Skip to main content
SpringerLink
Log in

Phosphoinositides as Determinants of Membrane Identity, Apicobasal Polarity, and Lumen Formation

  • Chapter
  • First Online:
Cell Polarity 1

  • 1458 Accesses

Abstract

Epithelial cells sense their surrounding environment via mechanical and chemical stimuli, responding to multiple sources of tension and force, including those generated by cell–cell and cell–extracellular matrix (ECM) interaction: they respond to these cues by developing an apicobasal axis of polarity. Phosphoinositides (PIs) are structural components of biological membranes that control a diverse array of signaling pathways through spatiotemporal recruitment of effectors containing PI-specific binding domain(s). Thus they have been shown to modulate a plethora of cellular processes including actin polymerization, cell migration, proliferation, differentiation, and vesicular trafficking. PIs are enriched in different membranes and their levels are tightly regulated by specific PI kinases and phosphatases. During the past decade, PIs have come to the fore as specific markers that define membrane identity, acting as critical regulators of the cell polarization process. In this review, we have examined how PIs are able to assign identity to polarized epithelial cell plasma membrane domains and integrate in space and time complex signaling pathways to trigger appropriate cellular responses to environmental cues. PIs are implicated in a vast array of cellular responses that are central for morphogenesis such as, but not limited to, cytoskeletal changes, cytokinesis, and recruitment of downstream effectors to govern mechanisms involved in polarization and lumen formation. Subversion by pathogens of PI metabolism and plasma membrane identity in polarized cells and the clinical relevance of research on PIs were also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Adler CE, Fetter RD, Bargmann CI (2006) UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat Neurosci 9(4):511–518

    PubMed Central  CAS  PubMed  Google Scholar 

  • Altan-Bonnet N, Balla T (2012) Phosphatidylinositol 4-kinases: hostages harnessed to build panviral replication platforms. Trends Biochem Sci 37(7):293–302

    PubMed Central  CAS  PubMed  Google Scholar 

  • Alvisi G, Madan V, Bartenschlager R (2011) Hepatitis C virus and host cell lipids: an intimate connection. RNA Biol 8(2):258–269

    CAS  PubMed  Google Scholar 

  • Awad A, Sar S, Barré R, Cariven C, Marin M, Salles JP et al (2013) SHIP2 regulates epithelial cell polarity through its lipid product, which binds to Dlg1, a pathway subverted by hepatitis C virus core protein. Mol Biol Cell 24(14):2171–2185

    PubMed Central  CAS  PubMed  Google Scholar 

  • Backers K, Blero D, Paternotte N, Zhang J, Erneux C (2003) The termination of PI3K signalling by SHIP1 and SHIP2 inositol 5-phosphatases. Adv Enzyme Regul 43:15–28

    CAS  PubMed  Google Scholar 

  • Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93(3):1019–1137

    PubMed Central  CAS  PubMed  Google Scholar 

  • Balla T, Várnai P (2009) Visualization of cellular phosphoinositide pools with GFP-fused protein-domains. Curr Protoc Cell Biol. Chapter 24:Unit 24.4

    Google Scholar 

  • Banham-Hall E, Clatworthy MR, Okkenhaug K (2012) The therapeutic potential for PI3K inhibitors in autoimmune rheumatic diseases. Open Rheumatol J 6:245–258

    PubMed Central  CAS  PubMed  Google Scholar 

  • Behnia R, Munro S (2005) Organelle identity and the signposts for membrane traffic. Nature 438(7068):597–604

    CAS  PubMed  Google Scholar 

  • Benedicto I, Molina-Jiménez F, Moreno-Otero R, López-Cabrera M, Majano PL (2011) Interplay among cellular polarization, lipoprotein metabolism and hepatitis C virus entry. World J Gastroenterol 17(22):2683–2690

    PubMed Central  PubMed  Google Scholar 

  • Berger KL, Cooper JD, Heaton NS, Yoon R, Oakland TE, Jordan TX et al (2009) Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication. Proc Natl Acad Sci U S A 106(18):7577–7582

    PubMed Central  CAS  PubMed  Google Scholar 

  • Berger KL, Kelly SM, Jordan TX, Tartell MA, Randall G (2011) Hepatitis C virus stimulates the phosphatidylinositol 4-kinase III alpha-dependent phosphatidylinositol 4-phosphate production that is essential for its replication. J Virol 85(17):8870–8883

    PubMed Central  CAS  PubMed  Google Scholar 

  • Berridge MJ, Irvine RF (1989) Inositol phosphates and cell signalling. Nature 341(6239):197–205

    CAS  PubMed  Google Scholar 

  • Bianco A, Reghellin V, Donnici L, Fenu S, Alvarez R, Baruffa C et al (2012) Metabolism of phosphatidylinositol 4-kinase IIIα-dependent PI4P Is subverted by HCV and is targeted by a 4-anilino quinazoline with antiviral activity. PLoS Pathog 8(3):e1002576

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bilder D, Li M, Perrimon N (2000) Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289(5476):113–116

    CAS  PubMed  Google Scholar 

  • Bishé B, Syed G, Siddiqui A (2012) Phosphoinositides in the hepatitis C virus life cycle. Viruses 4(10):2340–2358

    PubMed Central  PubMed  Google Scholar 

  • Bomsel M, Alfsen A (2003) Entry of viruses through the epithelial barrier: pathogenic trickery. Nat Rev Mol Cell Biol 4(1):57–68

    CAS  PubMed  Google Scholar 

  • Borawski J, Troke P, Puyang X, Gibaja V, Zhao S, Mickanin C et al (2009) Class III phosphatidylinositol 4-kinase alpha and beta are novel host factor regulators of hepatitis C virus replication. J Virol 83(19):10058–10074

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brass V, Gosert R, Moradpour D (2009) Investigation of the hepatitis C virus replication complex. Methods Mol Biol 510:195–209

    CAS  PubMed  Google Scholar 

  • Bruns JR, Ellis MA, Jeromin A, Weisz OA (2002) Multiple roles for phosphatidylinositol 4-kinase in biosynthetic transport in polarized Madin-Darby canine kidney cells. J Biol Chem 277(3):2012–2018

    CAS  PubMed  Google Scholar 

  • Bryant DM, Mostov KE (2008) From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 9(11):887–901

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bryant DM, Datta A, Rodríguez-Fraticelli AE, Peränen J, Martín-Belmonte F, Mostov KE (2010) A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 12(11):1035–1045. doi:10.1038/ncb2106, PMID: 20890297

    PubMed Central  CAS  PubMed  Google Scholar 

  • Burridge K, Wennerberg K (2004) Rho and Rac take center stage. Cell 116(2):167–179

    CAS  PubMed  Google Scholar 

  • Cai H, Devreotes PN (2011) Moving in the right direction: how eukaryotic cells migrate along chemical gradients. Semin Cell Dev Biol 22(8):834–841. doi:10.1016/j.semcdb.2011.07.020, PMID: 21821139

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cain RJ, Ridley AJ (2009) Phosphoinositide 3-kinases in cell migration. Biol Cell 101(1):13–29

    CAS  PubMed  Google Scholar 

  • Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296(5573):1655–1657

    CAS  PubMed  Google Scholar 

  • Cerruti B, Puliafito A, Shewan AM, Yu W, Combes AN, Little MH et al (2013) Polarity, cell division, and out-of-equilibrium dynamics control the growth of epithelial structures. J Cell Biol 203(2):359–372

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cho W, Stahelin RV (2005) Membrane-protein interactions in cell signaling and membrane trafficking. Annu Rev Biophys Biomol Struct 34:119–151

    CAS  PubMed  Google Scholar 

  • Chukkapalli V, Hogue IB, Boyko V, Hu W-S, Ono A (2008) Interaction between the human immunodeficiency virus type 1 Gag matrix domain and phosphatidylinositol-(4,5)-bisphosphate is essential for efficient gag membrane binding. J Virol 82(5):2405–2417

    PubMed Central  CAS  PubMed  Google Scholar 

  • Comer FI, Parent CA (2007) Phosphoinositides specify polarity during epithelial organ development. Cell 128(2):239–240

    CAS  PubMed  Google Scholar 

  • Cossart P, Sansonetti PJ (2004) Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304(5668):242–248

    CAS  PubMed  Google Scholar 

  • Cotter L, Ozçelik M, Jacob C, Pereira JA, Locher V, Baumann R et al (2010) Dlg1-PTEN interaction regulates myelin thickness to prevent damaging peripheral nerve overmyelination. Science 328(5984):1415–1418

    CAS  PubMed  Google Scholar 

  • Datta A, Bryant DM, Mostov KE (2011) Molecular regulation of lumen morphogenesis. Curr Biol 21(3):R126–R136. doi:10.1016/j.cub.2010.12.003, PMID: 21300279

    PubMed Central  CAS  PubMed  Google Scholar 

  • De Graaf P, Zwart WT, van Dijken RAJ, Deneka M, Schulz TKF, Geijsen N et al (2004) Phosphatidylinositol 4-kinasebeta is critical for functional association of rab11 with the Golgi complex. Mol Biol Cell 15(4):2038–2047

    PubMed Central  PubMed  Google Scholar 

  • De Matteis MA, Godi A (2004) PI-loting membrane traffic. Nat Cell Biol 6(6):487–492

    PubMed  Google Scholar 

  • Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443(7112):651–657

    PubMed  Google Scholar 

  • Dixon MJ, Gray A, Schenning M, Agacan M, Tempel W, Tong Y et al (2012) IQGAP proteins reveal an atypical phosphoinositide (aPI) binding domain with a pseudo C2 domain fold. J Biol Chem 287(27):22483–22496

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dyson JM, O’Malley CJ, Becanovic J, Munday AD, Berndt MC, Coghill ID et al (2001) The SH2-containing inositol polyphosphate 5-phosphatase, SHIP-2, binds filamin and regulates submembraneous actin. J Cell Biol 155(6):1065–1079

    PubMed Central  CAS  PubMed  Google Scholar 

  • Egger D, Wölk B, Gosert R, Bianchi L, Blum HE, Moradpour D et al (2002) Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J Virol 76(12):5974–5984, PMID: 12021330

    PubMed Central  CAS  PubMed  Google Scholar 

  • Elong Edimo W, Schurmans S, Roger PP, Erneux C (2014) SHIP2 signaling in normal and pathological situations: its impact on cell proliferation. Adv Biol Regul 54:142–51

    CAS  PubMed  Google Scholar 

  • Elsum I, Yates L, Humbert PO, Richardson HE (2012) The Scribble-Dlg-Lgl polarity module in development and cancer: from flies to man. Essays Biochem 53:141–168

    CAS  PubMed  Google Scholar 

  • Engel JN (ed) (2002) Molecular pathogenesis of acute Pseudomonas aeruginosa infections. Kluwer, New York

    Google Scholar 

  • Erneux C, Edimo WE, Deneubourg L, Pirson I (2011) SHIP2 multiple functions: a balance between a negative control of PtdIns(3,4,5)P3 level, a positive control of PtdIns(3,4)P2 production, and intrinsic docking properties. J Cell Biochem 112(9):2203–2209

    CAS  PubMed  Google Scholar 

  • Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wölk B et al (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446(7137):801–805

    CAS  PubMed  Google Scholar 

  • Flores AI, Narayanan SP, Morse EN, Shick HE, Yin X, Kidd G et al (2008) Constitutively active Akt induces enhanced myelination in the CNS. J Neurosci 28(28):7174–7183

    CAS  PubMed  Google Scholar 

  • Fukata M, Nakagawa M, Kaibuchi K (2003) Roles of Rho-family GTPases in cell polarisation and directional migration. Curr Opin Cell Biol 15(5):590–597

    CAS  PubMed  Google Scholar 

  • Gassama-Diagne A, Payrastre B (2009) Phosphoinositide signaling pathways: promising role as builders of epithelial cell polarity. Int Rev Cell Mol Biol 273:313–343

    CAS  PubMed  Google Scholar 

  • Gassama-Diagne A, Yu W, ter Beest M, Martin-Belmonte F, Kierbel A, Engel J et al (2006) Phosphatidylinositol-3,4,5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nat Cell Biol 8(9):963–970

    CAS  PubMed  Google Scholar 

  • Geiser TK, Kazmierczak BI, Garrity-Ryan LK, Matthay MA, Engel JN (2001) Pseudomonas aeruginosa ExoT inhibits in vitro lung epithelial wound repair. Cell Microbiol 3(4):223–236

    CAS  PubMed  Google Scholar 

  • Geron E, Schejter ED, Shilo B-Z (2013) Directing exocrine secretory vesicles to the apical membrane by actin cables generated by the formin mDia1. Proc Natl Acad Sci U S A 110(26):10652–10657

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gibson MC, Perrimon N (2003) Apicobasal polarization: epithelial form and function. Curr Opin Cell Biol 15(6):747–752

    CAS  PubMed  Google Scholar 

  • Goebbels S, Oltrogge JH, Kemper R, Heilmann I, Bormuth I, Wolfer S et al (2010) Elevated phosphatidylinositol 3,4,5-trisphosphate in glia triggers cell-autonomous membrane wrapping and myelination. J Neurosci 30(26):8953–8964

    CAS  PubMed  Google Scholar 

  • Goldstein B, Macara IG (2007) The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13(5):609–622

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guillot C, Lecuit T (2013) Mechanics of epithelial tissue homeostasis and morphogenesis. Science 340(6137):1185–1189

    CAS  PubMed  Google Scholar 

  • Hales CM, Vaerman J-P, Goldenring JR (2002) Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J Biol Chem 277(52):50415–50421

    CAS  PubMed  Google Scholar 

  • Hammond GRV, Fischer MJ, Anderson KE, Holdich J, Koteci A, Balla T et al (2012) PI4P and PI(4,5)P2 are essential but independent lipid determinants of membrane identity. Science 337(6095):727–730

    PubMed Central  CAS  PubMed  Google Scholar 

  • Harlan JE, Hajduk PJ, Yoon HS, Fesik SW (1994) Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 371(6493):168–170

    CAS  PubMed  Google Scholar 

  • Harris HJ, Clerte C, Farquhar MJ, Goodall M, Hu K, Rassam P et al (2013) Hepatoma polarization limits CD81 and hepatitis C virus dynamics. Cell Microbiol 15(3):430–445

    PubMed Central  CAS  PubMed  Google Scholar 

  • Heasman SJ, Ridley AJ (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9(9):690–701

    CAS  PubMed  Google Scholar 

  • Hicks AM, DeLong CJ, Thomas MJ, Samuel M, Cui Z (2006) Unique molecular signatures of glycerophospholipid species in different rat tissues analyzed by tandem mass spectrometry. Biochim Biophys Acta 1761(9):1022–1029

    CAS  PubMed  Google Scholar 

  • Houk AR, Jilkine A, Mejean CO, Boltyanskiy R, Dufresne ER, Angenent SB et al (2012) Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration. Cell 148(1–2):175–188

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hsu NY, Ilnytska O, Belov G, Santiana M, Chen YH, Takvorian PM, Pau C, van der Schaar H, Kaushik-Basu N, Balla T, Cameron CE, Ehrenfeld E, van Kuppeveld FJ, Altan-Bonnet N (2010) Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141(5):799–811. doi:10.1016/j.cell.2010.03.050, PMID: 20510927

    PubMed Central  CAS  PubMed  Google Scholar 

  • Inlora J, Chukkapalli V, Derse D, Ono A (2011) Gag localization and virus-like particle release mediated by the matrix domain of human T-lymphotropic virus type 1 Gag are less dependent on phosphatidylinositol-(4,5)-bisphosphate than those mediated by the matrix domain of HIV-1 Gag. J Virol 85(8):3802–3810

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jacobson C, Mostov K (2007) Catch the KIF5B train to the apical surface. Dev Cell 13(4):457–458

    CAS  PubMed  Google Scholar 

  • Jean S, Kiger AA (2012) Coordination between RAB GTPase and phosphoinositide regulation and functions. Nat Rev Mol Cell Biol 13(7):463–470

    CAS  PubMed  Google Scholar 

  • Jeanes A, Smutny M, Leerberg JM, Yap AS (2009) Phosphatidylinositol 3′-kinase signalling supports cell height in established epithelial monolayers. J Mol Histol 40(5–6):395–405

    CAS  PubMed  Google Scholar 

  • Kato K, Yazawa T, Taki K, Mori K, Wang S, Nishioka T et al (2012) The inositol 5-phosphatase SHIP2 is an effector of RhoA and is involved in cell polarity and migration. Mol Biol Cell 23(13):2593–2604

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kazmierczak BI, Mostov K, Engel JN (2001) Interaction of bacterial pathogens with polarized epithelium. Annu Rev Microbiol 55:407–435

    CAS  PubMed  Google Scholar 

  • Kierbel A, Gassama-Diagne A, Mostov K, Engel JN (2005) The phosphoinositol-3-kinase-protein kinase B/Akt pathway is critical for Pseudomonas aeruginosa strain PAK internalization. Mol Biol Cell 16(5):2577–2585

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kierbel A, Gassama-Diagne A, Rocha C, Radoshevich L, Olson J, Mostov K et al (2007) Pseudomonas aeruginosa exploits a PIP3-dependent pathway to transform apical into basolateral membrane. J Cell Biol 177(1):21–27

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kölsch V, Charest PG, Firtel RA (2008) The regulation of cell motility and chemotaxis by phospholipid signaling. J Cell Sci 121(Pt 5):551–559

    PubMed Central  PubMed  Google Scholar 

  • Kotelevets L, van Hengel J, Bruyneel E, Mareel M, van Roy F, Chastre E (2005) Implication of the MAGI-1b/PTEN signalosome in stabilization of adherens junctions and suppression of invasiveness. FASEB J 19(1):115–117

    CAS  PubMed  Google Scholar 

  • Krahn MP, Wodarz A (2012) Phosphoinositide lipids and cell polarity: linking the plasma membrane to the cytocortex. Essays Biochem 53:15–27

    CAS  PubMed  Google Scholar 

  • Krahn MP, Klopfenstein DR, Fischer N, Wodarz A (2010) Membrane targeting of Bazooka/PAR-3 is mediated by direct binding to phosphoinositide lipids. Curr Biol 20(7):636–642

    CAS  PubMed  Google Scholar 

  • Krauss M, Haucke V (2007) Phosphoinositides: regulators of membrane traffic and protein function. FEBS Lett 581(11):2105–2111

    CAS  PubMed  Google Scholar 

  • Kutateladze TG (2010) Translation of the phosphoinositide code by PI effectors. Nat Chem Biol 6(7):507–513

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lapierre LA, Kumar R, Hales CM, Navarre J, Bhartur SG, Burnette JO et al (2001) Myosin vb is associated with plasma membrane recycling systems. Mol Biol Cell 12(6):1843–1857

    PubMed Central  CAS  PubMed  Google Scholar 

  • Laprise P, Viel A, Rivard N (2004) Human homolog of disc-large is required for adherens junction assembly and differentiation of human intestinal epithelial cells. J Biol Chem 279(11):10157–10166

    CAS  PubMed  Google Scholar 

  • Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9(2):99–111

    CAS  PubMed  Google Scholar 

  • Lippincott-Schwartz J, Manley S (2009) Putting super-resolution fluorescence microscopy to work. Nat Methods 6(1):21–23

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu J, Zuo X, Yue P, Guo W (2007) Phosphatidylinositol 4,5-bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells. Mol Biol Cell 18(11):4483–4492

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu S, Yang W, Shen L, Turner JR, Coyne CB, Wang T (2009) Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection. J Virol 83(4):2011–2014

    PubMed Central  CAS  PubMed  Google Scholar 

  • Macklin WB (2010) The myelin brake: when enough is enough. Sci Signal 3(140):e32

    Google Scholar 

  • Marée AFM, Grieneisen VA, Edelstein-Keshet L (2012) How cells integrate complex stimuli: the effect of feedback from phosphoinositides and cell shape on cell polarization and motility. PLoS Comput Biol 8(3):e1002402

    PubMed Central  PubMed  Google Scholar 

  • Martin TF (1998) Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu Rev Cell Dev Biol 14:231–264

    CAS  PubMed  Google Scholar 

  • Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U, Gerke V et al (2007) PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128(2):383–397

    PubMed Central  CAS  PubMed  Google Scholar 

  • Martini M, Ciraolo E, Gulluni F, Hirsch E (2013) Targeting PI3K in cancer: any good news? Front Oncol 3:108

    PubMed Central  PubMed  Google Scholar 

  • Mason D, Mallo GV, Terebiznik MR, Payrastre B, Finlay BB, Brumell JH et al (2007) Alteration of epithelial structure and function associated with PtdIns(4,5)P2 degradation by a bacterial phosphatase. J Gen Physiol 129(4):267–283

    PubMed Central  CAS  PubMed  Google Scholar 

  • Massarwa R, Schejter ED, Shilo B-Z (2009) Apical secretion in epithelial tubes of the Drosophila embryo is directed by the Formin-family protein Diaphanous. Dev Cell 16(6):877–888

    CAS  PubMed  Google Scholar 

  • Mee CJ, Grove J, Harris HJ, Hu K, Balfe P, McKeating JA (2008) Effect of cell polarization on hepatitis C virus entry. J Virol 82(1):461–470

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mee CJ, Harris HJ, Farquhar MJ, Wilson G, Reynolds G, Davis C et al (2009) Polarization restricts hepatitis C virus entry into HepG2 hepatoma cells. J Virol 83(12):6211–6221

    PubMed Central  CAS  PubMed  Google Scholar 

  • Miyoshi J, Takai Y (2008) Structural and functional associations of apical junctions with cytoskeleton. Biochim Biophys Acta 1778(3):670–691

    CAS  PubMed  Google Scholar 

  • Muthuswamy SK, Xue B (2012) Cell polarity as a regulator of cancer cell behavior plasticity. Annu Rev Cell Dev Biol 28:599–625

    PubMed Central  CAS  PubMed  Google Scholar 

  • Narayanan SP, Flores AI, Wang F, Macklin WB (2009) Akt signals through the mammalian target of rapamycin pathway to regulate CNS myelination. J Neurosci 29(21):6860–6870

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nelson WJ (2003) Adaptation of core mechanisms to generate cell polarity. Nature 422(6933):766–774

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nelson CM (2013) Forces in epithelial origami. Dev Cell 26(6):554–556

    CAS  PubMed  Google Scholar 

  • Nelson CM, Bissell MJ (2006) Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 22:287–309

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nishio M, Watanabe K, Sasaki J, Taya C, Takasuga S, Iizuka R, Balla T, Yamazaki M, Watanabe H, Itoh R, Kuroda S, Horie Y, Förster I, Mak TW, Yonekawa H, Penninger JM, Kanaho Y, Suzuki A, Sasaki T (2007) Control of cell polarity and motility by the PtdIns(3,4,5)P3 phosphatase SHIP1. Nat Cell Biol 9(1):36–44, PMID: 17173042

    CAS  PubMed  Google Scholar 

  • Noren NK, Niessen CM, Gumbiner BM, Burridge K (2001) Cadherin engagement regulates Rho family GTPases. J Biol Chem 276(36):33305–33308

    CAS  PubMed  Google Scholar 

  • Noseda R, Belin S, Piguet F, Vaccari I, Scarlino S, Brambilla P et al (2013) DDIT4/REDD1/RTP801 is a novel negative regulator of Schwann cell myelination. J Neurosci 33(38):15295–15305

    PubMed Central  CAS  PubMed  Google Scholar 

  • O’Brien LE, Jou TS, Pollack AL, Zhang Q, Hansen SH, Yurchenco P et al (2001) Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat Cell Biol 3(9):831–838, PMID: 12094219

    PubMed  Google Scholar 

  • O’Brien LE, Zegers MMP, Mostov KE (2002) Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat Rev Mol Cell Biol 3(7):531–537

    PubMed  Google Scholar 

  • Ozato-Sakurai N, Fujita A, Fujimoto T (2011) The distribution of phosphatidylinositol 4,5-bisphosphate in acinar cells of rat pancreas revealed with the freeze-fracture replica labeling method. PLoS One 6(8):e23567

    PubMed Central  CAS  PubMed  Google Scholar 

  • Parise LV, Lee J, Juliano RL (2000) New aspects of integrin signaling in cancer. Semin Cancer Biol 10(6):407–414

    CAS  PubMed  Google Scholar 

  • Payrastre B (2004) Phosphoinositides: lipid kinases and phosphatases. Methods Mol Biol 273:201–212

    CAS  PubMed  Google Scholar 

  • Pece S, Chiariello M, Murga C, Gutkind JS (1999) Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex. J Biol Chem 274(27):19347–19351

    CAS  PubMed  Google Scholar 

  • Pesesse X, Dewaste V, De Smedt F, Laffargue M, Giuriato S, Moreau C et al (2001) The Src homology 2 domain containing inositol 5-phosphatase SHIP2 is recruited to the epidermal growth factor (EGF) receptor and dephosphorylates phosphatidylinositol 3,4,5-trisphosphate in EGF-stimulated COS-7 cells. J Biol Chem 276(30):28348–28355

    CAS  PubMed  Google Scholar 

  • Pilot F, Philippe J-M, Lemmers C, Lecuit T (2006) Spatial control of actin organization at adherens junctions by a synaptotagmin-like protein Btsz. Nature 442(7102):580–584

    CAS  PubMed  Google Scholar 

  • Pinal N, Goberdhan DCI, Collinson L, Fujita Y, Cox IM, Wilson C et al (2006) Regulated and polarized PtdIns(3,4,5)P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells. Curr Biol 16(2):140–149

    CAS  PubMed  Google Scholar 

  • Pizarro-Cerdá J, Cossart P (2004) Subversion of phosphoinositide metabolism by intracellular bacterial pathogens. Nat Cell Biol 6(11):1026–1033

    PubMed  Google Scholar 

  • Prasad N, Topping RS, Decker SJ (2001) SH2-containing inositol 5′-phosphatase SHIP2 associates with the p130(Cas) adapter protein and regulates cellular adhesion and spreading. Mol Cell Biol 21(4):1416–1428

    PubMed Central  CAS  PubMed  Google Scholar 

  • Reiss S, Rebhan I, Backes P, Romero-Brey I, Erfle H, Matula P et al (2011) Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe 9(1):32–45

    PubMed Central  CAS  PubMed  Google Scholar 

  • Reiter JF, Mostov K (2006) Vesicle transport, cilium formation, and membrane specialization: the origins of a sensory organelle. Proc Natl Acad Sci U S A 103(49):18383–18384

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rodríguez-Fraticelli AE, Martín-Belmonte F (2013) Mechanical control of epithelial lumen formation. Small GTPases 4(2):136–140

    PubMed Central  PubMed  Google Scholar 

  • Roland JT, Kenworthy AK, Peranen J, Caplan S, Goldenring JR (2007) Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol Biol Cell 18(8):2828–2837

    PubMed Central  CAS  PubMed  Google Scholar 

  • Roland JT, Bryant DM, Datta A, Itzen A, Mostov KE, Goldenring JR (2011) Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc Natl Acad Sci U S A 108(7):2789–2794

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rousso T, Shewan AM, Mostov KE, Schejter ED, Shilo B-Z (2013) Apical targeting of the formin Diaphanous in Drosophila tubular epithelia. eLife 2:e00666

    PubMed Central  PubMed  Google Scholar 

  • Royer C, Lu X (2011) Epithelial cell polarity: a major gatekeeper against cancer? Cell Death Differ 18(9):1470–1477

    PubMed Central  CAS  PubMed  Google Scholar 

  • Salyers A, Whitt D (eds) (2002) Bacterial pathogenesis: a molecular approach. ASM press, Washington, DC

    Google Scholar 

  • Santiago-Tirado FH, Legesse-Miller A, Schott D, Bretscher A (2011) PI4P and Rab inputs collaborate in myosin-V-dependent transport of secretory compartments in yeast. Dev Cell 20(1):47–59

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sasaki AT, Firtel RA (2006) Regulation of chemotaxis by the orchestrated activation of Ras, PI3K, and TOR. Eur J Cell Biol 85(9–10):873–895

    CAS  PubMed  Google Scholar 

  • Sasaki T, Takasuga S, Sasaki J, Kofuji S, Eguchi S, Yamazaki M et al (2009) Mammalian phosphoinositide kinases and phosphatases. Prog Lipid Res 48(6):307–343

    CAS  PubMed  Google Scholar 

  • Scheid MP, Huber M, Damen JE, Hughes M, Kang V, Neilsen P et al (2002) Phosphatidylinositol (3,4,5)P3 is essential but not sufficient for protein kinase B (PKB) activation; phosphatidylinositol (3,4)P2 is required for PKB phosphorylation at Ser-473: studies using cells from SH2-containing inositol-5-phosphatase knockout mice. J Biol Chem 277(11):9027–9035

    CAS  PubMed  Google Scholar 

  • Shewan A, Eastburn DJ, Mostov K (2011) Phosphoinositides in cell architecture. Cold Spring Harb Perspect Biol 3(8):a004796

    PubMed Central  PubMed  Google Scholar 

  • Srinivasan S, Wang F, Glavas S, Ott A, Hofmann F, Aktories K, Kalman D, Bourne HR (2003) Rac and Cdc42 play distinct roles in regulating PI(3,4,5)P3 and polarity during neutrophil chemotaxis. J Cell Biol 160(3):375–385, PMID: 12551955

    PubMed Central  CAS  PubMed  Google Scholar 

  • Snooks MJ, Bhat P, Mackenzie J, Counihan NA, Vaughan N, Anderson DA (2008) Vectorial entry and release of hepatitis A virus in polarized human hepatocytes. J Virol 82(17):8733–8742

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stenzel N, Fetzer CP, Heumann R, Erdmann KS (2009) PDZ-domain-directed basolateral targeting of the peripheral membrane protein FRMPD2 in epithelial cells. J Cell Sci 122(Pt 18):3374–3384

    CAS  PubMed  Google Scholar 

  • Subauste MC, Nalbant P, Adamson ED, Hahn KM (2005) Vinculin controls PTEN protein level by maintaining the interaction of the adherens junction protein beta-catenin with the scaffolding protein MAGI-2. J Biol Chem 280(7):5676–5681

    CAS  PubMed  Google Scholar 

  • Szalinski CM, Guerriero CJ, Ruiz WG, Docter BE, Rbaibi Y, Pastor-Soler NM et al (2013) PIP5KIβ selectively modulates apical endocytosis in polarized renal epithelial cells. PLoS One 8(1):e53790

    PubMed Central  CAS  PubMed  Google Scholar 

  • Takahama S, Hirose T, Ohno S (2008) aPKC restricts the basolateral determinant PtdIns(3,4,5)P3 to the basal region. Biochem Biophys Res Commun 368(2):249–255

    CAS  PubMed  Google Scholar 

  • Treyer A, Müsch A (2013) Hepatocyte polarity. Compr Physiol 3(1):243–287

    PubMed Central  PubMed  Google Scholar 

  • Trotard M, Lepère-Douard C, Régeard M, Piquet-Pellorce C, Lavillette D, Cosset F-L et al (2009) Kinases required in hepatitis C virus entry and replication highlighted by small interference RNA screening. FASEB J 23(11):3780–3789

    CAS  PubMed  Google Scholar 

  • Tyler WA, Gangoli N, Gokina P, Kim HA, Covey M, Levison SW et al (2009) Activation of the mammalian target of rapamycin (mTOR) is essential for oligodendrocyte differentiation. J Neurosci 29(19):6367–6378

    PubMed Central  CAS  PubMed  Google Scholar 

  • Van Zeijl L, Ponsioen B, Giepmans BNG, Ariaens A, Postma FR, Várnai P et al (2007) Regulation of connexin43 gap junctional communication by phosphatidylinositol 4,5-bisphosphate. J Cell Biol 177(5):881–891

    PubMed Central  PubMed  Google Scholar 

  • Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC et al (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70:535–602

    CAS  PubMed  Google Scholar 

  • Vanhaesebroeck B, Vogt PK, Rommel C (2010) PI3K: from the bench to the clinic and back. Curr Top Microbiol Immunol 347:1–19

    PubMed  Google Scholar 

  • Vanhaesebroeck B, Stephens L, Hawkins P (2012) PI3K signalling: the path to discovery and understanding. Nat Rev Mol Cell Biol 13(3):195–203

    CAS  PubMed  Google Scholar 

  • Várnai P, Lin X, Lee SB, Tuymetova G, Bondeva T, Spät A et al (2002) Inositol lipid binding and membrane localization of isolated pleckstrin homology (PH) domains. Studies on the PH domains of phospholipase C delta 1 and p130. J Biol Chem 277(30):27412–27422

    PubMed  Google Scholar 

  • Vázquez-Ulloa E, Lizano M, Avilés-Salas A, Alfaro-Moreno E, Contreras-Paredes A (2011) Abnormal distribution of hDlg and PTEN in premalignant lesions and invasive cervical cancer. Gynecol Oncol 122(3):663–668

    PubMed  Google Scholar 

  • Von Stein W, Ramrath A, Grimm A, Müller-Borg M, Wodarz A (2005) Direct association of Bazooka/PAR-3 with the lipid phosphatase PTEN reveals a link between the PAR/aPKC complex and phosphoinositide signaling. Development 132(7):1675–1686

    Google Scholar 

  • Wang L, Boyer JL (2004) The maintenance and generation of membrane polarity in hepatocytes. Hepatology 39(4):892–899

    PubMed  Google Scholar 

  • Wang F, Herzmark P, Weiner OD, Srinivasan S, Servant G, Bourne HR (2002) Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nat Cell Biol 4(7):513–518

    CAS  PubMed  Google Scholar 

  • Watton SJ, Downward J (1999) Akt/PKB localisation and 3′ phosphoinositide generation at sites of epithelial cell-matrix and cell-cell interaction. Curr Biol 9(8):433–436

    CAS  PubMed  Google Scholar 

  • Weber SS, Ragaz C, Hilbi H (2009) Pathogen trafficking pathways and host phosphoinositide metabolism. Mol Microbiol 71(6):1341–1352. doi:10.1111/j.1365-2958.2009.06608.x, PMID: 19208094

    CAS  PubMed  Google Scholar 

  • Weiger MC, Parent CA (2012) Phosphoinositides in chemotaxis. Subcell Biochem 59:217–254

    CAS  PubMed  Google Scholar 

  • Weiner OD, Neilsen PO, Prestwich GD, Kirschner MW, Cantley LC, Bourne HR (2002) A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat Cell Biol 4(7):509–513

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wilkins C, Woodward J, Lau DT-Y, Barnes A, Joyce M, McFarlane N et al (2013) IFITM1 is a tight junction protein that inhibits hepatitis C virus entry. Hepatology 57(2):461–469

    PubMed Central  CAS  PubMed  Google Scholar 

  • Woodfield RJ, Hodgkin MN, Akhtar N, Morse MA, Fuller KJ, Saqib K et al (2001) The p85 subunit of phosphoinositide 3-kinase is associated with beta-catenin in the cadherin-based adhesion complex. Biochem J 360(Pt 2):335–344

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wu H, Feng W, Chen J, Chan L-N, Huang S, Zhang M (2007) PDZ domains of Par-3 as potential phosphoinositide signaling integrators. Mol Cell 28(5):886–898

    CAS  PubMed  Google Scholar 

  • Wullschleger S, Wasserman DH, Gray A, Sakamoto K, Alessi DR (2011) Role of TAPP1 and TAPP2 adaptor binding to PtdIns(3,4)P2 in regulating insulin sensitivity defined by knock-in analysis. Biochem J 434(2):265–274

    CAS  PubMed  Google Scholar 

  • Wymann MP, Marone R (2005) Phosphoinositide 3-kinase in disease: timing, location, and scaffolding. Curr Opin Cell Biol 17(2):141–149

    CAS  PubMed  Google Scholar 

  • Wymann MP, Schneiter R (2008) Lipid signalling in disease. Nat Rev Mol Cell Biol 9(2):162–176. doi:10.1038/nrm2335, PMID: 18216772

    CAS  PubMed  Google Scholar 

  • Xiong X, Xu Q, Huang Y, Singh RD, Anderson R, Leof E et al (2012) An association between type Iγ PI4P 5-kinase and Exo70 directs E-cadherin clustering and epithelial polarization. Mol Biol Cell 23(1):87–98

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yan Y, Denef N, Tang C, Schüpbach T (2011) Drosophila PI4KIIIalpha is required in follicle cells for oocyte polarization and Hippo signaling. Development 138(9):1697–1703

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang HW, Shin M-G, Lee S, Kim J-R, Park WS, Cho K-H et al (2012) Cooperative activation of PI3K by Ras and Rho family small GTPases. Mol Cell 47(2):281–290

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yap AS, Kovacs EM (2003) Direct cadherin-activated cell signaling: a view from the plasma membrane. J Cell Biol 160(1):11–16

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yu W, Shewan AM, Brakeman P, Eastburn DJ, Datta A, Bryant DM et al (2008) Involvement of RhoA, ROCK I and myosin II in inverted orientation of epithelial polarity. EMBO Rep 9(9):923–929

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang J, Liu Z, Rasschaert J, Blero D, Deneubourg L, Schurmans S et al (2007) SHIP2 controls PtdIns(3,4,5)P(3) levels and PKB activity in response to oxidative stress. Cell Signal 19(10):2194–2200

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Association pour la Recherche sur le Cancer (ARC/SUBV/CKLQ6) to A.G.D. We acknowledge the support of the National Council for Scientific Research Lebanon for supporting A.A. A.M.S. is the recipient of a National Breast Cancer Foundation Early Career Researcher Fellowship.

Author information

Authors and Affiliations

  1. School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, QLD, 4072, Australia

    Annette M. Shewan

  2. Univ Paris-Sud, UMR-S 785, Villejuif, 94800, France

    Aline Awad, Juan Peng & Ama Gassama-Diagne

  3. Inserm Unité 785, Villejuif, 94800, France

    Aline Awad, Juan Peng & Ama Gassama-Diagne

  4. Centre Hépato-Biliaire, Hôpital Paul Brousse, 12-14 Avenue Paul Vaillant Couturier, Villejuif, 94800, France

    Ama Gassama-Diagne

Authors
  1. Annette M. Shewan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aline Awad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ama Gassama-Diagne
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ama Gassama-Diagne .

Editor information

Editors and Affiliations

  1. Institute-associated Research Group “Cell Adhesion and Cell Polarity”, Institute of Medical Biochemistry, Center for Molecular Biology of Inflammation (ZMBE), University Münster, Münster, Nordrhein-Westfalen, Germany

    Klaus Ebnet

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Shewan, A.M., Awad, A., Peng, J., Gassama-Diagne, A. (2015). Phosphoinositides as Determinants of Membrane Identity, Apicobasal Polarity, and Lumen Formation. In: Ebnet, K. (eds) Cell Polarity 1. Springer, Cham. https://doi.org/10.1007/978-3-319-14463-4_10

Download citation

Publish with us

Policies and ethics

Search

Navigation