Advertisement

The Journal of Membrane Biology

, Volume 194, Issue 2, pp 77–89 | Cite as

Phosphatidylinositol Phosphate Kinases Put PI4,5P2 in Its Place

  • R. L. Doughman
  • A. J. Firestone
  • R. A. AndersonEmail author
Article

Abstract

Phosphatidylinositol 4,5 bisphosphate (PI4,5P2) is a critical second messenger that regulates a myriad of diverse cellular activities including modulation of the actin cytoskeleton, vesicle trafficking, focal adhesion formation, and nuclear events. In order to effectively regulate these disparate cellular events, synthesis of PI4,5P2 by phosphatidylinositol phosphate kinases (PIP kinases) must be both spatially and temporally regulated. Two subfamilies of PIP kinases, types I and II, allow the generation of PI4,5P2 from independent pools of substrate, PI(4)P and PI(5)P respectively. In turn, type I and II PIP kinases show different subcellular localization and thus are involved in distinct signaling pathways. Additionally, several type I isoforms, and their splice variants, have now been shown to be differentially localized throughout the cell and to be involved in the synthesis of PI4,5P2 at distinct sites. These findings implicate PIP kinases as the major regulators of PI4,5P2-mediated events, making them key signaling enzymes in a variety of processes. Understanding the mechanisms regulating spatial and temporal synthesis of PI4,5P2 by PIP kinases is vital for understanding these processes as a whole. This review examines both structural and regulatory features that modulate activity, localization, and substrate usage of PIPKs.

Keywords

Phosphatidylinositol bisphosphate Phosphatidylinositol phosphate kinases Substrate specificity Rac Rho Arf 

References

  1. 1.
    Anderson, R.A., Boronenkov, I.V., Doughman, S.D., Kunz, J., Loijens, J.C. 1999Phosphatidylinositol phosphate kinases, a multifaceted family of signaling enzymes.J. Biol. Chem.27499079910CrossRefPubMedGoogle Scholar
  2. 2.
    Arneson, L.S., Kunz, J., Anderson, R.A., Traub, L.M. 1999Coupled inositide phosphorylation and phospholipase D activation initiates clathrin-coat assembly on lysosomes.J. Biol. Chem.2741779417805CrossRefPubMedGoogle Scholar
  3. 3.
    Auger, K.R., Serunian, L.A., Soltoff, S.P., Libby, P., Cantiey, L.C. 1989PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells.Cell57167175Google Scholar
  4. 4.
    Ayscough, K.R. 1998In vivo functions of actin-binding proteins.Curr. Opin. Cell Biol.10102111CrossRefPubMedGoogle Scholar
  5. 5.
    Balla, T., Bondeva, T., Varnai, P. 2000How accurately can we image inositol lipid in living cells?Trends Pharm. Sci.21238241CrossRefPubMedGoogle Scholar
  6. 6.
    Barbieri, M.A., Heath, CM., Peters, E.M., Wells, A., Davis, J.N., Stahl, P.D. 2001Phosphatidylinositol-4-phosphate 5-kinase-1beta is essential for epidermal growth factor receptor-mediated endocytosis.J. Biol. Chem.2764721247216CrossRefPubMedGoogle Scholar
  7. 7.
    Boronenkov, I.V., Loijens, J.C., Umeda, M., Anderson, R.A. 1998Phosphoinositide signaling pathways in nuclei are associated with nuclear speckles containing pre-mRNA processing factors.Mol. Biol. Cell.935473560PubMedGoogle Scholar
  8. 8.
    Brown, F.D., Rozelle, A.L., Yin, H.L., Balla, T., Donaldson, J.G. 2001Phosphatidylinositol 4,5 bisphosphate and Arf6-regulated membrane traffic.J. Cell. Biol.15410071017CrossRefPubMedGoogle Scholar
  9. 9.
    Botelho, R.J., Teruel, M., Dierckman, R., Anderson, R., Wells, A., York, J.D., Meyer, T., Grinstein, S. 2000Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis.J. Cell. Biol.15113531368CrossRefPubMedGoogle Scholar
  10. 10.
    Castellino, A.M., Parker, G.J., Boronenkov, I.V., Anderson, R.A., Chao, M.V. 1997A novel interaction between the juxtamembrane region of the p55 tumor necrosis factor receptor and phosphatidylinositol-4-phosphate 5-kinase.J. Biol. Chem.2725861587CrossRefPubMedGoogle Scholar
  11. 11.
    Chatah, N.E., Abrams, C.S. 2001G-protein-coupled receptor activation induces the membrane translocation and activation of phosphatidylinositol-4-phosphate 5-kinase I alpha by a Rac- and Rho-dependent pathway.J. Biol. Chem.2763405934065CrossRefPubMedGoogle Scholar
  12. 12.
    Chong, L.D., Traynor-Kaplan, A., Bokoch, G.M., Schwartz, M.A. 1994The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells.Cell79507513PubMedGoogle Scholar
  13. 13.
    Cockcroft, S., De Matteis, M.A. 2001Inositol lipids as spatial regulators of membrane traffic.J. Membrane Biol.180187194CrossRefGoogle Scholar
  14. 14.
    Coppolino, M.G., Dierckman, R., Loijens, J., Collins, R.F., Pouladi, M., Jongstra-Bilen, J., Schreiber, A.D., Trimble, W.S., Anderson, R., Grinstein, S. 2002Inhibition of phosphatidylinositol-4-phosphate 5-kinase Ia impairs localized actin remodelling and suppresses phagocytosis.J. Biol. Chem.2774384943857CrossRefPubMedGoogle Scholar
  15. 15.
    Czech, M.P. 2000PI4,5P2 and PI4,5P3: complex roles at the cell surface.Cell100603606PubMedGoogle Scholar
  16. 16.
    Davis, J.N., Rock, C.O., Cheng, M., Watson, J.B., Ashmun, R.A., Kirk, H., Kay, R.J., Roussel, M.F. 1997Complementation of growth factor receptor-dependent mitogenic signaling by a truncated type I phosphatidylinositol-4-phosphate 5-kinase.Mol. Cell Biol.1773987406PubMedGoogle Scholar
  17. 17.
    Desrivieres, S., Cooke, F.T., Parker, P.J., Hall, M.N. 1998MSS4, a phosphatidylinositol-4-phosphate 5-kinase required for organization of the actin cytoskeleton in Saccharomyces cerevisiae. J. Biol. Chem.2731578715793CrossRefPubMedGoogle Scholar
  18. 18.
    DeWald, D. 2002Phosphoinositide signaling: vac to the future in fabl kinase regulation.Curr. Biol.12R491R492CrossRefPubMedGoogle Scholar
  19. 19.
    Di Paolo, G., Pellegrini, L., Letinic, K., Cestra, G., Zoncu, R., Voronov, S., Chang, S., Guo, J., Wenk, M.R., De Camilli, P. 2002Recruitment and regulation of phosphatidylinositol phosphate kinase type 1gamma by the FERM domain of talin.Nature4208589CrossRefPubMedGoogle Scholar
  20. 20.
    Gary, J.D., Wurmser, A.E., Bonangelino, C.J., Weisman, L.S., Emr, S.D. 1998Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vascuolar size and membrane homeostasis.J. Cell Biol.1436579CrossRefPubMedGoogle Scholar
  21. 21.
    Gilmore, A.P., Burridge, K. 1996Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate.Nature381531535CrossRefPubMedGoogle Scholar
  22. 22.
    Godi, A., Pertile, P., Meyers, R., Marra, P., Di Tullio, G., Iurisci, C., Luini, A., Corda, D., De Matteis, M.A. 1999ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex.Nat. Cell Biol.1280287CrossRefPubMedGoogle Scholar
  23. 23.
    Halstead, J.R., Roefs, M., Ellson, C.D., D'Andrea, S., Chen, C., D'Santos, C.S., Divecha, N. 2001A novel pathway of cellular phosphatidylinositol(3,4,5)-trisphosphate synthesis is regulated by oxidative stress.Curr. Biol.11386395CrossRefPubMedGoogle Scholar
  24. 24.
    Hartwig, J.H., Kwiatkowski, D.J. 1991Actin-binding proteins.Curr. Opin. Cell Biol.38797PubMedGoogle Scholar
  25. 25.
    Hay, J.C., Fisette, P.L., Jenkins, G.H., Fukami, K., Takenawa, T., Anderson, R.A., Martin, T.F. 1995ATP-dependent inositide phosphorylation required for Ca2+-activated secretion.Nature374173177CrossRefPubMedGoogle Scholar
  26. 26.
    Higgs, H.N., Pollard, T.D. 2000Activation by Cdc42 and PI4,5P(2) of Wiskott Aldrich syndrome protein (WASp) stimulates actin nucleation by Arp2/3 complex.J. Cell Biol.15013111320CrossRefPubMedGoogle Scholar
  27. 27.
    Homma, K., Terui, S., Minemura, M., Qadota, H., Anraku, Y., Kanaho, Y., Ohya, Y. 1998Phosphatidylinositol-4-phosphate 5-kinase localized on the plasma membrane is essential for yeast cell morphogenesis.J. Biol. Chem.2731577915786CrossRefPubMedGoogle Scholar
  28. 28.
    Honda, A., Nogami, M., Yokozeki, T., Yamazaki, M., Nakamura, H., Watanabe, H., Kawamoto, K., Nakayama, K., Morris, A.J., Frohman, M.A., Kanaho, Y. 1999Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation.Cell99521532PubMedGoogle Scholar
  29. 29.
    Ikonomov, O.C., Sbrissa, D., Mlak, K., Kanzaki, M., Pessin, J., Shisheva, A. 2002Functional dissection of lipid and protein kinase signals of PIKfyve reveals the role of PtdIns 3,5-P2 production for endomembrane integrity.J. Biol. Chem.27792069211CrossRefPubMedGoogle Scholar
  30. 30.
    Ishihara, H., Shibasaki, Y., Kizuki, N., Katagiri, H., Yazaki, Y., Asano, T., Oka, Y. 1996Cloning of cDNAs encoding two isoforms of 68-kDa type I phosphatidylinositol-4-phosphate 5-kinase.J. Biol. Chem.2712361123614CrossRefPubMedGoogle Scholar
  31. 31.
    Ishihara, H., Shibasaki, Y., Kizuki, N., Wada, T., Yazaki, Y., Asano, T., Oka, Y. 1998Type 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.27387418748CrossRefPubMedGoogle Scholar
  32. 32.
    Itoh, T., Ijuin, T., Takenawa, T. 1998A novel phosphatidylinositol-5-phosphate 4-kinase (phosphatidylinositol-phosphate kinase IIgamma) is phosphorylated in the endoplasmic reticulum in response to mitogenic signals.J. Biol. Chem.2732029220299CrossRefPubMedGoogle Scholar
  33. 33.
    Itoh, T., Ishihara, H., Shibasaki, Y., Oka, Y., Takenawa, T. 2000Autophosphorylation of type I phosphatidylinositol phosphate kinase regulates its lipid kinase activity.J. Biol. Chem.2751938919394CrossRefPubMedGoogle Scholar
  34. 34.
    Jenkins, G.H., Fisette, P.L., Anderson, R.A. 1994Type I phosphatidylinositol 4-phosphate 5-kinase isoforms are specifically stimulated by phosphatidic acid.J. Biol. Chem.2691154711554PubMedGoogle Scholar
  35. 35.
    Johnson, R.P., Craig, S.W. 2000Actin activates a cryptic dimerization potential of the vinculin tail domain.J. Biol. Chem.27595105CrossRefPubMedGoogle Scholar
  36. 36.
    Jones, D.R., Sanjuan, M.A., Merida, I. 2000Type Ialpha phosphatidylinositol 4-phosphate 5-kinase is a putative target for increased intracellular phosphatidic acid.FEBS Lett.476160165CrossRefPubMedGoogle Scholar
  37. 37.
    Kunz, J., Fuelling, A., Kolbe, L., Anderson, R.A. 2002Stereo-specific substrate recognition by phosphatidylinositol phosphate kinases is swapped by changing a single amino acid residue.J. Biol. Chem.27756115619CrossRefPubMedGoogle Scholar
  38. 38.
    Kunz, J., Wilson, M.P., Kisseleva, M., Hurley, J.H., Majerus, P.W., Anderson, R.A. 2000The activation loop of phosphatidylinositol phosphate kinases determines signaling specificity.Mol. Cell5111PubMedGoogle Scholar
  39. 39.
    Lauffenburger, D.A., Horwitz, A.F. 1996Cell migration: a physically integrated molecular process.Cell84359369PubMedGoogle Scholar
  40. 40.
    Lee, E., De Camilli, P. 2002Dynamin at actin tails.Proc. Natl. Acad. Sci. U SA99161166CrossRefGoogle Scholar
  41. 41.
    Ling, K., Doughman, R.L., Firestone, A.J., Bunce, M.W., Anderson, R.A. 2002Type Igamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions.Nature4208993CrossRefPubMedGoogle Scholar
  42. 42.
    Loijens, J.C., Anderson, R.A. 1996Type I phosphatidylinositol-4-phosphate 5-kinases are distinct members of this novel lipid kinase family.J. Biol. Chem.2713293732943CrossRefPubMedGoogle Scholar
  43. 43.
    Maekawa, M., Eshizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K., Narumiya, S. 1999Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase.Science285895898Google Scholar
  44. 44.
    Martin, T.F. 2001PI(4,5)P(2) regulation of surface membrane traffic.Curr. Opin. Cell Biol.13493499CrossRefPubMedGoogle Scholar
  45. 45.
    Matsui, T., Yonemura, S., Tsukita, S. 1999Activation of ERM proteins in vivo by Rho involves phosphatidyl-inositol 4-phosphate 5-kinase and not ROCK kinases.Curr. Biol.912591262CrossRefPubMedGoogle Scholar
  46. 46.
    McEwen, R.K., Dove, S.K., Cooke, F.T., Painter, G.F., Holmes, A.B., Shisheva, A., Ohya, Y., Parker, P.J., Michell, R.H. 1999Complementation analysis in PtdInsP kinase-deficient yeast mutants demonstrates that Schizosaccharomyces pombe and murine Fab1p homologues are phosphatidylinositol 3-phosphate 5-kinases.J. Biol. Chem.274390533912Google Scholar
  47. 47.
    McLaughlin, S., Wang, J., Gambhir, A., Murray, D. 2002PI4,5P(2) and proteins: interactions, organization, and information flow.Annu. Rev. Biophys. Biomol. Struct.31151175CrossRefPubMedGoogle Scholar
  48. 48.
    Miyazawa, A., Umeda, M., Torikoshi, T., Yanagisawa, K., Yoshioka, T., Inoue, K. 1988Production and characterization of monoclonal antibodies that bind to phosphatidylinositol 4,5 bisphosphate.Mol. Immunol.2510251031CrossRefPubMedGoogle Scholar
  49. 49.
    Nobes, C.D., Hall, A. 1995Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia.Cell815362PubMedGoogle Scholar
  50. 50.
    Orth, J.D., Krueger, E.W., Cao, H., McNiven, M.A. 2002The large GTPase dynamin regulates actin comet formation and movement in living cells.Proc. Natl. Acad. Sci. US A99167172CrossRefGoogle Scholar
  51. 51.
    Oude Weernink, P.A., Schulte, P., Guo, Y., Wetzel, J., Amano, M., Kaibuchi, K., Haverland, S., Voss, M., Schmidt, M., Mayr, G.W., Jakobs, K.H. 2000Stimulation of phosphatidylinositol-4-phosphate 5-kinase by Rho-kinase.J. Biol. Chem.2751016810174CrossRefPubMedGoogle Scholar
  52. 52.
    Park, S.J., Itoh, T., Takenawa, T. 2001Phosphatidylinositol phosphate 5-kinase type I is regulated through phosphorylation response by extracellular stimuli.J. Biol. Chem.27647814787CrossRefPubMedGoogle Scholar
  53. 53.
    Rameh, L.E., Tolias, K.F., Duckworth, B.C., Cantley, L.C. 1997A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate.Nature390192196CrossRefPubMedGoogle Scholar
  54. 54.
    Randazzo, P.A., Nie, Z., Miura, K., Hsu, V.W. 2000Molecular aspects of the cellular activities of ADP-ribosylation factors.Sci STKE2000RE1Google Scholar
  55. 55.
    Rao, V.D., Misra, S., Boronenkov, I.V., Anderson, R.A., Hurley, J.H. 1998Structure of type IIbeta phosphatidylinositol phosphate kinase: a protein kinase fold flattened for interfacial phosphorylation.Cell94829839PubMedGoogle Scholar
  56. 56.
    Ren, X.D., Bokoch, G.M., Traynor-Kaplan, A., Jenkins, G.H., Anderson, R.A., Schwartz, M.A. 1996Physical association of the small GTPase Rho with a 68-kDa phosphatidylinositol 4-phosphate 5-kinase in Swiss 3T3 cells.Mol. Biol. Cell7435442PubMedGoogle Scholar
  57. 57.
    Rohatgi, R., Ho, H.Y., Kirschner, M.W. 2000Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate.J. Cell Biol.15012991310CrossRefPubMedGoogle Scholar
  58. 58.
    Rozelle, A.L., Machesky, L.M., Yamamoto, M., Driessens, M.H., Insall, R.H., Roth, M.G., Luby-Phelps, K., Marriott, G., Hall, A., Yin, H.L. 2000Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3.Curr. Biol.10311320CrossRefPubMedGoogle Scholar
  59. 59.
    Sbrissa, D., Ikonomov, O.C., Shisheva, A. 1999PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5-phosphoinositides. Effect of insulin.J. Biol. Chem.2742158921597CrossRefPubMedGoogle Scholar
  60. 60.
    Sbrissa, D., Ikonomov, O.C., Shisheva, A. 2002Phosphatidylinositol 3-phosphate-interacting domains in PIKfyve. Binding specificity and role in PIKfyve. Endomembrane localization.J. Biol. Chem.27760736079CrossRefPubMedGoogle Scholar
  61. 61.
    Sechi, A.S., Wehland, J. 2000The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P(2) influences cytoskeletal protein activity at the plasma membrane.J. Cell Sci.11336853695PubMedGoogle Scholar
  62. 62.
    Shibasaki, Y., Ishihara, H., Kizuki, N., Asano, T., Oka, Y., Yazaki, Y. 1997Massive actin polymerization induced by phosphatidylinositol-4-phosphate 5-kinase in vivo.J. Biol. Chem.21275787581Google Scholar
  63. 63.
    Shyng, S.L., Barbieri, A., Gumusboga, A., Cukras, C., Pike, L., Davis, J.N., Stahl, P.D., Nichols, C.G. 2000Modulation of nucleotide sensitivity of ATP-sensitive potassium channels by phosphatidylinositol-4-phosphate 5-kinase.Proc. Natl. Acad. Sci. USA97937941CrossRefPubMedGoogle Scholar
  64. 64.
    Skippen, A., Jones, D.H., Morgan, C.P., Li, M., Cockcroft, S. 2002Mechanism of ADP ribosylation factor-stimulated phosphatidylinositol 4,5-bisphosphate synthesis in HL60 cells.J. Biol. Chem.27758235831CrossRefPubMedGoogle Scholar
  65. 65.
    Small, J.V., Stradal, T., Vignal, E., Rottner, K. 2002The lamellipodium: where motility begins.Trends Cell Biol.12112120CrossRefPubMedGoogle Scholar
  66. 66.
    Stripp, C.S., Kolesnikova, T.V., Hemler, M.E. 2003Functional domains in tetraspanin proteins.Trends Biochem. Sci.28106112CrossRefPubMedGoogle Scholar
  67. 67.
    Toker, A. 1998The synthesis and cellular roles of phosphatidylinositol 4,5-bisphosphate.Curr. Opin. Cell Biol.10254261CrossRefPubMedGoogle Scholar
  68. 68.
    Tolias, K.F., Cantley, L.C., Carpenter, C.L. 1995Rho family GTPases bind to phosphoinositide kinases.J. Biol. Chem.2701765617659CrossRefPubMedGoogle Scholar
  69. 69.
    Tolias, K.F., Couvillon, A.D., Cantley, L.C., Carpenter, C.L. 1998Characterization of a Rac1- and RhoGDI-associated lipid kinase signaling complex.Mol. Cell Biol.18762770PubMedGoogle Scholar
  70. 70.
    Tolias, K.F., Rameh, L.E., Ishihara, H., Shibasaki, Y., Chen, J., Prestwich, G.D., Cantley, L.C., Carpenter, C.L. 1998Type I phosphatidylinositol-4-phosphate 5-kinases synthesize the novel lipids phosphatidylinositol 3,5-bisphosphate and phosphatidylinositol 5-phosphate.J. Biol. Chem.2731804018046CrossRefPubMedGoogle Scholar
  71. 71.
    Tolias, K.F., Hartwig, J.H., Ishihara, H., Shibasaki, Y., Cantley, L.C., Carpenter, C.L. 2000Type Ialpha phosphatidylinositol-4-phosphate 5-kinase mediates Rac-dependent actin assembly.Curr. Biol.10153156CrossRefPubMedGoogle Scholar
  72. 72.
    Vancurova, I., Choi, J.H., Lin, H., Kuret, J., Vancura, A. 1999Regulation of phosphatidylinositol 4-phosphate 5-kinase from Schizosaccharomyces pombe by casein kinase I.J. Biol. Chem.27411471155CrossRefPubMedGoogle Scholar
  73. 73.
    van Horck, P.P., Lavazais, E., Eickholt, B.J., Moolenaar, W.H., Divecha, N. 2002Essential role of Type I(alpha) phosphatidylinositol 4-phosphate 5-kinase in neurite remodeling.Curr. Biol.12241245CrossRefPubMedGoogle Scholar
  74. 74.
    Van Rheenen, J., Jalink, K. 2002Agonist-induced PI4,5P(2) hydrolysis inhibits cortical actin dynamics: Regulation at a global but not at a micrometer scale.Mol. Biol. Cell1332573267CrossRefPubMedGoogle Scholar
  75. 75.
    Watt, S.A., Kular, G., Fleming, I.N., Downes, C.P., Lucocq, J.M. 2002Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta 1.Biochem. J.363651666CrossRefGoogle Scholar
  76. 76.
    Weernink, P.A., Guo, Y., Zhang, C., Schmidt, M., Von Eichel-Streiber, C., Jakobs, K.H. 2000Control of cellular phosphatidylinositol 4,5-bisphosphate levels by adhesion signals and rho GTPases in NIH 3T3 fibroblasts involvement of both phosphatidylinositol-4-phosphate 5-kinase and phospholipase C.Eur. J. Biochem.26752375246CrossRefPubMedGoogle Scholar
  77. 77.
    Wenk, M.R., Pellegrini, L., Klenchin, V.A., Di Paolo, G., Chang, S., Daniell, L., Arioka, M., Martin, T.F., De Camilli, P. 2001PI4,5P kinase Igamma is the major PI(4,5)P(2) synthesizing enzyme at the synapse.Neuron327988PubMedGoogle Scholar
  78. 78.
    Yamamoto, A., DeWald, D.B., Boronenkov, I.V., Anderson, R.A., Emr, S.D., Koshland, D. 1995Novel PI(4)P 5-kinase homologue, Fab1p, essential for normal vacuole function and morphology in yeast.Mol. J. Biol. Cell6525539Google Scholar
  79. 79.
    Yamanoto, M., Hilgemann, D.H., Feng, S., Bito, H., Ishihara, H., Shibasaki, Y., Yin, H.L. 2001Phosphatidylinositol 4,5-bisphosphate induces actin stress-fiber formation and inhibits membrane ruffling in CV1 cells.Cell Biol.152867876CrossRefGoogle Scholar
  80. 80.
    Yamazaki, M., Miyazaki, H., Watanabe, H., Sasaki, T., Maehama, T., Frohman, M.A., Kanaho, Y. 2002A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export.J. Biol. Chem.2771722617230CrossRefPubMedGoogle Scholar
  81. 81.
    York, J.D., Odom, A.R., Murphy, R., Ives, E.B., Wente, S.R. 1999A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export.Science28596100CrossRefPubMedGoogle Scholar
  82. 82.
    Zhang, X., Loijens, J.C., Boronenkov, I.V., Parker, G.J., Norris, F.A., Chen, J., Thum, O., Prestwich, G.D., Majerus, P.W., Anderson, R.A. 1997Phosphatidylinositol-4-phosphate 5-kinase isozymes catalyze the synthesis of 3-phosphate-containing phosphatidylinositol signaling molecules.J. Biol. Chem.2721775617761CrossRefPubMedGoogle Scholar
  83. 83.
    Doughman, R.L., Firestone, A.J., Wojtasiak, M.L., Bunce, M.W., Anderson, R.A. 2003Membrane ruffling requires coordination between type I phosphatidylinositol phosphate kinase and Rac signaling.J. Biol. Chem.278M211397200CrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 2003

Authors and Affiliations

  • R. L. Doughman
    • 1
  • A. J. Firestone
    • 1
  • R. A. Anderson
    • 1
    Email author
  1. 1.Molecular and Cellular Pharmacology Program, Department of PharmacologyUniversity of Wisconsin-Madison, 1300 University Ave., Madison, WI 53706USA

Personalised recommendations