Home LiteratureArticle Details
PMID: 23083708 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Molecular brightness analysis reveals phosphatidylinositol 4-Kinase IIβ association with clathrin-coated vesicles in living cells.

Biophysical journal ·Vol. 103 ·No. 8 ·2012-10-17 ·Pages 1657-65

Li J, Barylko B, Johnson J, Mueller JD, Albanesi JP, Chen Y

Abstract

Mammalian cells express two classes of phosphatidylinositol 4-kinase (PI4K), designated as Types II and III, that phosphorylate phosphatidylinositol to generate PI4P. A number of studies have indicated that these enzymes are important for Golgi trafficking and both early and late stages of endocytosis. In this study, we focus on PI4KIIβ, a protein that is evenly distributed between membrane and soluble fractions, and is believed to participate in stimulus-dependent phosphoinositide signaling. Using molecular brightness analysis, we found that EGFP-tagged PI4KIIβ exists as two distinct species in the cytoplasm: a soluble monomer and a high-order complex enriched with multiple copies of PI4KIIβ. This observation was confirmed by an autocorrelation analysis that identified two species with distinct mobilities. We further demonstrate that the high-order complex enriched with PI4KIIβ is sensitive to inhibition of palmitoylation, indicating that it is associated with membranes, very likely vesicles. Indeed, we show that the high-order PI4KIIβ complex is sensitive to expression of dynamin 2 (K44A), a dominant-negative inhibitor of endocytosis. Using dual-color heterospecies partition analysis, we directly detected that PI4KIIβ comoves with clathrin light chain on vesicles. This analysis allows us to isolate the comobile species in the presence of strong background contribution from the monomeric pool of PI4KIIβ. Our results strongly suggest that PI4KIIβ is involved in an early stage of endocytosis and is associated with clathrin-coated vesicles. Moreover, we establish molecular brightness as a powerful tool for characterizing cellular cytosolic vesicles that are otherwise difficult to characterize by other techniques.

MeSH Terms
1-Phosphatidylinositol 4-Kinase/metabolism Cell Line, Tumor Cell Membrane/metabolism,ultrastructure Clathrin-Coated Vesicles/enzymology,metabolism Cytosol/metabolism Dynamin II/metabolism Endocytosis Humans Lipoylation Spectrometry, Fluorescence
Chemicals
1-Phosphatidylinositol 4-Kinase Dynamin II
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Li Jinhui
Physics Department, University of Minnesota, Minneapolis, Minnesota, USA.
Barylko Barbara
Johnson Jolene
Mueller Joachim D
Albanesi Joseph P
Chen Yan
References (51)
51 references, click to expand
  1. Phosphatidylinositol-4-kinase type II alpha contains an AP-3-sorting motif and a kinase domain that are both required for endosome traffic.
    Mol Biol Cell. 2008 Apr;19(4):1415-26 PMID: 18256276
  2. Phosphatidylinositol-4-kinase type II alpha is a component of adaptor protein-3-derived vesicles.
    Mol Biol Cell. 2005 Aug;16(8):3692-704 PMID: 15944223
  3. Concentration correlation spectroscopy: a new biophysical probe based on occupation number fluctuations.
    Annu Rev Biophys Bioeng. 1975;4(00):311-34 PMID: 1098559
  4. A monoclonal antibody distinguishes two types of phosphatidylinositol 4-kinase.
    Biochem J. 1991 Jan 1;273(Pt 1):63-6 PMID: 1846531
  5. Crowding effects on diffusion in solutions and cells.
    Annu Rev Biophys. 2008;37:247-63 PMID: 18573081
  6. ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex.
    Nat Cell Biol. 1999 Sep;1(5):280-7 PMID: 10559940
  7. Heterospecies partition analysis reveals binding curve and stoichiometry of protein interactions in living cells.
    Proc Natl Acad Sci U S A. 2010 Mar 2;107(9):4117-22 PMID: 20142515
  8. Fluorescence correlation spectroscopy: past, present, future.
    Biophys J. 2011 Dec 21;101(12):2855-70 PMID: 22208184
  9. Palmitoylation controls the catalytic activity and subcellular distribution of phosphatidylinositol 4-kinase II{alpha}.
    J Biol Chem. 2009 Apr 10;284(15):9994-10003 PMID: 19211550
  10. Probing the endocytic pathway in live cells using dual-color fluorescence cross-correlation analysis.
    Biophys J. 2002 Aug;83(2):1184-93 PMID: 12124298
  11. Subcellular locations of phosphatidylinositol 4-kinase isoforms.
    J Biol Chem. 1997 May 16;272(20):13236-41 PMID: 9148941
  12. DNA-induced polymerization of HIV-1 integrase analyzed with fluorescence fluctuation spectroscopy.
    J Biol Chem. 2002 Oct 11;277(41):38045-52 PMID: 12147698
  13. The photon counting histogram in fluorescence fluctuation spectroscopy.
    Biophys J. 1999 Jul;77(1):553-67 PMID: 10388780
  14. Disruption of Golgi structure and function in mammalian cells expressing a mutant dynamin.
    J Cell Sci. 2000 Jun;113 ( Pt 11):1993-2002 PMID: 10806110
  15. Maintenance of hormone-sensitive phosphoinositide pools in the plasma membrane requires phosphatidylinositol 4-kinase IIIalpha.
    Mol Biol Cell. 2008 Feb;19(2):711-21 PMID: 18077555
  16. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation.
    J Cell Biol. 1994 Nov;127(4):915-34 PMID: 7962076
  17. Neuronal calcium sensor-1 and phosphatidylinositol 4-kinase beta stimulate extracellular signal-regulated kinase 1/2 signaling by accelerating recycling through the endocytic recycling compartment.
    Mol Biol Cell. 2006 Sep;17(9):4130-41 PMID: 16837555
  18. Observing protein interactions and their stoichiometry in living cells by brightness analysis of fluorescence fluctuation experiments.
    Methods Enzymol. 2010;472:345-63 PMID: 20580971
  19. Determining the stoichiometry of protein heterocomplexes in living cells with fluorescence fluctuation spectroscopy.
    Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3147-52 PMID: 17307882
  20. Localization of a highly active pool of type II phosphatidylinositol 4-kinase in a p97/valosin-containing-protein-rich fraction of the endoplasmic reticulum.
    Biochem J. 2003 Jul 1;373(Pt 1):57-63 PMID: 12650639
  21. Stabilization of phosphatidylinositol 4-kinase type IIbeta by interaction with Hsp90.
    J Biol Chem. 2011 Apr 8;286(14):12775-84 PMID: 21330372
  22. Phosphatidylinositol 4-kinases: old enzymes with emerging functions.
    Trends Cell Biol. 2006 Jul;16(7):351-61 PMID: 16793271
  23. Coordination of Golgi functions by phosphatidylinositol 4-kinases.
    Trends Cell Biol. 2011 Feb;21(2):113-21 PMID: 21282087
  24. A novel family of phosphatidylinositol 4-kinases conserved from yeast to humans.
    J Biol Chem. 2001 Mar 16;276(11):7705-8 PMID: 11244087
  25. Molecular characterisation of recombinant green fluorescent protein by fluorescence correlation microscopy.
    Biochem Biophys Res Commun. 1995 Dec 5;217(1):21-7 PMID: 8526912
  26. Fluorescence correlation spectroscopy studies of Peptide and protein binding to phospholipid vesicles.
    Biophys J. 2004 Aug;87(2):1044-53 PMID: 15298909
  27. Dual-color time-integrated fluorescence cumulant analysis.
    Biophys J. 2006 Oct 1;91(7):2687-98 PMID: 16815900
  28. Probing diffusion laws within cellular membranes by Z-scan fluorescence correlation spectroscopy.
    Biophys J. 2006 Aug 1;91(3):L23-5 PMID: 16751239
  29. Mammalian phosphatidylinositol 4-kinases.
    IUBMB Life. 2003 Feb;55(2):59-65 PMID: 12749687
  30. 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
  31. Phosphatidylinositol 4-kinase is required for endosomal trafficking and degradation of the EGF receptor.
    J Cell Sci. 2006 Feb 1;119(Pt 3):571-81 PMID: 16443754
  32. Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area.
    Int Rev Cytol. 2000;192:189-221 PMID: 10553280
  33. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi.
    Cell. 2003 Aug 8;114(3):299-310 PMID: 12914695
  34. Molecular determinants of activation and membrane targeting of phosphoinositol 4-kinase IIbeta.
    Biochem J. 2008 Jan 15;409(2):501-9 PMID: 17927563
  35. Observation volumes and {gamma}-factors in two-photon fluorescence fluctuation spectroscopy.
    Biophys J. 2005 Sep;89(3):2077-90 PMID: 15994890
  36. Probing protein oligomerization in living cells with fluorescence fluctuation spectroscopy.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15492-7 PMID: 14673112
  37. Heuristic statistical analysis of fluorescence fluctuation data with bright spikes: application to ligand binding to the human serotonin receptor expressed in Escherichia coli cells.
    Biol Chem. 2001 Mar;382(3):355-61 PMID: 11347881
  38. Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):3995-4000 PMID: 12646710
  39. Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion.
    Biophys J. 1997 Apr;72(4):1900-7 PMID: 9083693
  40. Relationship between phosphatidylinositol 4-phosphate synthesis, membrane organization, and lateral diffusion of PI4KIIalpha at the trans-Golgi network.
    J Lipid Res. 2010 Aug;51(8):2314-24 PMID: 20388919
  41. PIK1, an essential phosphatidylinositol 4-kinase associated with the yeast nucleus.
    EMBO J. 1994 May 15;13(10):2352-61 PMID: 8194527
  42. Fluorescence-intensity distribution analysis and its application in biomolecular detection technology.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13756-61 PMID: 10570145
  43. Molecular brightness determined from a generalized form of Mandel's Q-parameter.
    Biophys J. 2005 Nov;89(5):3531-47 PMID: 16143637
  44. Molecular brightness characterization of EGFP in vivo by fluorescence fluctuation spectroscopy.
    Biophys J. 2002 Jan;82(1 Pt 1):133-44 PMID: 11751302
  45. Type II phosphatidylinositol 4-kinase beta is a cytosolic and peripheral membrane protein that is recruited to the plasma membrane and activated by Rac-GTP.
    J Biol Chem. 2002 Nov 29;277(48):46586-93 PMID: 12324459
  46. Total internal reflection with fluorescence correlation spectroscopy.
    Nat Protoc. 2007;2(4):878-90 PMID: 17446873
  47. Dynamics of fluorescence marker concentration as a probe of mobility.
    Biophys J. 1976 Nov;16(11):1315-29 PMID: 974223
  48. Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments.
    J Biol Chem. 2002 May 31;277(22):20041-50 PMID: 11923287
  49. The effect of variable liposome brightness on quantifying lipid-protein interactions using fluorescence correlation spectroscopy.
    Biochim Biophys Acta. 2011 Oct;1808(10):2559-68 PMID: 21683682
  50. Differential evanescence nanometry: live-cell fluorescence measurements with 10-nm axial resolution on the plasma membrane.
    Biophys J. 2008 Mar 15;94(6):2333-42 PMID: 17993495
  51. Phosphatidylinositol 4-kinases.
    Eur J Biochem. 1998 Apr 15;253(2):357-70 PMID: 9654085
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
1542-0086
Published
2012-10-17
Epub
2012-00-16
Pages
1657-65
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC3475384
Subset
IM
Grants
NIGMS NIH HHS · GM091743 · United States
NIGMS NIH HHS · GM075401 · United States
NIGMS NIH HHS · P01 GM091743 · United States
NIGMS NIH HHS · R01 GM075401 · United States
NIGMS NIH HHS · GM64589 · United States
NIGMS NIH HHS · R01 GM064589 · 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]