Home LiteratureArticle Details
PMID: 17395624 Published · ppublish English Journal Article Research Support, N.I.H., Intramural

Imaging and manipulating phosphoinositides in living cells.

The Journal of physiology ·Vol. 582 ·No. Pt 3 ·2007-08-01 ·Pages 927-37

Balla T

Abstract

Phosphoinositides are minor phospholipid constituents of virtually every biological membrane yet they play fundamental roles in controlling membrane-bound signalling events. Phosphoinositides are produced from phosphatidylinositol (PtdIns) by phosphorylation of one or more of three positions (3, 4 and 5) of the inositol headgroup located at the membrane cytoplasmic interface by distinct families of inositol lipid kinases. Intriguingly, many of the kinase reactions are catalysed by more than one form of the kinases even in simple organisms and these enzymes often assume non-redundant functions. A similar diversity is seen with inositide phosphatases, the enzymes that dephosphorylate phosphoinositides with a certain degree of specificity and the impairments of which are often linked to human diseases. This degree of multiplicity at the enzyme level together with the universal roles of these lipids in cell regulation assumes that inositol lipids are spatially and functionally restricted in specific membrane compartments. Studying the compartmentalized roles of these lipids at the cellular level represents a major methodological challenge. Over the last 10 years significant progress has been made in creating reagents that can monitor inositol lipid changes in live cells with fluorescence or confocal microscopy. New methods are also being developed to manipulate these lipids in specific membrane compartments in a regulated fashion. This article recalls some historical aspects of inositide research and describes the new methodological advances highlighting their great potential as well as the problems one can encounter with their use.

MeSH Terms
1-Phosphatidylinositol 4-Kinase/metabolism Animals Inositol Phosphates/physiology Lipids/physiology Phosphatidylinositols/physiology Phosphorylation Protein Kinases/physiology TOR Serine-Threonine Kinases
Chemicals
Inositol Phosphates Lipids Phosphatidylinositols Protein Kinases MTOR protein, human 1-Phosphatidylinositol 4-Kinase TOR Serine-Threonine Kinases
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Balla Tamas
National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892, USA. [email protected]
References (69)
69 references, click to expand
  1. Insulin-dependent translocation of ARNO to the plasma membrane of adipocytes requires phosphatidylinositol 3-kinase.
    Curr Biol. 1998 Apr 9;8(8):463-6 PMID: 9550703
  2. Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities.
    Biochem J. 2000 Oct 1;351(Pt 1):19-31 PMID: 11001876
  3. Receptor activity-independent recruitment of betaarrestin2 reveals specific signalling modes.
    EMBO J. 2004 Oct 13;23(20):3950-61 PMID: 15385966
  4. Inositol phospholipids and cell surface receptor function.
    Biochim Biophys Acta. 1975 Mar 25;415(1):81-47 PMID: 164246
  5. Intracellular delivery of phosphoinositides and inositol phosphates using polyamine carriers.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11286-91 PMID: 11005844
  6. Regulation of purified subtypes of phosphatidylinositol-specific phospholipase C beta by G protein alpha and beta gamma subunits.
    J Biol Chem. 1993 May 5;268(13):9667-74 PMID: 8387502
  7. A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling.
    Cell. 2006 May 19;125(4):733-47 PMID: 16647110
  8. The molecular heterogeneity of protein kinase C and its implications for cellular regulation.
    Nature. 1988 Aug 25;334(6184):661-5 PMID: 3045562
  9. Novel function of phosphatidylinositol 4,5-bisphosphate as a cofactor for brain membrane phospholipase D.
    J Biol Chem. 1994 Aug 26;269(34):21403-6 PMID: 8063770
  10. Structural and functional characterization of inositol 1,4,5-trisphosphate receptor channel from mouse cerebellum.
    J Biol Chem. 1991 Jan 15;266(2):1109-16 PMID: 1845986
  11. Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate.
    Proc Natl Acad Sci U S A. 2007 Mar 6;104(10):3793-8 PMID: 17360432
  12. PTEN and myotubularins: families of phosphoinositide phosphatases.
    Methods Enzymol. 2003;366:43-56 PMID: 14674238
  13. Selective cellular effects of overexpressed pleckstrin-homology domains that recognize PtdIns(3,4,5)P3 suggest their interaction with protein binding partners.
    J Cell Sci. 2005 Oct 15;118(Pt 20):4879-88 PMID: 16219693
  14. An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways.
    Nat Methods. 2005 Jun;2(6):415-8 PMID: 15908919
  15. Spatial analysis of 3' phosphoinositide signaling in living fibroblasts: II. Parameter estimates for individual cells from experiments.
    Biophys J. 2004 Jan;86(1 Pt 1):599-608 PMID: 14695304
  16. A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositolphospholipids.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5317-21 PMID: 7777504
  17. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells.
    EMBO J. 2000 Sep 1;19(17):4577-88 PMID: 10970851
  18. The sequence of phosphatidylinositol-4-phosphate 5-kinase defines a novel family of lipid kinases.
    J Biol Chem. 1995 Feb 17;270(7):2881-4 PMID: 7852364
  19. Controlled dimerization of ErbB receptors provides evidence for differential signaling by homo- and heterodimers.
    Mol Cell Biol. 1999 Oct;19(10):6845-57 PMID: 10490623
  20. Control of cell polarity and motility by the PtdIns(3,4,5)P3 phosphatase SHIP1.
    Nat Cell Biol. 2007 Jan;9(1):36-44 PMID: 17173042
  21. Inositol trisphosphate, a novel second messenger in cellular signal transduction.
    Nature. 1984 Nov 22-28;312(5992):315-21 PMID: 6095092
  22. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion.
    Cell. 2000 Jan 21;100(2):221-8 PMID: 10660045
  23. A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate.
    Nature. 1997 Nov 13;390(6656):192-6 PMID: 9367159
  24. Monitoring agonist-induced phospholipase C activation in live cells by fluorescence resonance energy transfer.
    J Biol Chem. 2001 May 4;276(18):15337-44 PMID: 11152673
  25. Production and characterization of monoclonal antibodies that bind to phosphatidylinositol 4,5-bisphosphate.
    Mol Immunol. 1988 Oct;25(10):1025-31 PMID: 2851103
  26. The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase.
    Nature. 1992 Jul 16;358(6383):239-42 PMID: 1321346
  27. Distinct Golgi populations of phosphatidylinositol 4-phosphate regulated by phosphatidylinositol 4-kinases.
    J Biol Chem. 2005 Mar 18;280(11):10501-8 PMID: 15634669
  28. Cloning and sequence of multiple forms of phospholipase C.
    Cell. 1988 Jul 15;54(2):161-9 PMID: 3390863
  29. Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells.
    J Cell Biol. 2006 Nov 6;175(3):377-82 PMID: 17088424
  30. Signalling through the lipid products of phosphoinositide-3-OH kinase.
    Nature. 1997 Jun 12;387(6634):673-6 PMID: 9192891
  31. Evidence that the inositol phospholipids are necessary for exocytosis. Loss of inositol phospholipids and inhibition of secretion in permeabilized cells caused by a bacterial phospholipase C and removal of ATP.
    Biochem J. 1990 May 15;268(1):15-25 PMID: 2160809
  32. Spatiotemporal dynamics of inositol 1,4,5-trisphosphate that underlies complex Ca2+ mobilization patterns.
    Science. 1999 May 28;284(5419):1527-30 PMID: 10348740
  33. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting.
    Science. 1993 Apr 2;260(5104):88-91 PMID: 8385367
  34. Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton's tyrosine kinase pleckstrin homology domain visualized in single living cells.
    J Biol Chem. 1999 Apr 16;274(16):10983-9 PMID: 10196179
  35. The role of the phosphoinositides at the Golgi complex.
    Biochim Biophys Acta. 2005 Jul 10;1744(3):396-405 PMID: 15979509
  36. The site of diphosphoinositide synthesis in rat liver.
    Biochem Biophys Res Commun. 1965 Nov 22;21(4):333-8 PMID: 4286175
  37. Active Arf6 recruits ARNO/cytohesin GEFs to the PM by binding their PH domains.
    Mol Biol Cell. 2007 Jun;18(6):2244-53 PMID: 17409355
  38. A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system.
    EMBO J. 1995 Jul 17;14(14):3339-48 PMID: 7628435
  39. Imaging phosphoinositide dynamics using GFP-tagged protein domains.
    Biol Cell. 2005 Jul;97(7):501-18 PMID: 15966865
  40. Spatial sensing in fibroblasts mediated by 3' phosphoinositides.
    J Cell Biol. 2000 Dec 11;151(6):1269-80 PMID: 11121441
  41. Phosphatidylinositol phosphate kinases.
    J Endocrinol Invest. 2004;27(6 Suppl):137-42 PMID: 15481814
  42. Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels.
    Science. 2006 Dec 1;314(5804):1454-7 PMID: 16990515
  43. Regulation of phosphoinositide signaling by the inositol polyphosphate 5-phosphatases.
    IUBMB Life. 2006 Aug;58(8):451-6 PMID: 16916781
  44. THE STRUCTURE OF A MYOINOSITOL MANNOSIDE FROM MYCOBACTERIUM TUBERCULOSIS GLYCOLIPID.
    Biochemistry. 1964 May;3:682-5 PMID: 14193639
  45. Characterization of phosphatidylinositol kinase activity associated with the insulin receptor.
    Eur J Biochem. 1986 Mar 3;155(2):345-51 PMID: 3007126
  46. Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools.
    J Cell Biol. 1998 Oct 19;143(2):501-10 PMID: 9786958
  47. Type I phosphatidylinositol kinase makes a novel inositol phospholipid, phosphatidylinositol-3-phosphate.
    Nature. 1988 Apr 14;332(6165):644-6 PMID: 2833705
  48. Compartmental signal modulation: Endosomal phosphatidylinositol 3-phosphate controls endosome morphology and selective cargo sorting.
    Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15473-8 PMID: 17030795
  49. Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells.
    Curr Biol. 1998 Mar 12;8(6):343-6 PMID: 9512420
  50. Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains.
    Mol Cell. 2004 Mar 12;13(5):677-88 PMID: 15023338
  51. Tyrosine 1101 of Tie2 is the major site of association of p85 and is required for activation of phosphatidylinositol 3-kinase and Akt.
    Mol Cell Biol. 1998 Jul;18(7):4131-40 PMID: 9632797
  52. Subcellular targeting by membrane lipids.
    Curr Opin Cell Biol. 2001 Apr;13(2):146-52 PMID: 11248547
  53. The cloning and sequence of the C isoform of PtdIns4P 5-kinase.
    Biochem J. 1995 Aug 1;309 ( Pt 3):715-9 PMID: 7639683
  54. GTP hydrolysis by ADP-ribosylation factor is dependent on both an ADP-ribosylation factor GTPase-activating protein and acid phospholipids.
    J Biol Chem. 1994 Apr 8;269(14):10758-63 PMID: 8144664
  55. Live cell imaging of phosphoinositide dynamics with fluorescent protein domains.
    Biochim Biophys Acta. 2006 Aug;1761(8):957-67 PMID: 16702024
  56. Phospholipase C in living cells: activation, inhibition, Ca2+ requirement, and regulation of M current.
    J Gen Physiol. 2005 Sep;126(3):243-62 PMID: 16129772
  57. A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type-III alpha: studies with the PH domains of the oxysterol binding protein and FAPP1.
    Mol Biol Cell. 2005 Mar;16(3):1282-95 PMID: 15635101
  58. Multiple pools of phosphatidylinositol 4-phosphate detected using the pleckstrin homology domain of Osh2p.
    J Biol Chem. 2004 Oct 22;279(43):44683-9 PMID: 15271978
  59. Enzyme secretion and the incorporation of P32 into phospholipides of pancreas slices.
    J Biol Chem. 1953 Aug;203(2):967-77 PMID: 13084667
  60. Characteristics of rat liver phosphatidylinositol kinase and its presence in the plasma membrane.
    Biochim Biophys Acta. 1967 Dec 5;144(3):649-58 PMID: 4294903
  61. The phosphoinositide 3-kinase pathway.
    Science. 2002 May 31;296(5573):1655-7 PMID: 12040186
  62. Elimination of plasma membrane phosphatidylinositol (4,5)-bisphosphate is required for exocytosis from mast cells.
    J Cell Sci. 2006 May 15;119(Pt 10):2084-94 PMID: 16687737
  63. Phosphatidylinositol phosphate kinases put PI4,5P(2) in its place.
    J Membr Biol. 2003 Jul 15;194(2):77-89 PMID: 14502432
  64. Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1.
    Biochem J. 2002 May 1;363(Pt 3):657-66 PMID: 11964166
  65. Probing phosphoinositide functions in signaling and membrane trafficking.
    Trends Cell Biol. 2005 May;15(5):259-68 PMID: 15866030
  66. Phosphatidylinositol 4-kinases: old enzymes with emerging functions.
    Trends Cell Biol. 2006 Jul;16(7):351-61 PMID: 16793271
  67. Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains.
    Mol Cell. 1998 Jul;2(1):157-62 PMID: 9702203
  68. FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P.
    Nat Cell Biol. 2004 May;6(5):393-404 PMID: 15107860
  69. PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane.
    Science. 2006 Dec 1;314(5804):1458-61 PMID: 17095657
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
2007-08-01
Epub
2007-00-29
Pages
927-37
Language
English
Region
England
NLM ID
0266262
PMCID
PMC2075240
Subset
IM
Grants
Intramural NIH HHS · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]