Controlled Peptide-Mediated Vesicle Fusion Assessed by Simultaneous Dual-Colour Time-Lapsed Fluorescence Microscopy.
Cholesterol
/ chemistry
Color
Dimerization
Fluorescence Resonance Energy Transfer
Lipids
/ chemistry
Lipopeptides
/ chemistry
Membrane Fusion
Microscopy, Confocal
Microscopy, Fluorescence
/ methods
Peptides
/ chemistry
Polysorbates
/ chemistry
Spectrometry, Fluorescence
Unilamellar Liposomes
/ chemistry
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
20 02 2020
20 02 2020
Historique:
received:
17
09
2019
accepted:
31
01
2020
entrez:
22
2
2020
pubmed:
23
2
2020
medline:
31
12
2020
Statut:
epublish
Résumé
We have employed a model system, inspired by SNARE proteins, to facilitate membrane fusion between Giant Unilamellar Vesicles (GUVs) and Large Unilamellar Vesicles (LUVs) under physiological conditions. In this system, two synthetic lipopeptide constructs comprising the coiled-coil heterodimer-forming peptides K
Identifiants
pubmed: 32080270
doi: 10.1038/s41598-020-59926-z
pii: 10.1038/s41598-020-59926-z
pmc: PMC7033240
doi:
Substances chimiques
Lipids
0
Lipopeptides
0
Peptides
0
Polysorbates
0
Unilamellar Liposomes
0
Cholesterol
97C5T2UQ7J
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3087Références
Ma, M., Paredes, A. & Bong, D. Intra- and intermembrane pairwise molecular recognition between synthetic hydrogen-bonding phospholipids. J. Am. Chem. Soc. 130, 14456–14458, https://doi.org/10.1021/ja806954u (2008).
doi: 10.1021/ja806954u
pubmed: 18850702
Chan, Y. H. M., van Lengerich, B. & Boxer, S. G. Lipid-anchored DNA mediates vesicle fusion as observed by lipid and content mixing. Biointerphases 3, FA17–FA21, https://doi.org/10.1116/1.2889062 (2008).
doi: 10.1116/1.2889062
pubmed: 20408664
Jumeaux, C. et al. MicroRNA Detection by DNA-Mediated Liposome Fusion. Chembiochem 19, 434–438, https://doi.org/10.1002/cbic.201700592 (2018).
doi: 10.1002/cbic.201700592
pubmed: 29333674
pmcid: 5861668
Meng, Z. J. et al. Efficient Fusion of Liposomes by Nucleobase Quadruple-Anchored DNA. Chem. Eur. J. 23, 9391–9396, https://doi.org/10.1002/chem.201701379 (2017).
doi: 10.1002/chem.201701379
pubmed: 28513997
Ries, O., Loffler, P. M. G., Rabe, A., Malavan, J. J. & Vogel, S. Efficient liposome fusion mediated by lipid-nucleic acid conjugates. Org. Biomol. Chem. 15, 8936–8945, https://doi.org/10.1039/C7OB01939D (2017).
doi: 10.1039/C7OB01939D
pubmed: 29043358
Stengel, G., Zahn, R. & Hook, F. DNA-induced programmable fusion of phospholipid vesicles. J. Am. Chem. Soc. 129, 9584–9585, https://doi.org/10.1021/ja073200k (2007).
doi: 10.1021/ja073200k
pubmed: 17629277
Chan, Y. H. M., van Lengerich, B. & Boxer, S. G. Effects of linker sequences on vesicle fusion mediated by lipid-anchored DNA oligonucleotides. P. Natl. Acad. Sci. USA 106, 979–984, https://doi.org/10.1073/pnas.0812356106 (2009).
doi: 10.1073/pnas.0812356106
Flavier, K. M. & Boxer, S. G. Vesicle Fusion Mediated by Solanesol-Anchored DNA. Biophysical Journal 113, 1260–1268, https://doi.org/10.1016/j.bpj.2017.05.034 (2017).
doi: 10.1016/j.bpj.2017.05.034
pubmed: 28647061
pmcid: 5607041
Loffler, P. M. G. et al. A DNA-Programmed Liposome Fusion Cascade. Angew. Chem. Int. Ed. 56, 13228–13231, https://doi.org/10.1002/anie.201703243 (2017).
doi: 10.1002/anie.201703243
Xu, W., Wang, J., Rothman, J. E. & Pincet, F. Accelerating SNARE-Mediated Membrane Fusion by DNA–Lipid Tethers. Angew. Chem. Int. Ed. 54, 14388–14392, https://doi.org/10.1002/anie.201506844 (2015).
doi: 10.1002/anie.201506844
Noonan, P. S., Mohan, P., Goodwin, A. P. & Schwartz, D. K. DNA Hybridization-Mediated Liposome Fusion at the Aqueous Liquid Crystal Interface. Adv. Funct. Mater. 24, 3206–3212, https://doi.org/10.1002/adfm.201303885 (2014).
doi: 10.1002/adfm.201303885
pubmed: 25506314
pmcid: 4262931
Lygina, A. S., Meyenberg, K., Jahn, R. & Diederichsen, U. Transmembrane Domain Peptide/Peptide Nucleic Acid Hybrid as a Model of a SNARE Protein in Vesicle Fusion. Angew. Chem. Int. Ed. 50, 8597–8601, https://doi.org/10.1002/anie.201101951 (2011).
doi: 10.1002/anie.201101951
Rabe, A., Loffler, P. M. G., Ries, O. & Vogel, S. Programmable fusion of liposomes mediated by lipidated PNA. Chem. Commun. 53, 11921–11924, https://doi.org/10.1039/C7CC06058K (2017).
doi: 10.1039/C7CC06058K
Muheeb, S., Daniel, B., Dragomir, M., Reinhard, J. & Ulf, D. Distance Regulated Vesicle Fusion and Docking Mediated by β-Peptide Nucleic Acid SNARE Protein Analogues. Chem. Bio. Chem. 17, 479–485, https://doi.org/10.1002/cbic.201500517 (2016).
doi: 10.1002/cbic.201500517
Ayumi, K., Kiyomi, M., Toshihisa, M. & Toshiki, T. Construction of a pH-Responsive Artificial Membrane Fusion System by Using Designed Coiled-Coil Polypeptides. Chem-Eur. J. 14, 7343–7350, https://doi.org/10.1002/chem.200701726 (2008).
doi: 10.1002/chem.200701726
Kashiwada, A. et al. Design and Characterization of Endosomal-pH-Responsive Coiled Coils for Constructing an Artificial Membrane Fusion System. Chem-Eur. J. 17, 6179–6186, https://doi.org/10.1002/chem.201003392 (2011).
doi: 10.1002/chem.201003392
pubmed: 21503987
Meyenberg, K., Lygina, A. S., van den Bogaart, G., Jahn, R. & Diederichsen, U. SNARE derived peptide mimic inducing membrane fusion. Chem. Commun. 47, 9405–9407, https://doi.org/10.1039/c1cc12879e (2011).
doi: 10.1039/c1cc12879e
Skyttner, C., Enander, K., Aronsson, C. & Aili, D. Tuning Liposome Membrane Permeability by Competitive Coiled Coil Heterodimerization and Heterodimer Exchange. Langmuir 34, 6529–6537, https://doi.org/10.1021/acs.langmuir.8b00592 (2018).
doi: 10.1021/acs.langmuir.8b00592
pubmed: 29758162
Gong, Y., Luo, Y. M. & Bong, D. Membrane activation: Selective vesicle fusion via small molecule recognition. J. Am. Chem. Soc. 128, 14430–14431, https://doi.org/10.1021/ja0644576 (2006).
doi: 10.1021/ja0644576
pubmed: 17090005
Kashiwada, A., Tsuboi, M. & Matsuda, K. Target-selective vesicle fusion induced by molecular recognition on lipid bilayers. Chem. Commun. 695–697, https://doi.org/10.1039/b815688c (2009).
Kashiwada, A., Yamane, I., Tsuboi, M., Ando, S. & Matsuda, K. Design, Construction, and Characterization of High-Performance Membrane Fusion Devices with Target-Selectivity. Langmuir 28, 2299–2305, https://doi.org/10.1021/la2038075 (2012).
doi: 10.1021/la2038075
pubmed: 22204500
Whitehead, S. A. et al. Artificial Membrane Fusion Triggered by Strain-Promoted Alkyne-Azide Cycloaddition. Bioconjug. Chem. 28, 923–932, https://doi.org/10.1021/acs.bioconjchem.6600578 (2017).
doi: 10.1021/acs.bioconjchem.6600578
pubmed: 28248084
pmcid: 5990007
Valérie, M.-A. et al. Selective Adhesion, Lipid Exchange and Membrane-Fusion Processes between Vesicles of Various Sizes Bearing Complementary Molecular Recognition Groups. ChemPhysChem 2, 367–376, doi:10.1002/1439-7641(20010618)2:6<367::AID-CPHC367>3.0.CO;2-# (2001).
Litowski, J. R. & Hodges, R. S. Designing heterodimeric two-stranded alpha-helical coiled-coils: the effect of chain length on protein folding, stability and specificity. J. Pept. Res. 58, 477–492, https://doi.org/10.1034/j.1399-3011.2001.10972.x (2001).
doi: 10.1034/j.1399-3011.2001.10972.x
pubmed: 12005418
Marsden, H. R., Elbers, N. A., Bomans, P. H. H., Sommerdijk, N. & Kros, A. A Reduced SNARE Model for Membrane Fusion. Angew. Chem. Int. Ed. 48, 2330–2333, https://doi.org/10.1002/anie.200804493 (2009).
doi: 10.1002/anie.200804493
Zheng, T. T. et al. A non-zipper-like tetrameric coiled coil promotes membrane fusion. RSC Advances 6, 7990–7998, https://doi.org/10.1039/c5ra26175a (2016).
doi: 10.1039/c5ra26175a
Zheng, T. T. et al. Controlling the rate of coiled coil driven membrane fusion. Chem. Commun. 49, 3649–3651, https://doi.org/10.1039/c3cc38926j (2013).
doi: 10.1039/c3cc38926j
Daudey, G. A., Zope, H. R., Voskuhl, J., Kros, A. & Boyle, A. L. Membrane-Fusogen Distance Is Critical for Efficient Coiled-Coil-Peptide-Mediated Liposome Fusion. Langmuir 33, 12443–12452, https://doi.org/10.1021/acs.langmuir.7b02931 (2017).
doi: 10.1021/acs.langmuir.7b02931
pubmed: 28980816
pmcid: 5666511
Crone, N. S. A., Minnee, D., Kros, A. & Boyle, A. L. Peptide-Mediated Liposome Fusion: The Effect of Anchor Positioning. Int. J. Mol. Sci. 19, https://doi.org/10.3390/ijms19010211 (2018).
doi: 10.3390/ijms19010211
Versluis, F., Dominguez, J., Voskuhl, J. & Kros, A. Coiled-coil driven membrane fusion: zipper-like vs. non-zipper-like peptide orientation. Faraday Discuss. 166, 349–359, https://doi.org/10.1039/c3fd00061c (2013).
doi: 10.1039/c3fd00061c
pubmed: 24611287
Versluis, F. et al. In Situ Modification of Plain Liposomes with Lipidated Coiled Coil Forming Peptides Induces Membrane Fusion. J. Am. Chem. Soc. 135, 8057–8062, https://doi.org/10.1021/ja4031227 (2013).
doi: 10.1021/ja4031227
pubmed: 23659206
Mora, N. L. et al. Targeted anion transporter delivery by coiled-coil driven membrane fusion. Chem. Sci. 7, 1768–1772, https://doi.org/10.1039/c5sc04282h (2016).
doi: 10.1039/c5sc04282h
pubmed: 28936326
pmcid: 5592372
Yang, J. et al. Drug Delivery via Cell Membrane Fusion Using Lipopeptide Modified Liposomes. ACS Cent. Sci. 2, 621–630, https://doi.org/10.1021/acscentsci.6b00172 (2016).
doi: 10.1021/acscentsci.6b00172
pubmed: 27725960
pmcid: 5043431
Yang, J. et al. Application of Coiled Coil Peptides in Liposomal Anticancer Drug Delivery Using a Zebrafish Xenograft Model. ACS Nano 10, 7428–7435, https://doi.org/10.1021/acsnano.6b01410 (2016).
doi: 10.1021/acsnano.6b01410
pubmed: 27504667
Kong, L., Askes, S. H., Bonnet, S., Kros, A. & Campbell, F. Temporal Control of Membrane Fusion through Photolabile PEGylation of Liposome Membranes. Angew. Chem. Int. Ed. 55, 1396–1400, https://doi.org/10.1002/anie.201509673 (2016).
doi: 10.1002/anie.201509673
Yoon, T. Y., Okumus, B., Zhang, F., Shin, Y. K. & Ha, T. Multiple intermediates in SNARE-induced membrane fusion. Proc. Natl. Acad. Sci. USA 103, 19731–19736, https://doi.org/10.1073/pnas.0606032103 (2006).
doi: 10.1073/pnas.0606032103
pubmed: 17167056
Karatekin, E. et al. A fast, single-vesicle fusion assay mimics physiological SNARE requirements. Proc. Natl. Acad. Sci. USA 107, 3517–3521, https://doi.org/10.1073/pnas.0914723107 (2010).
doi: 10.1073/pnas.0914723107
pubmed: 20133592
Kyoung, M. et al. In vitro system capable of differentiating fast Ca2+-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release. Proc. Natl. Acad. Sci. USA 108, E304–313, https://doi.org/10.1073/pnas.1107900108 (2011).
doi: 10.1073/pnas.1107900108
pubmed: 21705659
Bowen, M. E., Weninger, K., Brunger, A. T. & Chu, S. Single molecule observation of liposome-bilayer fusion thermally induced by soluble N-ethyl maleimide sensitive-factor attachment protein receptors (SNAREs). Biophys. J. 87, 3569–3584, https://doi.org/10.1529/biophysj.104.048637 (2004).
doi: 10.1529/biophysj.104.048637
pubmed: 15347585
pmcid: 1304822
Tareste, D., Shen, J., Melia, T. J. & Rothman, J. E. SNAREpin/Munc18 promotes adhesion and fusion of large vesicles to giant membranes. Proc. Natl. Acad. Sci. USA 105, 2380–2385, https://doi.org/10.1073/pnas.0712125105 (2008).
doi: 10.1073/pnas.0712125105
pubmed: 18268324
Witkowska, A. & Jahn, R. Rapid SNARE-Mediated Fusion of Liposomes and Chromaffin Granules with Giant Unilamellar Vesicles. Biophys. J. 113, 1251–1259, https://doi.org/10.1016/j.bpj.2017.03.010 (2017).
doi: 10.1016/j.bpj.2017.03.010
pubmed: 28400045
pmcid: 5607038
van den Bogaart, G. et al. Membrane protein sequestering by ionic protein–lipid interactions. Nature 479, 552, https://doi.org/10.1038/nature10545 (2011).
doi: 10.1038/nature10545
pubmed: 22020284
pmcid: 3409895
Kuhlmann, J. W., Junius, M., Diederichsen, U. & Steinem, C. SNARE-Mediated Single-Vesicle Fusion Events with Supported and Freestanding Lipid Membranes. Biophys. J. 112, 2348–2356, https://doi.org/10.1016/j.bpj.2017.04.032 (2017).
doi: 10.1016/j.bpj.2017.04.032
pubmed: 28591607
pmcid: 5474721
Etzerodt, T. P., Trier, S., Henriksen, J. R. & Andresen, T. L. A GALA lipopeptide mediates pH- and membrane charge dependent fusion with stable giant unilamellar vesicles. Soft Matter 8, 5933–5939, https://doi.org/10.1039/c2sm25075f (2012).
doi: 10.1039/c2sm25075f
Kahya, N., Pecheur, E. I., de Boeij, W. P., Wiersma, D. A. & Hoekstra, D. Reconstitution of membrane proteins into giant unilamellar vesicles via peptide-induced fusion. Biophys. J. 81, 1464–1474, https://doi.org/10.1016/S0006-3495(01)75801-8 (2001).
doi: 10.1016/S0006-3495(01)75801-8
pubmed: 11509360
pmcid: 1301625
Mora, N. L. et al. Preparation of size tunable giant vesicles from cross-linked dextran(ethylene glycol) hydrogels. Chem. Commun. 50, 1953–1955, https://doi.org/10.1039/c3cc49144g (2014).
doi: 10.1039/c3cc49144g
Koukalova, A. et al. Distinct roles of SNARE-mimicking lipopeptides during initial steps of membrane fusion. Nanoscale 10, 19064–19073, https://doi.org/10.1039/c8nr05730c (2018).
doi: 10.1039/c8nr05730c
pubmed: 30288507
Rabe, M., Schwieger, C., Zope, H. R., Versluis, F. & Kros, A. Membrane Interactions of Fusogenic Coiled-Coil Peptides: Implications for Lipopeptide Mediated Vesicle Fusion. Langmuir 30, 7724–7735, https://doi.org/10.1021/la500987c (2014).
doi: 10.1021/la500987c
pubmed: 24914996
Rabe, M. et al. A Coiled-Coil Peptide Shaping Lipid Bilayers upon Fusion. Biophys. J. 111, 2162–2175, https://doi.org/10.1016/j.bpj.2016.10.010 (2016).
doi: 10.1016/j.bpj.2016.10.010
pubmed: 27851940
pmcid: 5113151
Walde, P., Cosentino, K., Engel, H. & Stano, P. Giant Vesicles: Preparations and Applications. Chembiochem 11, 848–865, https://doi.org/10.1002/cbic.201000010 (2010).
doi: 10.1002/cbic.201000010
pubmed: 20336703
Larsen, J., Hatzakis, N. S. & Stamou, D. Observation of Inhomogeneity in the Lipid Composition of Individual Nanoscale Liposomes. J. Am. Chem. Soc. 133, 10685–10687, https://doi.org/10.1021/ja203984j (2011).
doi: 10.1021/ja203984j
pubmed: 21688773
Apellániz, B., Nieva, J. L., Schwille, P. & García-Sáez, A. J. All-or-None versus Graded: Single-Vesicle Analysis Reveals Lipid Composition Effects on Membrane Permeabilization. Biophys. J. 99, 3619–3628, https://doi.org/10.1016/j.bpj.2010.09.027 (2010).
doi: 10.1016/j.bpj.2010.09.027
pubmed: 21112286
pmcid: 2998612
Lohse, B., Bolinger, P.-Y. & Stamou, D. Encapsulation Efficiency Measured on Single Small Unilamellar Vesicles. J. Am. Chem. Soc. 130, 14372–14373, https://doi.org/10.1021/ja805030w (2008).
doi: 10.1021/ja805030w
pubmed: 18842043
Mortensen, K. I., Tassone, C., Ehrlich, N., Andresen, T. L. & Flyvbjerg, H. How To Characterize Individual Nanosize Liposomes with Simple Self-Calibrating Fluorescence Microscopy. Nano Lett. 18, 2844–2851, https://doi.org/10.1021/acs.nanolett.7b05312 (2018).
doi: 10.1021/acs.nanolett.7b05312
pubmed: 29614230
Otten, D., Brown, M. F. & Beyer, K. Softening of Membrane Bilayers by Detergents Elucidated by Deuterium NMR Spectroscopy. J. Phys. Chem. B 104, 12119–12129, https://doi.org/10.1021/jp001505e (2000).
doi: 10.1021/jp001505e
Krielgaard, L. et al. Effect of tween 20 on freeze-thawing- and agitation-induced aggregation of recombinant human factor XIII. J. Pharm. Sci. 87, 1597–1603, https://doi.org/10.1021/js980126i (1998).
doi: 10.1021/js980126i
Benda, A. et al. How to determine diffusion coefficients in planar phospholipid systems by confocal fluorescence correlation spectroscopy. Langmuir 19, 4120–4126, https://doi.org/10.1021/la0270136 (2003).
doi: 10.1021/la0270136
Kessel, A., Ben-Tal, N. & May, S. Interactions of cholesterol with lipid bilayers: The preferred configuration and fluctuations. Biophys. J. 81, 643–658, https://doi.org/10.1016/S0006-3495(01)75729-3 (2001).
doi: 10.1016/S0006-3495(01)75729-3
pubmed: 11463613
pmcid: 1301541
Mora, N. L. et al. Evaluation of dextran(ethylene glycol) hydrogel films for giant unilamellar lipid vesicle production and their application for the encapsulation of polymersomes. Soft Matter 13, 5580–5588, https://doi.org/10.1039/c7sm00551b (2017).
doi: 10.1039/c7sm00551b
pubmed: 28730206
pmcid: 5586486
Struck, D. K., Hoekstra, D. & Pagano, R. E. Use of Resonance Energy-Transfer to Monitor Membrane-Fusion. Biochemistry 20, 4093–4099, https://doi.org/10.1021/bi00517a023 (1981).
doi: 10.1021/bi00517a023
pubmed: 7284312
Stryer, L. & Haugland, R. P. Energy transfer: a spectroscopic ruler. Proc. Natl. Acad. Sci. USA 58, 719–726, https://doi.org/10.1073/pnas.58.2.719 (1967).
doi: 10.1073/pnas.58.2.719
pubmed: 5233469
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675, https://doi.org/10.1038/nmeth.2089 (2012).
doi: 10.1038/nmeth.2089
pubmed: 5554542
pmcid: 5554542