Structure and Lateral Organization of Phosphatidylinositol 4,5-bisphosphate
"> Figure 1
<p>Membrane processes associated with or dependent on phosphatidylinositol 4,5-bisphosphate (PI(4,5)P<sub>2</sub>). Figure created with BioRender.com.</p> "> Figure 2
<p>PI(4,5)P2 headgroup features. The PI(4,5)P<sub>2</sub> headgroup consists of <span class="html-italic">myo</span>-inositol ring where every hydroxyl substituent is at the equatorial position except for the hydroxyl in the position 2 of the ring, which is in an axial position. In the case of PIP2, the hydroxyls in positions 4 and 5 are enzymatically phosphorylated. It is linked to the diacylglycerol (DAG) backbone via a phosphodiester bond in position 1 (<b>A</b>). At pH 7.0, one of the phosphodiester proton dissociates, and the one remaining is shared between the two vicinal phosphomonoester groups. In terms of potential charge this means that, at pH 7.0, the charges would be −1.58 and −1.41 for the phosphomonoester groups at positions 4 and 5, respectively [<a href="#B19-molecules-25-03885" class="html-bibr">19</a>]. The lower charge of the 5-phosphomonoester group is attributed to a network of intramolecular hydrogen bonds that it is engaged in, which stabilize the proton (<b>B</b>). Carbon atoms are colored in grey, hydrogen in white, oxygen in red, and phosphorus in orange. Snapshots obtained from a simulation of a bilayer consisting of 95:5 mol ratio 1-palmitoyl-2-oleoyl-<span class="html-italic">sn</span>-glycero-3-phosphocholine (POPC): PI(4,5)P2, using the CHARMM36m forcefield run in GROMACS2019. Images were modeled using VMD.</p> "> Figure 3
<p>Examples of PI(4,5)P<sub>2</sub> headgroup tilt when inserted into a phospholipid membrane. PI(4,5)P<sub>2</sub> presents a significant headgroup tilt, when inserted into a bilayer, ranging from almost parallel to the membrane plane (<b>A</b>) to a more conservative ~40° tilt (<b>B</b>). Whilst the more dramatic headgroup tilt appears to be favored from interactions between its negatively charged phosphate groups and the positively charged membrane surface, the more moderate tilt surges from the establishment of intramolecular hydrogen bonds between the C2 hydroxyl and the pro-R-oxygen of the phosphodiester phosphate. Carbon atoms are colored in grey, hydrogen in white, oxygen in red, and phosphorus in orange. Snapshots obtained from a simulation of a bilayer consisting of 95:5 mol ratio POPC: PI(4,5)P<sub>2</sub>, using the CHARMM36m forcefield run in GROMACS2019. Images were modeled using VMD.</p> "> Figure 4
<p>Snapshots of calcium ions interacting with the PI(4,5)P<sub>2</sub> headgroup phosphates. Calcium can bind to PI(4,5)P<sub>2</sub> either solely near the 4-phophomonoester (<b>A</b>) or in between the phosphomonoester groups (<b>B</b>). However, simultaneous binding between the two phosphomonoester groups is approximately 10 kcal/mol more unfavorable [<a href="#B31-molecules-25-03885" class="html-bibr">31</a>]. Carbon atoms are colored in grey, hydrogen in white, oxygen in red, phosphorus in orange, and calcium in blue. Snapshots obtained from a simulation of a bilayer consisting of 95:5 mol ratio POPC: PI(4,5)P<sub>2</sub> in the presence of calcium in a 5:1 calcium to PI(4,5)P<sub>2</sub> ratio, using the CHARMM36m forcefield run in GROMACS2019. Images were modeled using VMD.</p> "> Figure 5
<p>Snapshots of experiments on mixed lipid monolayers, containing different mol % of 1-stearoyl-2-oleoyl-<span class="html-italic">sn</span>-glycero-3-phosphocholine (SOPC) and PI(4,5)P2, while exposed to calcium. Reprinted from Biophysical Journal, 101, Ellenbroek, W.G.; Wang, Y.H.; Christian, D.A.; Discher, D.E.; Janmey, P.A.; Liu, A.J. Divalent cation-dependent formation of electrostatic PIP2 clusters in lipid monolayers. 2178–2184, Copyright (2011), with permission from Elsevier [<a href="#B69-molecules-25-03885" class="html-bibr">69</a>].</p> "> Figure 6
<p>Crosslinking of PI(4,5)P<sub>2</sub> lipids induces the formation of PI(4,5)P<sub>2</sub> nanodomains. As a single divalent cation can bind up to 2 PI(4,5)P<sub>2</sub> lipids and each lipid can potentially bind 3 divalent cations, a network of electrostatic interactions can crosslink PI(4,5)P<sub>2</sub> lipids together (<b>A</b>). As the number of clustered lipids increases, PI(4,5)P<sub>2</sub> nanodomains are formed (<b>B</b>). Coarse grain beads representing the inositol headgroup and acyl-chains are colored in grey, the glycerol component in red, the phosphate groups in orange, and calcium in blue. Snapshots obtained from a simulation of a bilayer consisting of 95:5 mol ratio POPC: PI(4,5)P<sub>2</sub> in the presence of calcium in a 5:1 calcium to PI(4,5)P<sub>2</sub> ratio, using the martini 2.2 coarse-grained forcefield run in GROMACS2019. Images were modeled using VMD.</p> "> Figure 7
<p>Ternary diagram for the POPC:PSM:Chol lipid mixture at 25 °C (<b>A</b>) and 37 °C (<b>B</b>). Color-code depicts decrease in measured fluorescence anisotropies of a PI(4,5)P<sub>2</sub> fluorescent analog (TF-PI(4,5)P<sub>2</sub>) upon inclusion of 100 µM Ca<sup>2+</sup>. Since the decrease reflects homo-FRET between analogs incorporated within the same clusters, darker areas correspond to more efficient PI(4,5)P<sub>2</sub> clustering. Adapted with permission from Sarmento, M.J.; Coutinho, A.; Fedorov, A.; Prieto, M.; Fernandes, F. Membrane order is a key regulator of divalent cation-induced clustering of PI(3,5)P<sub>2</sub> and PI(4,5)P<sub>2</sub>. Langmuir 2017, 33, 12463–12477 [<a href="#B78-molecules-25-03885" class="html-bibr">78</a>]. Copyright (2017) American Chemical Society.</p> ">
Abstract
:1. Introduction
2. The Phosphoinositide Family
3. PI(4,5)P2 Structure
3.1. Headgroup Conformation
3.2. Membrane Conformation Dynamics
3.3. Headgroup Charge
3.4. Acyl-Chain Composition
4. Lateral Organization of PI(4,5)P2
4.1. Sequestration by Proteins
4.2. PI(4,5)P2 Interactions with Divalent Cations
4.3. Effect of Cholesterol on PI(4,5)P2 Properties and Distribution
4.4. Effect of the Cytoskeleton and Curvature on PI(4,5)P2 Lateral Organization
5. Concluding Remarks
Funding
Conflicts of Interest
References
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Borges-Araújo, L.; Fernandes, F. Structure and Lateral Organization of Phosphatidylinositol 4,5-bisphosphate. Molecules 2020, 25, 3885. https://doi.org/10.3390/molecules25173885
Borges-Araújo L, Fernandes F. Structure and Lateral Organization of Phosphatidylinositol 4,5-bisphosphate. Molecules. 2020; 25(17):3885. https://doi.org/10.3390/molecules25173885
Chicago/Turabian StyleBorges-Araújo, Luís, and Fabio Fernandes. 2020. "Structure and Lateral Organization of Phosphatidylinositol 4,5-bisphosphate" Molecules 25, no. 17: 3885. https://doi.org/10.3390/molecules25173885