Segregation of PIP2 and PIP3 into Distinct Nanoscale Regions Within the Plasma Membrane

Overview

Journal Biol Open

Specialty Biology

Date 2012 Dec 6

PMID 23213479

Citations 88

Authors

Jie Wang

David A Richards

Affiliations

Soon will be listed here.

Abstract

PIP(2) and PIP(3) are implicated in a wide variety of cellular signaling pathways at the plasma membrane. We have used STORM imaging to localize clusters of PIP(2) and PIP(3) to distinct nanoscale regions within the plasma membrane of PC12 cells. With anti-phospholipid antibodies directly conjugated with AlexaFluor 647, we found that PIP(2) clusters in membrane domains of 64.5±27.558 nm, while PIP(3) clusters had a size of 125.6±22.408 nm. With two color direct STORM imaging we show that >99% of phospholipid clusters have only one or other phospholipid present. These results indicate that lipid nano-domains can be readily identified using super-resolution imaging techniques, and that the lipid composition and size of clusters is tightly regulated.

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References

Huang B, Babcock H, Zhuang X . Breaking the diffraction barrier: super-resolution imaging of cells. Cell. 2010; 143(7):1047-58. PMC: 3272504. DOI: 10.1016/j.cell.2010.12.002. View

Corbin J, Dirkx R, Falke J . GRP1 pleckstrin homology domain: activation parameters and novel search mechanism for rare target lipid. Biochemistry. 2004; 43(51):16161-73. PMC: 3625374. DOI: 10.1021/bi049017a. View

Miao B, Skidan I, Yang J, You Z, Fu X, Famulok M . Inhibition of cell migration by PITENINs: the role of ARF6. Oncogene. 2011; 31(39):4317-32. PMC: 3310973. DOI: 10.1038/onc.2011.593. View

Sieber J, Willig K, Kutzner C, Gerding-Reimers C, Harke B, Donnert G . Anatomy and dynamics of a supramolecular membrane protein cluster. Science. 2007; 317(5841):1072-6. DOI: 10.1126/science.1141727. View

Brown D, Rose J . Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 1992; 68(3):533-44. DOI: 10.1016/0092-8674(92)90189-j. View

Wang Y, Collins A, Guo L, Smith-Dupont K, Gai F, Svitkina T . Divalent cation-induced cluster formation by polyphosphoinositides in model membranes. J Am Chem Soc. 2012; 134(7):3387-95. PMC: 3445022. DOI: 10.1021/ja208640t. View

Pike L . The challenge of lipid rafts. J Lipid Res. 2008; 50 Suppl:S323-8. PMC: 2674732. DOI: 10.1194/jlr.R800040-JLR200. View

Maffucci T, Raimondi C, Abu-Hayyeh S, Dominguez V, Sala G, Zachary I . A phosphoinositide 3-kinase/phospholipase Cgamma1 pathway regulates fibroblast growth factor-induced capillary tube formation. PLoS One. 2009; 4(12):e8285. PMC: 2788267. DOI: 10.1371/journal.pone.0008285. View

Hein B, Willig K, Hell S . Stimulated emission depletion (STED) nanoscopy of a fluorescent protein-labeled organelle inside a living cell. Proc Natl Acad Sci U S A. 2008; 105(38):14271-6. PMC: 2538451. DOI: 10.1073/pnas.0807705105. View

10.

Lee A, Birdsall N, Metcalfe J, Toon P, Warren G . Clusters in lipid bilayers and the interpretation of thermal effects in biological membranes. Biochemistry. 1974; 13(18):3699-705. DOI: 10.1021/bi00715a013. View

11.

Pike L . Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J Lipid Res. 2006; 47(7):1597-8. DOI: 10.1194/jlr.E600002-JLR200. View

12.

Goebbels S, Oltrogge J, Kemper R, Heilmann I, Bormuth I, Wolfer S . Elevated phosphatidylinositol 3,4,5-trisphosphate in glia triggers cell-autonomous membrane wrapping and myelination. J Neurosci. 2010; 30(26):8953-64. PMC: 6632897. DOI: 10.1523/JNEUROSCI.0219-10.2010. View

13.

van den Bogaart G, Meyenberg K, Risselada H, Amin H, Willig K, Hubrich B . Membrane protein sequestering by ionic protein-lipid interactions. Nature. 2011; 479(7374):552-5. PMC: 3409895. DOI: 10.1038/nature10545. View

14.

Manley S, Gillette J, Patterson G, Shroff H, Hess H, Betzig E . High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods. 2008; 5(2):155-7. DOI: 10.1038/nmeth.1176. View

15.

Singer S, Nicolson G . The fluid mosaic model of the structure of cell membranes. Science. 1972; 175(4023):720-31. DOI: 10.1126/science.175.4023.720. View

16.

Insall R, Weiner O . PIP3, PIP2, and cell movement--similar messages, different meanings?. Dev Cell. 2001; 1(6):743-7. PMC: 2819114. DOI: 10.1016/s1534-5807(01)00086-7. View

17.

Vanhaesebroeck B, Leevers S, Ahmadi K, Timms J, Katso R, Driscoll P . Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem. 2001; 70:535-602. DOI: 10.1146/annurev.biochem.70.1.535. View

18.

Menager C, Arimura N, Fukata Y, Kaibuchi K . PIP3 is involved in neuronal polarization and axon formation. J Neurochem. 2004; 89(1):109-18. DOI: 10.1046/j.1471-4159.2004.02302.x. View

19.

Paolo G, De Camilli P . Phosphoinositides in cell regulation and membrane dynamics. Nature. 2006; 443(7112):651-7. DOI: 10.1038/nature05185. View

20.

McLaughlin S, Murray D . Plasma membrane phosphoinositide organization by protein electrostatics. Nature. 2005; 438(7068):605-11. DOI: 10.1038/nature04398. View