Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate - PubMed (original) (raw)
. 2013 Jul 11;499(7457):233-7.
doi: 10.1038/nature12360. Epub 2013 Jul 3.
Marielle Eichhorn-Gruenig, Dmytro Puchkov, Johannes Schöneberg, Alexander Ullrich, André Lampe, Rainer Müller, Sirus Zarbakhsh, Federico Gulluni, Emilio Hirsch, Michael Krauss, Carsten Schultz, Jan Schmoranzer, Frank Noé, Volker Haucke
Affiliations
- PMID: 23823722
- DOI: 10.1038/nature12360
Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate
York Posor et al. Nature. 2013.
Abstract
Phosphoinositides serve crucial roles in cell physiology, ranging from cell signalling to membrane traffic. Among the seven eukaryotic phosphoinositides the best studied species is phosphatidylinositol-4,5-bisphosphate (PI(4,5)P2), which is concentrated at the plasma membrane where, among other functions, it is required for the nucleation of endocytic clathrin-coated pits. No phosphatidylinositol other than PI(4,5)P2 has been implicated in clathrin-mediated endocytosis, whereas the subsequent endosomal stages of the endocytic pathway are dominated by phosphatidylinositol-3-phosphates(PI(3)P). How phosphatidylinositol conversion from PI(4,5)P2-positive endocytic intermediates to PI(3)P-containing endosomes is achieved is unclear. Here we show that formation of phosphatidylinositol-3,4-bisphosphate (PI(3,4)P2) by class II phosphatidylinositol-3-kinase C2α (PI(3)K C2α) spatiotemporally controls clathrin-mediated endocytosis. Depletion of PI(3,4)P2 or PI(3)K C2α impairs the maturation of late-stage clathrin-coated pits before fission. Timed formation of PI(3,4)P2 by PI(3)K C2α is required for selective enrichment of the BAR domain protein SNX9 at late-stage endocytic intermediates. These findings provide a mechanistic framework for the role of PI(3,4)P2 in endocytosis and unravel a novel discrete function of PI(3,4)P2 in a central cell physiological process.
Comment in
- Cell biology: Lipid switches and traffic control.
Schmid SL, Mettlen M. Schmid SL, et al. Nature. 2013 Jul 11;499(7457):161-2. doi: 10.1038/nature12408. Epub 2013 Jul 3. Nature. 2013. PMID: 23823719 No abstract available.
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References
- J Biol Chem. 2007 Sep 21;282(38):28226-36 - PubMed
- J Biol Chem. 2005 Dec 9;280(49):40766-72 - PubMed
- Dev Cell. 2009 Dec;17(6):811-22 - PubMed
- Biochem J. 1997 Aug 15;326 ( Pt 1):139-47 - PubMed
- EMBO J. 2007 Nov 14;26(22):4788-800 - PubMed
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