Phosphoinositide Signaling
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1 Phosphoinositide Signaling Pietro De Camilli Department of Cell Biology Howard Hughes Medical Institute Program in Cellular Neuroscience, Neurodegeneration and Repair Yale University School of Medicine NIDA SAB meeting April 26, 2013
2 Phosphoinositides PtdIns PH domains Fyve domains PX domains etc.
3 Wendy Hill Membrane traffic in nerve terminals to cell body late endosomes synaptic vesicles endosomes
4 A cycle of PI(4,5)P2 synthesis and hydrolysis nested within the synaptic vesicle cycle PI 4-kinases PI4P 5-kinases (PIP kinase type 1γ) PI4P PI(4,5)P2 PI synaptojanin (PI(4,5)P2 phosphatase) PI(4,5)P2
5 A phosphoinositide code for cellular membranes PI4P PI(4,5)P 2 PI(3,5)P 2 PI3P PI(3,4)P 2 PI(3,4,5)P 3
6 Four PI 4-kinases in mammalian cells PI4-kinase IIIα (Stt4 in yeast) PI4-kinase IIIβ (Pik1 in yeast) PI4P PI(4,5)P 2 PI(3,5)P 2 PI3P PI(3,4)P 2 PI(3,4,5)P 3 PI4-kinase IIα & β (Lsb6 in yeast)
7 Stt4 is targeted to the plasma membrane in a complex with Efr3 and Ypp1 Yeast GFP-Stt4 PI4KIIIα Baird et al. (Emr lab), J Cell Biol 2008 Mammalian cell anti-pi4kiiiα Anti-PI4KIIIα immunoprecipitation Wong, (Cantley lab) J. Biol. Chem.1997
8 GFP-PI4KIIIα is cytosolic Based on the sequence reported in: Nakagawa, T., K. Goto, and H. Kondo Cloning, expression, and localization of 230-kDa phosphatidylinositol 4- kinase. J. Biol. Chem. 271 : Fubito Nakatsu
9 PI4KA (which encodes PI4KIIIα) had an incorrectly annotated translation start site M1 M1* likely the correct start site annotated start site recombinant endog. M1 M1* PI4KIIIα Fubito Nakatsu
10 ribosome Harringtonine mrna Ribosome footprinting after harringtonine treatment enabled determination of PI4KIIIα translational start sites Method in: Ingolia et al. (Weissman lab), Cell 2011 initiating ribosomes only Nuclease digestion M1 T* M1* Deep sequencing library collaboration with N. Ingolia s lab (Carnegie Institute)
11 EFR3B-Tomato GFP-PI4KIIIα TTC7B-GFP together alone A PI4KIIIα/EFR3/TTC7 complex as in yeast 2 µm 20 µm What is the function of this complex? Jeremy Baskin and Fubito Nakatsu
12 Conditional PI4KIIIα KO mice Germline gene disruption = embryonic lethality onditional KO crossed to CreER expressing mouse hen isolation of mouse embrynic fibroblasts (MEFs) + tamoxifen conditional PI4KIIIα MEFs Fubito Nakatsu
13 PI4KIIIα KO MEFs confirm central role of this kinasein plasma membrane PI4P synthesis No change in levels of other PI 4-kinases Decrease in total PI4P Decrease in PI4P at the plasma membrane but not at the Golgi apparatus Fubito Nakatsu
14 PI4KIIIα KO MEFs confirm central role of this kinasein plasma membrane PI4P synthesis Disruption of F-actin No change in levels of other PI 4-kinases Decrease in total PI4P Fubito Nakatsu
15 In PI4IIIα KO MEFs the drop of PI(4,5)P2 is much less robust than the loss of PI4P PI4P PI(4,5)P2 GFP-PH PLCγ Control compensatory increase of PI4P 5-kinases (Type 1 PIP kinases) 5 µm Fubito Nakatsu KO 20 µm PI(4,5)P2 decreases at plasma membrane but accumulates on cytoplasmic vesicles
16 In PI4IIIα KO cells PI4P 5-kinases are localized on internal vesicles rather than at the plasma membrane PI4P PI(4,5)P2 PI4P 5-kinase PI(4,5)P2 (PHPLCd) Wild type cell PI4IIIα KO cell Fubito Nakatsu
17 A phosphoinositide code for cellular membranes PI4P PI(4,5)P 2 PI(3,5)P 2 PI3P PI(3,4)P 2 PI(3,4,5)P 3 Can we by pass the problems intrinsic to genetic studies?long-term nature -> adaptive/compensatory changes
18 Light-induced protein heterodimerization
19 Optogenetic depletion of PI(4,5)P2 at the plasma membrane (blue light-mediated recruitment of a PI(4,5)P2 5-phosphatase) CAAX Idevall-Hagren et al. PNAS 2012
20 Optogenetic depletion of PI(4,5)P2 at the plasma membrane (blue light-mediated recruitment of a PI(4,5)P2 5-phosphatase) CAAX Movie Idevall-Hagren et al. PNAS 2012
21 PI(4,5)P2 hydrolysis upon blue light-induced inositol 5 -phosphatase recruitment Idevall-Hagren et al. PNAS 2012
22 Loss of K + currents upon blue light-induced inositol 5 -phosphatase recruitment KCNQ2/3 (Kv7.2/7.3) channels whole cell currents blue light (458 nm) 1s pulse of blue light (458 nm) > 95% current inhibition: t1/2 = 1.2 ± 0.3 s Recovery: t1/2 = 286 ± 33 s tsa-201 cells Eamonn Dickson, Bertil Hille Idevall-Hagren et al. PNAS 2012
23 Local blue light-illumination produces local effects and opposite effects at distant sites Focal PI(4,5)P2 depletion Movie PC12 cells Movie COS-7 cell Idevall-Hagren et al. PNAS 2012
24 Light-induced recruitment of PI 3-kinase to the plasma membrane and induction of ruffling mcherry-cry2-ish2 Movie COS-7 cells Idevall-Hagren et al. PNAS 2012
25 Using optogenetics to discover new biology
26 ER-plasma membrane contacts PDI PAG 10 m From Orci fibroblast PM neuron
27 The extended synaptotagmins: a family of proteins implicated in tethering the ER to the plasma membrane? E-Syt3 in neuron Giordano et al. Cell 2013
28 The extended synaptotagmins: a family of proteins implicated in tethering the ER to the plasma membrane? is PI(4,5)P2 needed to contact formation? Giordano et al. Cell 2013
29 Optogenetic depletion of PI(4,5)P2 dissociates E-Syt3 Movie irfp-ph-plcδ [PI(4,5)P2 biosensor] from the plasma membrane Movie E-Syt3-mCherry Loss of cortical ER induced by E-Syt3 overexpression as seen by EM Nucleus Nucleus PM PM Giordano et al. Cell 2013
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0 m m 0. m cm mm 00 µm 0 µm 00 nm 0 nm Human height Length of some nerve and muscle cells Chicken egg Frog egg Most plant and animal cells Most bacteria Smallest bacteria Viruses Proteins Unaided eye Light
Type of file: PDF Title of file for HTML: Supplementary Information Description: Supplementary Figures
Type of file: PDF Title of file for HTML: Supplementary Information Description: Supplementary Figures Type of file: MOV Title of file for HTML: Supplementary Movie 1 Description: NLRP3 is moving along
Human height. Length of some nerve and muscle cells. Chicken egg. Frog egg. Most plant and animal cells Nucleus Most bacteria Mitochondrion
10 m 1 m 0.1 m 1 cm Human height Length of some nerve and muscle cells Chicken egg Unaided eye 1 mm Frog egg 100 µm 10 µm 1 µm 100 nm 10 nm Most plant and animal cells Nucleus Most bacteria Mitochondrion
Plasma membranes. Plasmodesmata between plant cells. Gap junctions between animal cells Cell junctions. Cell-cell recognition
Cell Communication Cell Signaling Cell-to-cell communication is essential for multicellular organisms Communicate by chemical messengers Animal and plant cells have cell junctions that directly connect