Acyl-chain saturation regulates the order of phosphatidylinositol 4,5-bisphosphate nanodomains.
Journal
Communications chemistry
ISSN: 2399-3669
Titre abrégé: Commun Chem
Pays: England
ID NLM: 101725670
Informations de publication
Date de publication:
29 Nov 2021
29 Nov 2021
Historique:
received:
16
05
2021
accepted:
10
11
2021
entrez:
25
1
2023
pubmed:
29
11
2021
medline:
29
11
2021
Statut:
epublish
Résumé
Phosphatidylinositol 4,5-bisphosphate (PI(4,5)P
Identifiants
pubmed: 36697613
doi: 10.1038/s42004-021-00603-1
pii: 10.1038/s42004-021-00603-1
pmc: PMC9814227
doi:
Types de publication
Journal Article
Langues
eng
Pagination
164Informations de copyright
© 2021. The Author(s).
Références
Monteiro, M. E., Sarmento, M. J. & Fernandes, F. Role of calcium in membrane interactions by PI(4,5)P2-binding proteins. Biochem. Soc. Trans. 42, 1441–6 (2014).
pubmed: 25233429
doi: 10.1042/BST20140149
Di Paolo, G. & De Camilli, P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651–657 (2006).
pubmed: 17035995
doi: 10.1038/nature05185
Koch, M. & Holt, M. Coupling exo- and endocytosis: an essential role for PIP2 at the synapse. Biochim. Biophys. Acta 1821, 1114–1132 (2012).
pubmed: 22387937
doi: 10.1016/j.bbalip.2012.02.008
Martin, T. F. J. in Subcellular Biochemistry Vol. 59, 111–130 (Springer New York, 2012).
dos Remedios, C. G. & Nosworthy, N. J. in Actin-Binding Proteins and Disease 290–297, https://doi.org/10.1007/978-0-387-71749-4_12 (Springer New York, 2008).
Suh, B.-C. & Hille, B. PIP 2 is a necessary cofactor for ion channel function: how and why? Annu. Rev. Biophys. 37, 175–195 (2008).
pubmed: 18573078
pmcid: 2692585
doi: 10.1146/annurev.biophys.37.032807.125859
Mücksch, F. et al. Quantification of phosphoinositides reveals strong enrichment of PIP2 in HIV-1 compared to producer cell membranes. Sci. Rep. 9, 17661 (2019).
pubmed: 31776383
pmcid: 6881329
doi: 10.1038/s41598-019-53939-z
Bertin, A. et al. Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J. Mol. Biol. 404, 711–731 (2010).
pubmed: 20951708
pmcid: 3005623
doi: 10.1016/j.jmb.2010.10.002
Mandal, K. Review of PIP2 in cellular signaling, functions and diseases. Int. J. Mol. Sci. 21, 8342 (2020).
pmcid: 7664428
doi: 10.3390/ijms21218342
Sarmento, M. J., Coutinho, A., Fedorov, A., Prieto, M. & Fernandes, F. Ca2+ induces PI(4,5)P2 clusters on lipid bilayers at physiological PI(4,5)P2 and Ca2+ concentrations. Biochim. Biophys. Acta 1838, 822–830 (2014).
pubmed: 24316170
doi: 10.1016/j.bbamem.2013.11.020
Rauch, M. E., Ferguson, C. G., Prestwich, G. D. & Cafiso, D. S. Myristoylated alanine-rich C kinase substrate (MARCKS) sequesters spin-labeled phosphatidylinositol 4,5-bisphosphate in lipid bilayers. J. Biol. Chem. 277, 14068–14076 (2002).
pubmed: 11825894
doi: 10.1074/jbc.M109572200
Wang, J. et al. Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions. J. Biol. Chem. 277, 34401–34412 (2002).
pubmed: 12097325
doi: 10.1074/jbc.M203954200
Wen, Y., Vogt, V. M. & Feigenson, G. W. Multivalent cation-bridged PI(4,5)P2 clusters form at very low concentrations. Biophys. J. 114, 2630–2639 (2018).
pubmed: 29874613
pmcid: 6129474
doi: 10.1016/j.bpj.2018.04.048
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)P2 and PI(4,5)P2. Langmuir 33, 12463–12477 (2017).
pubmed: 28961003
doi: 10.1021/acs.langmuir.7b00666
Bozelli, J. C. & Epand, R. M. Specificity of acyl chain composition of phosphatidylinositols. Proteomics 19, 1900138 (2019).
doi: 10.1002/pmic.201900138
De Craene, J.-O., Bertazzi, D., Bär, S. & Friant, S. Phosphoinositides, major actors in membrane trafficking and lipid signaling pathways. Int. J. Mol. Sci. 18, 634 (2017).
pmcid: 5372647
doi: 10.3390/ijms18030634
D’Souza, K. & Epand, R. M. Enrichment of phosphatidylinositols with specific acyl chains. Biochim. Biophys. Acta 1838, 1501–1508 (2014).
pubmed: 24120446
doi: 10.1016/j.bbamem.2013.10.003
Hicks, A. M., DeLong, C. J., Thomas, M. J., Samuel, M. & Cui, Z. Unique molecular signatures of glycerophospholipid species in different rat tissues analyzed by tandem mass spectrometry. Biochim. Biophys. Acta 1761, 1022–1029 (2006).
pubmed: 16860597
doi: 10.1016/j.bbalip.2006.05.010
Traynor-Kaplan, A. et al. Fatty-acyl chain profiles of cellular phosphoinositides. Biochim. Biophys. Acta 1862, 513–522 (2017).
pmcid: 5392126
doi: 10.1016/j.bbalip.2017.02.002
Manni, M. M. et al. Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage. Elife 7, e34394 (2018).
Mujalli, A. et al. Profiling of phosphoinositide molecular species in human and mouse platelets identifies new species increasing following stimulation. Biochim. Biophys. Acta 1863, 1121–1131 (2018).
doi: 10.1016/j.bbalip.2018.06.009
Koizumi, A. et al. Increased fatty acyl saturation of phosphatidylinositol phosphates in prostate cancer progression. Sci. Rep. 9, 13257 (2019).
Saad, J. S. et al. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl Acad. Sci. USA 103, 11364–9 (2006).
pubmed: 16840558
pmcid: 1544092
doi: 10.1073/pnas.0602818103
James, D. J., Khodthong, C., Kowalchyk, J. A. & Martin, T. F. J. Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. J. Cell Biol. 182, 355–366 (2008).
pubmed: 18644890
pmcid: 2483516
doi: 10.1083/jcb.200801056
Mu, L. et al. A phosphatidylinositol 4,5-bisphosphate redistribution-based sensing mechanism initiates a phagocytosis programing. Nat. Commun. 9, 4259 (2018).
pubmed: 30323235
pmcid: 6189171
doi: 10.1038/s41467-018-06744-7
Tadross, M. R., Tsien, R. W. & Yue, D. T. Ca2+ channel nanodomains boost local Ca
pubmed: 24019485
pmcid: 3785779
doi: 10.1073/pnas.1313898110
Lakowicz, J. R. Principles of Fluorescence Spectroscopy (Springer, 2006).
Attwood, S., Choi, Y. & Leonenko, Z. Preparation of DOPC and DPPC supported planar lipid bilayers for atomic force microscopy and atomic force spectroscopy. Int. J. Mol. Sci. 14, 3514–3539 (2013).
pubmed: 23389046
pmcid: 3588056
doi: 10.3390/ijms14023514
do Canto, A. M. T. M. et al. Diphenylhexatriene membrane probes DPH and TMA-DPH: a comparative molecular dynamics simulation study. Biochim. Biophys. Acta 1858, 2647–2661 (2016).
pubmed: 27475296
doi: 10.1016/j.bbamem.2016.07.013
Shrivastava, S., Paila, Y. D., Dutta, A. & Chattopadhyay, A. Differential effects of cholesterol and its immediate biosynthetic precursors on membrane organization. Biochemistry 47, 5668–5677 (2008).
pubmed: 18442257
doi: 10.1021/bi8001677
Marsh, D. Handbook of Lipid Bilayers (CRC, 2013).
Sklar, L. A. The partition of cis-parinaric acid and trans-parinaric acid among aqueous, fluid lipid, and solid lipid phases. Mol. Cell. Biochem. 32, 169–177 (1980).
pubmed: 7007869
doi: 10.1007/BF00227444
Florine, K. I. & Feigenson, G. W. Influence of the calcium-induced gel phase on the behavior of small molecules in phosphatidylserine and phosphatidylserine–phosphatidylcholine multilamellar vesicles. Biochemistry 26, 1757–1768 (1987).
pubmed: 3036210
doi: 10.1021/bi00380a039
Marrink, S. J., Risselada, H. J., Yefimov, S. & Tieleman, D. P. & De Vries, A. H. The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B 111, 7812–7824 (2007).
pubmed: 17569554
doi: 10.1021/jp071097f
Alessandri, R. et al. Pitfalls of the Martini Model. J. Chem. Theory Comput. 15, 5448–5460 (2019).
pubmed: 31498621
pmcid: 6785803
doi: 10.1021/acs.jctc.9b00473
Koynova, R. & Caffrey, M. Phases and phase transitions of the phosphatidylcholines. Biochim. Biophys. Acta 1376, 91–145 (1998).
pubmed: 9666088
doi: 10.1016/S0304-4157(98)00006-9
Nagle, J. F. & Tristram-Nagle, S. Structure of lipid bilayers. Biochim. Biophys. Acta 1469, 159–95 (2000).
pubmed: 11063882
pmcid: 2747654
doi: 10.1016/S0304-4157(00)00016-2
Lin, X. et al. Roles of PIP2 in the membrane binding of MIM I-BAR: insights from molecular dynamics simulations. FEBS Lett. 592, 2533–2542 (2018).
pubmed: 29995324
doi: 10.1002/1873-3468.13186
Marrink, S. J., Risselada, J. & Mark, A. E. Simulation of gel phase formation and melting in lipid bilayers using a coarse grained model. Chem. Phys. Lipids 135, 223–244 (2005).
pubmed: 15921980
doi: 10.1016/j.chemphyslip.2005.03.001
Carpenter, T. S. et al. Capturing phase behavior of ternary lipid mixtures with a refined Martini coarse-grained force field. J. Chem. Theory Comput. 14, 6050–6062 (2018).
pubmed: 30253091
doi: 10.1021/acs.jctc.8b00496
Mayer, L. D., Hope, M. J. & Cullis, P. R. Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim. Biophys. Acta 858, 161–168 (1986).
pubmed: 3707960
doi: 10.1016/0005-2736(86)90302-0
Weinberger, A. et al. Gel-assisted formation of giant unilamellar vesicles. Biophys. J. 105, 154–164 (2013).
pubmed: 23823234
pmcid: 3699747
doi: 10.1016/j.bpj.2013.05.024
Sarmento, M. J., Prieto, M. & Fernandes, F. Reorganization of lipid domain distribution in giant unilamellar vesicles upon immobilization with different membrane tethers. Biochim. Biophys. Acta 1818, 2605–2615 (2012).
pubmed: 22664063
doi: 10.1016/j.bbamem.2012.05.028
Loura, L. M. S., Fedorov, A. & Prieto, M. Partition of membrane probes in a gel/fluid two-component lipid system: a fluorescence resonance energy transfer study. Biochim. Biophys. Acta 1467, 101–112 (2000).
pubmed: 10930513
doi: 10.1016/S0005-2736(00)00211-X
El Kirat, K., Morandat, S. & Dufrêne, Y. F. Nanoscale analysis of supported lipid bilayers using atomic force microscopy. Biochim. Biophys. Acta 1798, 750–765 (2010).
pubmed: 19664999
doi: 10.1016/j.bbamem.2009.07.026
Franquelim, H. G., Gaspar, D., Veiga, A. S., Santos, N. C. & Castanho, M. A. R. B. Decoding distinct membrane interactions of HIV-1 fusion inhibitors using a combined atomic force and fluorescence microscopy approach. Biochim. Biophys. Acta 1828, 1777–1785 (2013).
pubmed: 23500616
doi: 10.1016/j.bbamem.2013.03.006
Chopinet, L., Formosa, C., Rols, M. P., Duval, R. E. & Dague, E. Imaging living cells surface and quantifying its properties at high resolution using AFM in QI
pubmed: 23522742
doi: 10.1016/j.micron.2013.02.003
Smolyakov, G., Formosa-Dague, C., Severac, C., Duval, R. E. & Dague, E. High speed indentation measures by FV, QI and QNM introduce a new understanding of bionanomechanical experiments. Micron 85, 8–14 (2016).
pubmed: 27023832
doi: 10.1016/j.micron.2016.03.002
Aufderhorst-Roberts, A., Chandra, U. & Connell, S. D. Three-phase coexistence in lipid membranes. Biophys. J. 112, 313–324 (2017).
pubmed: 28122217
pmcid: 5266263
doi: 10.1016/j.bpj.2016.12.025
Hutter, J. L. & Bechhoefer, J. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64, 1868–1873 (1993).
doi: 10.1063/1.1143970
López, C. A., Sovova, Z., van Eerden, F. J., de Vries, A. H. & Marrink, S. J. Martini force field parameters for glycolipids. J. Chem. Theory Comput. 9, 1694–1708 (2013).
pubmed: 26587629
doi: 10.1021/ct3009655
Martini Coarse Grain Forcefield for Biomolecules. http://cgmartini.nl/ . (2021).
Abraham, M. J. et al. Gromacs: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2, 19–25 (2015).
doi: 10.1016/j.softx.2015.06.001
Wassenaar, T. A., Ingólfsson, H. I., Böckmann, R. A., Tieleman, D. P. & Marrink, S. J. Computational lipidomics with insane: a versatile tool for generating custom membranes for molecular simulations. J. Chem. Theory Comput. 11, 2144–2155 (2015).
pubmed: 26574417
doi: 10.1021/acs.jctc.5b00209
De Jong, D. H., Baoukina, S., Ingólfsson, H. I. & Marrink, S. J. Martini straight: boosting performance using a shorter cutoff and GPUs. Comput. Phys. Commun. 199, 1–7 (2016).
doi: 10.1016/j.cpc.2015.09.014
Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101 (2007).
pubmed: 17212484
doi: 10.1063/1.2408420
Parrinello, M. & Rahman, A. Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52, 7182–7190 (1981).
doi: 10.1063/1.328693
Michaud-Agrawal, N., Denning, E. J., Woolf, T. B. & Beckstein, O. MDAnalysis: a toolkit for the analysis of molecular dynamics simulations. J. Comput. Chem. 32, 2319–2327 (2011).
pubmed: 21500218
pmcid: 3144279
doi: 10.1002/jcc.21787
Pérez, F. & Granger, B. E. IPython: A System for Interactive Scientific Computing. www.python.org . (2007).
Harris, C. R. et al. Array programming with NumPy. Nature 585, 357–362 (2020).
pubmed: 32939066
pmcid: 7759461
doi: 10.1038/s41586-020-2649-2
Virtanen, P. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat. Methods 17, 261–272 (2020).
pubmed: 32015543
pmcid: 7056644
doi: 10.1038/s41592-019-0686-2
Fabian, P. et al. Scikit-learn: machine learning in Python. J. Machine Learn. Res. 12 http://scikit-learn.sourceforge.net . (2011).
Hunter, J. D. Matplotlib: a 2D graphics environment. Comput. Sci. Eng. 9, 90–95 (2007).
doi: 10.1109/MCSE.2007.55
Salfer, M., Collado, J. F., Baumeister, W., FernándezBusnadiego, R. & Martínez-Sánchez, A. Reliable estimation of membrane curvature for cryo-electron tomography. PLoS Comput. Biol. 16, e1007962 (2020).
pubmed: 32776920
pmcid: 7444595
doi: 10.1371/journal.pcbi.1007962
Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33–38 (1996).
pubmed: 8744570
doi: 10.1016/0263-7855(96)00018-5