fiber formation and inhibits membrane ruffling in CV1 cells. J Cell Biol 152:867–876PubMedGoogle Scholar
  47. 47.
    Boronenkov IV, Loijens JC, Umeda M, Anderson RA (1998) Phosphoinositide signaling pathways in nuclei are associated with nuclear speckles containing pre-mRNA processing factors. Mol Biol Cell 9:3547–3560PubMedGoogle Scholar
  48. 48.
    Padron D, Wang YJ, Yamamoto M, Yin H, Roth MG (2003) Phosphatidylinositol phosphate 5-kinase Iβ recruits AP-2 to the plasma membrane and regulates rates of constitutive endocytosis. J Cell Biol 162:693–701PubMedGoogle Scholar
  49. 49.
    Bairstow SF, Ling K, Su X, Firestone AJ, Carbonara C, Anderson RA (2006) Type Iγ661 phosphatidylinositol phosphate kinase directly interacts with AP2 and regulates endocytosis. J Biol Chem 281:20632–20642PubMedGoogle Scholar
  50. 50.
    Krauss M, Kukhtina V, Pechstein A, Haucke V (2006) Stimulation of phosphatidylinositol kinase type I-mediated phosphatidylinositol (4,5)-bisphosphate synthesis by AP-2 μ-cargo complexes. Proc Natl Acad Sci USA 103:11934–11939PubMedGoogle Scholar
  51. 51.
    Nakano-Kobayashi A, Yamazaki M, Unoki T, Hongu T, Murata C, Taguchi R, Katada T, Frohman MA, Yokozeki T, Kanaho Y (2007) Role of activation of PIP5Kγ661 by AP-2 complex in synaptic vesicle endocytosis. EMBO J 26:1105–1116PubMedGoogle Scholar
  52. 52.
    Ling K, Doughman RL, Iyer VV, Firestone AJ, Bairstow SF, Mosher DF, Schaller MD, Anderson RA (2003) Tyrosine phosphorylation of type Iγ phosphatidylinositol phosphate kinase by Src regulates an integrin-talin switch. J Cell Biol 163:1339–1349PubMedGoogle Scholar
  53. 53.
    Powner DJ, Payne RM, Pettitt TR, Giudici ML, Irvine RF, Wakelam MJ (2005) Phospholipase D2 stimulates integrin-mediated adhesion via phosphatidylinositol 4-phosphate 5-kinase Iγb. J Cell Sci 118:2975–2986PubMedGoogle Scholar
  54. 54.
    El Sayegh TY, Arora PD, Ling K, Laschinger C, Janmey PA, Anderson RA, McCulloch CA (2007) Phosphatidylinositol-4,5 bisphosphate produced by PIP5KIγ regulates gelsolin, actin assembly, and adhesion strength of N-cadherin junctions. Mol Biol Cell 18:3026–3038PubMedGoogle Scholar
  55. 55.
    McEwen RK, Dove SK, Cooke FT, Painter GF, Holmes AB, Shisheva A, Ohya Y, Parker PJ, Michell RH (1999) Complementation analysis in PtdInsP kinase-deficient yeast mutants demonstrates that Schizosaccharomyces pombe and murine Fab1p homologues are phosphatidylinositol 3-phosphate 5-kinases. J Biol Chem 274:33905–33912PubMedGoogle Scholar
  56. 56.
    Kunz J, Wilson MP, Kisseleva M, Hurley JH, Majerus PW, Anderson RA (2000) The activation loop of phosphatidylinositol phosphate kinases determines signaling specificity. Mol Cell 5:1–11PubMedGoogle Scholar
  57. 57.
    Homma K, Terui S, Minemura M, Qadota H, Anraku Y, Kanaho Y, Ohya Y (1998) Phosphatidylinositol-4-phosphate 5-kinase localized on the plasma membrane is essential for yeast cell morphogenesis. J Biol Chem 273:15779–15786PubMedGoogle Scholar
  58. 58.
    Boronenkov IV, Anderson RA (1995) The sequence of phosphatidylinositol-4-phosphate 5-kinase defines a novel family of lipid kinases. J Biol Chem 270:2881–2884PubMedGoogle Scholar
  59. 59.
    Castellino AM, Parker GJ, Boronenkov IV, Anderson RA, Chao MV (1997) A novel interaction between the juxtamembrane region of the p55 tumor necrosis factor receptor and phosphatidylinositol-4-phosphate 5-kinase. J Biol Chem 272:5861–5870PubMedGoogle Scholar
  60. 60.
    Itoh T, Ijuin T, Takenawa T (1998) A novel phosphatidylinositol-5-phosphate 4-kinase (phosphatidylinositol-phosphate kinase IIγ) is phosphorylated in the endoplasmic reticulum in response to mitogenic signals. J Biol Chem 273:20292–20299PubMedGoogle Scholar
  61. 61.
    Rameh LE, Tolias KF, Duckworth BC, Cantley LC (1997) A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate. Nature 390:192–196PubMedGoogle Scholar
  62. 62.
    Rao VD, Misra S, Boronenkov IV, Anderson RA, Hurley JH (1998) Structure of type IIβ phosphatidylinositol phosphate kinase: a protein kinase fold flattened for interfacial phosphorylation. Cell 94:829–839PubMedGoogle Scholar
  63. 63.
    Clarke JH, Richardson JP, Hinchliffe KA, Irvine RF (2007) Type II PtdInsP kinases: location, regulation and function. Biochem Soc Symp 74:149–159PubMedGoogle Scholar
  64. 64.
    Ciruela A, Hinchliffe KA, Divecha N, Irvine RF (2000) Nuclear targeting of the β isoform of type II phosphatidylinositol phosphate kinase (phosphatidylinositol 5-phosphate 4-kinase) by its α-helix 7. Biochem J 346:587–591PubMedGoogle Scholar
  65. 65.
    Bazenet CE, Ruano AR, Brockman JL, Anderson RA (1990) The human erythrocyte contains two forms of phosphatidylinositol-4-phosphate 5-kinase which are differentially active toward membranes. J Biol Chem 265:18012–18022PubMedGoogle Scholar
  66. 66.
    Whiteford CC, Brearley CA, Ulug ET (1997) Phosphatidylinositol 3,5-bisphosphate defines a novel PI 3-kinase pathway in resting mouse fibroblasts. Biochem J 323:597–601PubMedGoogle Scholar
  67. 67.
    Kunz J, Fuelling A, Kolbe L, Anderson RA (2002) Stereo-specific substrate recognition by phosphatidylinositol phosphate kinases is swapped by changing a single amino acid residue. J Biol Chem 277:5611–5619PubMedGoogle Scholar
  68. 68.
    Jarquin-Pardo M, Fitzpatrick A, Galiano FJ, First EA, Davis JN (2007) Phosphatidic acid regulates the affinity of the murine phosphatidylinositol 4-phosphate 5-kinase-Iβ for phosphatidylinositol-4-phosphate. J Cell Biochem 100:112–128PubMedGoogle Scholar
  69. 69.
    Szymanska E, Sobota A, Czurylo E, Kwiatkowska K (2008) Expression of PI(4,5)P2-binding proteins lowers the PI(4,5)P2 level and inhibits FcγRIIA-mediated cell spreading and phagocytosis. Eur J Immunol 38:260–272PubMedGoogle Scholar
  70. 70.
    Lemmon MA (2008) Membrane recognition by phospholipids-binding domains. Nature 9:99–111Google Scholar
  71. 71.
    Watt SA, Kular G, Fleming IN, Downes CP, Lucocq JM (2002) Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase Cδ1. Biochem J 363:657–666PubMedGoogle Scholar
  72. 72.
    Fairn GD, Ogata K, Botelho RJ, Stahl PD, Anderson RA, De Camilli P, Meyer T, Wodak S, Grinstein S (2009) An electrostatic switch displaces phosphatidylinositol phosphate kinases from the membrane during phagocytosis. J Cell Biol 187:701–714PubMedGoogle Scholar
  73. 73.
    Scott CC, Dobson W, Botelho RJ, Coady-Osberg N, Chavrier P, Knecht DA, Heath C, Stahl P, Grinstein S (2005) Phosphatidylinositol-4,5-bisphosphate hydrolysis directs actin remodeling during phagocytosis. J Cell Biol 169:139–149PubMedGoogle Scholar
  74. 74.
    Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX, Macia E, Kirchhausen T, Albanesi JP, Roth MG, Yin HL (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114:293–299Google Scholar
  75. 75.
    Levine TP, Munro S (2002) Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr Biol 12:695–704PubMedGoogle Scholar
  76. 76.
    Godi A, Di Campli A, Konstantakopoulos A, Di Tullio G, Alessi DR, Kular GS, Daniele T, Marra P, Lucocq JM, De Matteis MA (2004) FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nature Cell Biol 6:393–404PubMedGoogle Scholar
  77. 77.
    Balla A, Tuymetova G, Tsiomenko A, Varnai P, Balla T (2005) A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type-IIIα: studies with the PH domains of the oxysterol binding protein and FAPP1. Mol Biol Cell 16:1282–1295PubMedGoogle Scholar
  78. 78.
    Tran D, Gascard P, Berthon B, Fukami K, Takenawa T, Giraud F, Claret M (1993) Cellular distribution of polyphosphoinositides in rat hepatocytes. Cell Signal 5:565–581PubMedGoogle Scholar
  79. 79.
    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 19:4577–4588PubMedGoogle Scholar
  80. 80.
    Vieira OV, Verkade P, Manninen A, Simons K (2005) FAPP2 is involved in the transport of apical cargo in polarized MDCK cells. J Cell Biol 170:521–526PubMedGoogle Scholar
  81. 81.
    Wang J, Sun HQ, Macia E, Kirchhausen T, Watson H, Bonifacino JS, Yin HL (2007) PI4P promotes the recruitment of the GGA adaptor proteins to the trans-Golgi network and regulates their recognition of the ubiquitin sorting signal. Mol Biol Cell 18:2646–2655PubMedGoogle Scholar
  82. 82.
    D’Angelo G, Vicinanza M, Di Campli A, De Matteis MA (2008) The multiple roles of PtdIns(4)P—not just the precursor of PtdIns(4,5)P2. J Cell Sci 121:1955–1963PubMedGoogle Scholar
  83. 83.
    Balla A, Kim YJ, Varnai P, Szentpetery Z, Knight Z, Shokat KM, Balla T (2008) Maintenance of hormone-sensitive phosphoinositide pools in the plasma membrane requires phosphatidylinositol 4-kinase IIIα. Mol Biol Cell 19:711–721PubMedGoogle Scholar
  84. 84.
    Hammond GR, Schiavo G, Irvine RF (2009) Immunocytochemical techniques reveal multiple, distinct cellular pools of PtdIns4P and PtdIns(4,5)P2. Biochem J 422:23–35PubMedGoogle Scholar
  85. 85.
    Cockcroft S, Taylor JA, Judah JD (1985) Subcellular localisation of inositol lipid kinases in rat liver. Biochim Biophys Acta 845:163–170PubMedGoogle Scholar
  86. 86.
    Wong K, Meyers R, Cantley LC (1997) Subcellular locations of phosphatidylinositol 4-kinase isoforms. J Biol Chem 272:13236–13241PubMedGoogle Scholar
  87. 87.
    Barylko B, Gerber SH, Binns D, Grichine N, Khvotchev M, Südhof TC, Albanesi JP (2001) A novel family of phosphatidylinositol 4-kinases conserved from yeast to humans. J Biol Chem 276:7705–7708PubMedGoogle Scholar
  88. 88.
    Wei YJ, Sun HQ, Yamamoto M, Wlodarski P, Kunii K, Martinez M, Barylko B, Albanesi JP, Yin HL (2002) Type II phosphatidylinositol 4-kinase β is a cytosolic and peripheral membrane protein that is recruited to the plasma membrane and activated by Rac-GTP. J Biol Chem 277:46586–46593PubMedGoogle Scholar
  89. 89.
    Balla A, Tuymetova G, Barshishat M, Geiszt M, Balla T (2002) Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J Biol Chem 277:20041–20050PubMedGoogle Scholar
  90. 90.
    Weixel KM, Blumental-Perry A, Watkins SC, Aridor M, Weisz OA (2005) Distinct Golgi populations of phosphatidylinositol 4-phosphate regulated by phosphatidylinositol 4-kinases. J Biol Chem 280:10501–10508PubMedGoogle Scholar
  91. 91.
    Jung G, Wang J, Wlodarski P, Barylko B, Binns DD, Shu H, Yin HL, Albanesi JP (2008) Molecular determinants of activation and membrane targeting of phosphoinositol 4-kinase IIβ. Biochem J 409:501–509PubMedGoogle Scholar
  92. 92.
    Wang YJ, Li WH, Wang J, Xu K, Dong P, Luo X, Yin HL. Critical role of PIP5KIγ87 in InsP3-mediated Ca2+ signaling. J Cell Biol 167:1005–1010Google Scholar
  93. 93.
    Tolias KF, Cantley LC, Carpenter CL (1995) Rho family GTPases bind to phosphoinositide kinases. J Biol Chem 270:17656–17699PubMedGoogle Scholar
  94. 94.
    van Hennik PB, ten Klooster JP, Halstead JR, Voermans C, Anthony EC, Divecha N, Hordijk PL (2003) The C-terminal domain of Rac1 contains two motifs that control targeting and signaling specificity. J Biol Chem 278:39166–39175PubMedGoogle Scholar
  95. 95.
    Oude Weernink PA, Meletiadis K, Hommeltenberg S, Hinz M, Ishihara H, Schmidt M, Jakobs KH (2004) Activation of type I phosphatidylinositol 4-phosphate 5-kinase isoforms by the Rho GTPases, RhoA, Rac1, and Cdc42. J Biol Chem 279:7840–7849Google Scholar
  96. 96.
    Ren XD, Bokoch GM, Traynor-Kaplan A, Jenkins GH, Anderson RA, Schwartz MA (1996) Physical association of the small GTPase Rho with a 68-kDa phosphatidylinositol 4-phosphate 5-kinase in Swiss 3T3 cells. Mol Biol Cell 7:435–442PubMedGoogle Scholar
  97. 97.
    Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, Watanabe H, Kawamoto K, Nakayama K, Morris AJ, Frohman MA, Kanaho Y (1999) Phosphatidylinositol 4-phosphate 5-kinase α is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99:521–532PubMedGoogle Scholar
  98. 98.
    Chong LD, Traynor-Kaplan A, Bokoch GM, Schwartz MA (1994) The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell 79:507–513PubMedGoogle Scholar
  99. 99.
    Chatah NE, Abrams CS (2001) G-protein-coupled receptor activation induces the membrane translocation and activation of phosphatidylinositol-4-phosphate 5-kinase Iα by a Rac- and Rho-dependent pathway. J Biol Chem 276:34059–34065PubMedGoogle Scholar
  100. 100.
    Yamazaki M, Miyazaki H, Watanabe H, Sasaki T, Maehama T, Frohman MA, Kanaho Y (2002) Phosphatidylinositol 4-phosphate 5-kinase is essential for ROCK-mediated neurite remodeling. J Biol Chem 277:17226–17230PubMedGoogle Scholar
  101. 101.
    Yang SA, Carpenter CL, Abrams CS (2004) Rho and Rho-kinase mediate thrombin-induced phosphatidylinositol 4-phosphate 5-kinase trafficking in platelets. J Biol Chem 279:42331–42336PubMedGoogle Scholar
  102. 102.
    Heasman SJ, Ridley AJ (2009) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9:690–701Google Scholar
  103. 103.
    Abramovici H, Mojtabaie P, Parks RJ, Zhong XP, Koretzky GA, Topham MK, Gee SH (2009) Diacylglycerol kinase ζ regulates actin cytoskeleton reorganization through dissociation of Rac1 from RhoGDI. Mol Biol Cell 20:2049–2059PubMedGoogle Scholar
  104. 104.
    Luo B, Prescott SM, Topham MK (2004) Diacylglycerol kinase ζ regulates phosphatidylinositol 4-phosphate 5-kinase Iα by a novel mechanism. Cell Signal 16:91–897Google Scholar
  105. 105.
    Illenberger D, Walliser C, Nurnberg B, Diaz Lorente M, Gierschik P (2003) Specificity and structural requirements of phospholipase C-β stimulation by Rho GTPases versus G protein βγ dimers. J Biol Chem 278:3006–3014PubMedGoogle Scholar
  106. 106.
    Piechulek T, Rehlen T, Walliser C, Vatter P, Moepps B, Gierschik P (2005) Isozyme-specific stimulation of phospholipase C-γ2 by Rac GTPases. J Biol Chem 280:38923–38931PubMedGoogle Scholar
  107. 107.
    Bunney TD, Opaleye O, Roe SM, Vatter P, Baxendale RW, Walliser C, Everett KL, Josephs MB, Christow C, Rodrigues-Lima F, Gierschik P, Pearl LH, Katan M (2009) Structural insights into formation of an active signaling complex between Rac and phospholipase Cγ2. Mol Cell 34:223–233PubMedGoogle Scholar
  108. 108.
    Pratt SJ, Epple H, Ward M, Feng Y, Braga VM, Longmore GD (2005) The LIM protein Ajuba influences p130Cas localization and Rac1 activity during cell migration. J Cell Biol 168:813–824PubMedGoogle Scholar
  109. 109.
    Krauss M, Kinuta M, Wenk MR, De Camilli P, Takei K, Haucke V (2003) ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Iγ. J Cell Biol 162:113–124PubMedGoogle Scholar
  110. 110.
    Hiroyama M, Exton JH (2005) Localization and regulation of phospholipase D2 by ARF6. J Cell Biochem 95:149–164PubMedGoogle Scholar
  111. 111.
    Perez-Mansilla B, Ha VL, Justin N, Wilkins AJ, Carpenter CL, Thomas GM (2006) The differential regulation of phosphatidylinositol 4-phosphate 5-kinases and phospholipase D1 by ADP-ribosylation factors 1 and 6. Biochim Biophys Acta 1761:1429–1442PubMedGoogle Scholar
  112. 112.
    Divecha N, Roefs M, Halstead JR, D’Andrea S, Fernandez-Borga M, Oomen L, Saqib KM, Wakelam MJ, D’Santos C (2000) Interaction of the type Iα PIPkinase with phospholipase D: a role for the local generation of phosphatidylinositol 4,5-bisphosphate in the regulation of PLD2 activity. EMBO J 19:5440–5449PubMedGoogle Scholar
  113. 113.
    Skippen A, Jones DH, Morgan CP, Li M, Cockcroft S (2002) Mechanism of ADP ribosylation factor-stimulated phosphatidylinositol 4,5-bisphosphate synthesis in HL60 cells. J Biol Chem 277:5823–5831PubMedGoogle Scholar
  114. 114.
    Aikawa Y, Martin TF (2003) ARF6 regulates a plasma membrane pool of phosphatidylinositol(4,5)bisphosphate required for regulated exocytosis. J Cell Biol 162:647–659PubMedGoogle Scholar
  115. 115.
    Begle A, Tryoen-Toth P, de Barry J, Bader MF, Vitale N (2009) ARF6 regulates the synthesis of fusogenic lipids for calcium-regulated exocytosis in neuroendocrine cells. J Biol Chem 284:4836–4845PubMedGoogle Scholar
  116. 116.
    Santy LC, Ravichandran KS, Casanova JE (2005) The DOCK180/Elmo complex couples ARNO-mediated Arf6 activation to the downstream activation of Rac1. Curr Biol 15:1749–1754PubMedGoogle Scholar
  117. 117.
    Myers KR, Casanova JE (2008) Regulation of actin cytoskeleton dynamics by Arf-family GTPases. Trends Cell Biol 18:184–192PubMedGoogle Scholar
  118. 118.
    Gingras AR, Bate N, Goult BT, Hazelwood L, Canestrelli I, Grossmann JG, Liu H, Putz NS, Roberts GC, Volkmann N, Hanein D, Barsukov IL, Critchley DR (2008) The structure of the C-terminal actin-binding domain of talin. EMBO J 27:458–469PubMedGoogle Scholar
  119. 119.
    Gingras AR, Ziegler WH, Bobkov AA, Joyce MG, Fasci D, Himmel M, Rothemund S, Ritter A, Grossmann JG, Patel B, Bate N, Goult BT, Emsley J, Barsukov IL, Roberts GC, Liddington RC, Ginsberg MH, Critchley DR (2009) Structural determinants of integrin binding to the talin rod. J Biol Chem 284:8866–8876PubMedGoogle Scholar
  120. 120.
    Barsukov IL, Prescot A, Bate N, Patel B, Floyd DN, Bhanji N, Bagshaw CR, Letinic K, Di Paolo G, De Camilli P, Roberts GC, Critchley DR (2003) Phosphatidylinositol phosphate kinase type 1γ and β1-integrin cytoplasmic domain bind to the same region in the talin FERM domain. J Biol Chem 278:31202–31209PubMedGoogle Scholar
  121. 121.
    de Pereda JM, Wegener KL, Santelli E, Bate N, Ginsberg MH, Critchley DR, Campbell ID, Liddington RC (2005) Structural basis for phosphatidylinositol phosphate kinase type Iγ binding to talin at focal adhesions. J Biol Chem 280:8381–8386PubMedGoogle Scholar
  122. 122.
    Kong X, Wang X, Misra S, Qin J (2006) Structural basis for the phosphorylation-regulated focal adhesion targeting of type Iγ phosphatidylinositol phosphate kinase (PIPKIγ) by talin. J Mol Biol 359:47–54PubMedGoogle Scholar
  123. 123.
    Hamada K, Shimizu T, Matsui T, Tsukita S, Hakoshima T (2000) Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J 19:4449–4462PubMedGoogle Scholar
  124. 124.
    Martel V, Racaud-Sultan C, Dupe S, Marie C, Paulhe F, Galmiche A, Block MR, Albiges-Rizo C (2001) Conformation, localization, and integrin binding of talin depend on its interaction with phosphoinositides. J Biol Chem 276:21217–21227PubMedGoogle Scholar
  125. 125.
    Saltel F, Mortier E, Hytonen VP, Jacquier MC, Zimmermann P, Vogel V, Liu W, Wehrle-Haller B (2009) New PI(4,5)P2- and membrane proximal integrin-binding motifs in the talin head control β3-integrin clustering. J Cell Biol 187:715–731PubMedGoogle Scholar
  126. 126.
    Bairstow SF, Ling K, Anderson RA (2002) Phosphatidylinositol phosphate kinase type Iγdirectly associates with and regulates Shp-1 tyrosine phosphatase. J Biol Chem 280:23884–23891Google Scholar
  127. 127.
    Sun Y, Ling K, Wagoner MP, Anderson RA (2007) Type Iγ phosphatidylinositol phosphate kinase is required for EGF-stimulated directional cell migration. J Cell Biol 178:297–308PubMedGoogle Scholar
  128. 128.
    Tanentzapf G, Brown NH (2006) An interaction between integrin and the talin FERM domain mediates integrin activation but not linkage to the cytoskeleton. Nat Cell Biol 8:601–606PubMedGoogle Scholar
  129. 129.
    Cheung TY, Fairchild MJ, Zarivach R, Tanentzapf G, Van Petegem F (2009) Crystal structure of the talin integrin binding domain 2. J Mol Biol 387:787–793PubMedGoogle Scholar
  130. 130.
    Wenk MR, Pellegrini L, Klenchin VA, Di Paolo G, Chang S, Daniell L, Arioka M, Martin TF, De Camilli P (2001) PIP kinase Iγ is the major PI(4,5)P2 synthesizing enzyme at the synapse. Neuron 32:79–88PubMedGoogle Scholar
  131. 131.
    Kahlfeldt N, Vahedi-Faridi A, Koo SJ, Schäfer JG, Krainer G, Keller S, Saenger W, Krauss M, Haucke V (2010) Molecular basis for association of PIPKIγ-p90 with clathrin adaptor AP-2. J Biol Chem 285:2734–2749PubMedGoogle Scholar
  132. 132.
    Thieman JR, Mishra SK, Ling K, Doray B, Anderson RA, Traub LM (2009) Clathrin regulates the association of PIPKIγ661 with the AP-2 adaptor β2 appendage. J Biol Chem 284:13924–13939PubMedGoogle Scholar
  133. 133.
    Paleotti O, Macia E, Luton F, Klein S, Partisani M, Chardin P, Kirchhausen T, Franco M (2005) The small G-protein ARF6GTP recruits the AP-2 adaptor complex to membranes. J Biol Chem 280:21661–21666PubMedGoogle Scholar
  134. 134.
    Jung N, Haucke V (2007) Clathrin-mediated endocytosis at synapses. Traffic 81129-11136Google Scholar
  135. 135.
    Barbieri MA, Heath CM, Peters EM, Wells A, Davis JN, Stahl PD (2001) Phosphatidylinositol-4-phosphate 5-kinase-1β is essential for epidermal growth factor receptor-mediated endocytosis. J Biol Chem 276:47212–47216PubMedGoogle Scholar
  136. 136.
    Botelho RJ, Teruel M, Dierckman R, Anderson R, Wells A, York JD, Meyer T, Grinstein S (2000) Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J Cell Biol 151:1353–1368PubMedGoogle Scholar
  137. 137.
    Golebiewska U, Nyako M, Woturski W, Zaitseva I, McLaughlin S (2008) Diffusion coefficient of fluorescent phosphatidylinositol 4,5-bisphosphate in the plasma membrane of cells. Mol Biol Cell 19:1663–1669PubMedGoogle Scholar
  138. 138.
    Wagner ML, Tamm LK (2001) Reconstituted syntaxin1a/SNAP25 interacts with negatively charged lipids as measured by lateral diffusion in planar supported bilayers. Biophys J 81:266–275PubMedGoogle Scholar
  139. 139.
    Golebiewska U, Gambhir A, Hangyas-Mihalyne G, Zaitseva I, Radler J, McLaughlin S (2006) Membrane-bound basic peptides sequester multivalent (PIP2), but not monovalent (PS), acidic lipids. Biophys J 91:588–599PubMedGoogle Scholar
  140. 140.
    van Rheenen J, Jalink K (2002) Agonist-induced PIP2 hydrolysis inhibits cortical actin dynamics: regulation at a global but not at a micrometer scale. Mol Biol Cell 13:3257–3267PubMedGoogle Scholar
  141. 141.
    Haugh JM, Codazzi F, Teruel M, Meyer T (2000) Spatial sensing in fibroblasts mediated by 3’ phosphoinositides. J Cell Biol 151:1269–1280PubMedGoogle Scholar
  142. 142.
    McLaughlin S, Wang J, Gambhir A, Murray D (2002) PIP2 and proteins: interactions, organization, and information flow. Annu Rev Biophys Biomol Struct 31:151–175PubMedGoogle Scholar
  143. 143.
    Cho H, Kim YA, Yoon JY, Lee D, Kim JH, Lee SH, Ho WK (2005) Low mobility of phosphatidylinositol 4,5-bisphosphate underlies receptor specificity of Gq-mediated ion channel regulation in atrial myocytes. Proc Natl Acad Sci USA 102:15241–15246PubMedGoogle Scholar
  144. 144.
    Cho H, Kim YA, Ho WK (2006) Phosphate number and acyl chain length determine the subcellular location and lateral mobility of phosphoinositides. Mol Cells 22:97–103PubMedGoogle Scholar
  145. 145.
    Hilgemann DW (2007) Local PIP2 signals: when, where, and how? Pflugers Arch 455:55–67PubMedGoogle Scholar
  146. 146.
    Stefanova I, Horejsi V, Ansotegui IJ, Knapp W, Stockinger H (1991) GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science 254:1016–1019PubMedGoogle Scholar
  147. 147.
    Fra AM, Williamson E, Simons K, Parton RG (1994) Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J Biol Chem 269:30745–30748PubMedGoogle Scholar
  148. 148.
    Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572PubMedGoogle Scholar
  149. 149.
    Brown DA, London E (1997) Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes? Biochem Biophys Res Commun 240:1–7PubMedGoogle Scholar
  150. 150.
    Fridriksson EK, Shipkova PA, Sheets ED, Holowka D, Baird B, McLafferty FW (1999) Quantitative analysis of phospholipids in functionally important membrane domains from RBL-2H3 mast cells using tandem high-resolution mass spectrometry. Biochemistry 38:8056–8063PubMedGoogle Scholar
  151. 151.
    Brown DA, Rose JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:344–533Google Scholar
  152. 152.
    Ahmed SN, Brown DA, London E (1997) On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry 36:10944–10953PubMedGoogle Scholar
  153. 153.
    Montixi C, Langlet C, Bernard AM, Thimonier J, Dubois C, Wurbel MA, Chauvin JP, Pierres M, He HT (1998) Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J 17:5334–5348PubMedGoogle Scholar
  154. 154.
    Sheets ED, Holowka D, Baird B (1999) Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FcεRI and their association with detergent-resistant membranes. J Cell Biol 145:877–887PubMedGoogle Scholar
  155. 155.
    Hope HR, Pike LJ (1996) Phosphoinositides and phosphoinositide-utilizing enzymes in detergent-insoluble lipid domains. Mol Biol Cell 7:843–851PubMedGoogle Scholar
  156. 156.
    Pike LJ, Casey L (1996) Localization and turnover of phosphatidylinositol 4,5-bisphosphate in caveolin-enriched membrane domains. J Biol Chem 271:6453–26456Google Scholar
  157. 157.
    Pike LJ, Miller JM (1998) Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J Biol Chem 273:22298–22304PubMedGoogle Scholar
  158. 158.
    Waugh MG, Lawson D, Tan SK, Hsuan JJ (1998) Phosphatidylinositol 4-phosphate synthesis in immunoisolated caveolae-like vesicles and low buoyant density non-caveolar membranes. J Biol Chem 273:17115–17121PubMedGoogle Scholar
  159. 159.
    Liu Y, Casey L, Pike LJ (1998) Compartmentalization of phosphatidylinositol 4,5-bisphosphate in low-density membrane domains in the absence of caveolin. Biochem Biophys Res Commun 245:684–690PubMedGoogle Scholar
  160. 160.
    Hur EM, Park YS, Lee BD, Jang IH, Kim HS, Kim TD, Suh PG, Ryu SH, Kim KT (2004) Sensitization of epidermal growth factor-induced signaling by bradykinin is mediated by c-Src. Implications for a role of lipid microdomains. J Biol Chem 279:5852–5860PubMedGoogle Scholar
  161. 161.
    Bodin S, Giuriato S, Ragab J, Humbel BM, Viala C, Vieu C, Chap H, Payrastre B (2001) Production of phosphatidylinositol 3,4,5-trisphosphate and phosphatidic acid in platelet rafts: evidence for a critical role of cholesterol-enriched domains in human platelet activation. Biochemistry 40:15209–15290Google Scholar
  162. 162.
    Heerklotz H (2002) Triton promotes domain formation in lipid raft mixtures. Biophys J 83:2693–2701PubMedGoogle Scholar
  163. 163.
    Korzeniowski M, Kwiatkowska K, Sobota A (2003) Insights into the association of FcγRII and TCR with detergent-resistant membrane domains: isolation of the domains in detergent-free density gradients facilitates membrane fragment reconstitution. Biochemistry 42:5358–5367PubMedGoogle Scholar
  164. 164.
    Shogomori H, Brown DA (2003) Use of detergents to study membrane rafts: the good, the bad, and the ugly. J Biol Chem 384:1259–1263Google Scholar
  165. 165.
    Kwik J, Boyle S, Fooksman D, Margolis L, Sheetz MP, Edidin M (2003) Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci USA 100:13964–13969PubMedGoogle Scholar
  166. 166.
    Van Rheenen J, Achame EM, Janssen H, Calafat J, Jalink K (2005) PIP2 signaling in lipid domains: a critical re-evaluation. EMBO J 24:1664–1673PubMedGoogle Scholar
  167. 167.
    Yaradanakul A, Hilgemann DW (2007) Unrestricted diffusion of exogenous and endogenous PIP2 in baby hamster kidney and Chinese hamster ovary cell plasmalemma. J Membr Biol 220:53–67PubMedGoogle Scholar
  168. 168.
    Janes PW, Ley SC, Magee AI (1999) Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J Cell Biol 147:447–461PubMedGoogle Scholar
  169. 169.
    Holowka D, Sheets ED, Baird B (2000) Interactions between FcεRI and lipid raft components are regulated by the actin cytoskeleton. J Cell Sci 113:1009–1019PubMedGoogle Scholar
  170. 170.
    Wilson BS, Pfeiffer JR, Surviladze Z, Gaudet EA, Oliver JM (2001) High-resolution mapping of mast cell membranes reveals primary and secondary domains of FcεRI and LAT. J Cell Biol 154:645–658PubMedGoogle Scholar
  171. 171.
    Kwiatkowska K, Frey J, Sobota A (2003) Phosphorylation of FcγRIIA is required for the receptor-induced actin rearrangement and capping: the role of membrane rafts. J Cell Sci 116:537–550PubMedGoogle Scholar
  172. 172.
    Saito K, Tolias KF, Saci A, Koon HB, Humphries LA, Scharenberg A, Rawlings DJ, Kinet JP, Carpenter CL (2003) BTK regulates PtdIns-4,5-P2 synthesis: importance for calcium signaling and PI3K activity. Immunity 19:669–678PubMedGoogle Scholar
  173. 173.
    Foster LJ, De Hoog CL, Mann M (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 100:5813–5818PubMedGoogle Scholar
  174. 174.
    Parmryd I, Adler J, Patel R, Magee AI (2003) Imaging metabolism of phosphatidylinositol 4,5-bisphosphate in T-cell GM1-enriched domains containing Ras proteins. Exp Cell Res 285:27–38PubMedGoogle Scholar
  175. 175.
    Strzelecka-Kiliszek A, Korzeniowski M, Kwiatkowska K, Mrozinska K, Sobota A (2004) Activated FcγRII and signalling molecules revealed in rafts by ultra-structural observations of plasma-membrane sheets. Mol Membr Biol 21:101–108PubMedGoogle Scholar
  176. 176.
    Korzeniowski M, Shakor AB, Makowska A, Drzewiecka A, Bielawska A, Kwiatkowska K, Sobota A (2007) FcγRII activation induces cell surface ceramide production which participates in the assembly of the receptor signaling complex. Cell Physiol Biochem 20:347–356PubMedGoogle Scholar
  177. 177.
    Raucher D, Stauffer T, Chen W, Shen K, Guo S, York JD, Sheetz MP, Meyer T (2000) Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100:221–228PubMedGoogle Scholar
  178. 178.
    Hagelberg C, Allan D (1990) Restricted diffusion of integral membrane proteins and polyphosphoinositides leads to their depletion in microvesicles released from human erythrocytes. Biochem J 271:831–834PubMedGoogle Scholar
  179. 179.
    Gambhir A, Hangyas-Mihalyne G, Zaitseva I, Cafiso DS, Wang J, Murray D, Pentyala SN, Smith SO, McLaughlin S (2004) Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys J 86:2188–2207PubMedGoogle Scholar
  180. 180.
    McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 43:605–611Google Scholar
  181. 181.
    Tong J, Nguyen L, Vidal A, Simon SA, Skene JH, McIntosh TJ (2008) Role of GAP-43 in sequestering phosphatidylinositol 4,5-bisphosphate to raft bilayers. Biophys J 94:125–133PubMedGoogle Scholar
  182. 182.
    Laux T, Fukami K, Thelen M, Golub T, Frey D, Caroni P (2000) GAP43, MARCKS, and CAP23 modulate PI(4,5)P2 at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 149:455–1471Google Scholar
  183. 183.
    Golub T, Caroni P (2005) PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J Cell Biol 169:151–165PubMedGoogle Scholar

Copyright information

© Springer Basel AG 2010

Authors and Affiliations

  1. 1.Laboratory of Plasma Membrane ReceptorsNencki Institute of Experimental BiologyWarsawPoland

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