Cell-sized asymmetric lipid vesicles facilitate the investigation of asymmetric membranes

Nature Chemistry

Volumn 8, Issue 9, 2016, Pages 881-889

  Kamiya, Koki ^a,b   Kawano, Ryuji ^a,e   Osaki, Toshihisa ^a,c   Akiyoshi, Kazunari ^d   Takeuchi, Shoji ^a,c  

^a KANAGAWA ACADEMY OF SCIENCE AND TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c INSTITUTE OF INDUSTRIAL SCIENCE   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1,2-DIOLEOYLPHOSPHATIDYLSERINE; 1,2-OLEOYLPHOSPHATIDYLCHOLINE; ALKANE; BACTERIOCIN; CONNEXIN 43; CYCLOPEPTIDE; DECANE; DIPALMITOYLPHOSPHATIDYLCHOLINE; FLUORESCENT DYE; LANTHIOPEPTIN; LIPOSOME; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE; RHODAMINE;

CHEMISTRY; LIPID BILAYER; PARTICLE SIZE;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; ALKANES; BACTERIOCINS; CONNEXIN 43; FLUORESCENT DYES; LIPID BILAYERS; PARTICLE SIZE; PEPTIDES, CYCLIC; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLSERINES; RHODAMINES; UNILAMELLAR LIPOSOMES;

EID: 84984620247     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.2537     Document Type: Article

References (42)

1. Bacia, K., Schwille, P. & Kurzchalia, T. Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. Proc. Natl Acad. Sci. USA 102, 3272-3277 (2005).
2. Kaneda, M. et al. Direct formation of proteo-liposomes by in vitro synthesis and cellular cytosolic delivery with connexin-expressing liposomes. Biomaterials 30, 3971-3977 (2009).
3. Kamiya, K., Tsumoto, K., Yoshimura, T. & Akiyoshi, K. Cadherin-integrated liposomes with potential application in a drug delivery system. Biomaterials 32, 9899-9907 (2011).
4. Kurihara, K. et al. Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nature Chem. 3, 775-781 (2011).
5. Matosevic, M. Synthesizing artificial cells from giant unilamellar vesicles: state-of-the art in the development of microfluidic technology. Bioessays 34, 992-1001 (2012).
6. Pautot, S., Frisken, B. J. & Weitz, D. A. Engineering asymmetric vesicles. Proc. Natl Acad. Sci. USA 100, 10718-10721 (2003).
7. Hu, P. C., Li, S. & Malmstadt, N. Microfluidic fabrication of asymmetric giant lipid vesicles. ACS Appl. Mater. Interfaces 3, 1434-1440 (2011).
8. Funakoshi, K., Suzuki, H. & Takeuchi, S. Formation of giant lipid vesicle like compartments from a planar lipid membrane by a pulsed jet flow. J. Am. Chem. Soc. 129, 12608-12609 (2007).
9. Richmond, D. L. et al. Forming giant vesicles with controlled membrane composition, asymmetry, and contents. Proc. Natl Acad. Sci. USA 108, 9431-9436 (2011).
10. Arriaga, L. R. et al. Ultrathin shell double emulsion templated giant unilamellar lipid vesicles with controlled microdomain formation. Small 10, 950-956 (2014).
11. van Swaay, D. & de Mello, A. Microfluidic methods for forming liposomes. Lab. Chip 13, 752-767 (2013).
12. Devaux, P. F., Herrmann, A., Ohlwein, N. & Kozlov, M. M. How lipid flippases can modulate membrane structure. Biochim. Biophys. Acta 1778, 1591-1600 (2008).
13. Hanson, P. K. & Nichols, J. W. Energy-dependent flip of fluorescence-labeled phospholipids is regulated by nutrient starvation and transcription factors, PDR1 and PDR3. J. Biol. Chem. 276, 9861-9867 (2001).
14. Uchida, K., Emoto, K., Daleke, D. L., Inoue, K. & Umeda, M. Induction of apoptosis by phosphatidylserine. J. Biochem. 123, 1073-1078 (1998).
15. Funakoshi, K., Suzuki, H. & Takeuchi, S. Lipid bilayer formation by contacting monolayers in a microfluidic device for membrane protein analysis. Anal. Chem. 78, 8169-8174 (2006).
16. Kawano, R. et al. Automated parallel recording of topologically identified single ion channels. Sci. Rep. 3, 1995 (2013).
17. Hagedorn, J. G., Martys, N. S. & Douglas, J. F. Breakup of a fluid thread in a confined geometry: droplet-plug transition, perturbation sensitivity, and kinetic stabilization with confinement. Phys. Rev. E 69, 056312 (2004).
18. Ogl?cka, K., Rangmani, P., Liedberg, B., Kraut, R. S. & Parikh, A. N. Oscillatory phase separation in giant lipid vesicles induced by transmembrane osmotic differentials. eLIFE 3, e03695 (2014).
19. Bangham, A. D. & Home, R. W. Negative staining of phospholipids and their structural modification by surface-active agents as observed in the electron microscope. J. Mol. Biol. 8, 660-668 (1964).
20. Reeves, J. P. & Dowben, R. M. Formation and properties of thin-walled phospholipid vesicles. J. Cell Physiol. 73, 49-60 (1969).
21. Tsuji, Y. et al. Droplet split-and-contact method for high-throughput transmembrane electrical recording. Anal. Chem. 85, 10913-10919 (2013).
22. Cherney, D. P., Conboy, J. C. & Harris, J. M. Optical-trapping Raman microscopy detection of single unilamellar lipid vesicles. Anal. Chem. 75, 6621-6628 (2003).
23. Ota, S., Yoshizawa, S. & Takeuchi, S. Microfluidic formation of monodisperse, cell-sized, and unilamellar vesicles. Angew. Chem. Int. Ed. 48, 6533-6537 (2009).
24. Rodrigues, N., Pincet, F. & Cribier, S. Giant vesicles formed by gentle hydration and electroformation: a comparison by fluorescence microscopy. Colloids Surf. B 42, 125-130 (2005).
25. van Engeland, M., Nieland, L. J., Ramaekers, F. C., Schutte, B. & Reutelingsperger, C. P. Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31, 1-9 (1998).
26. Chan, A., Reiter, R., Wiese, S., Fertig, G. & Gold, R. Plasma membrane phospholipid asymmetry precedes DNA fragmentation in different apoptotic cell models. Histochem. Cell Biol. 110, 553-558 (1998).
27. Matsuzaki, K., Murase, O., Fujii, N. & Miyajima, K. An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 35, 11361-11368 (1996).
28. Bai, J. & Pagano, R. E. Measurement of spontaneous transfer and transbilayer movement of BODIPY-labeled lipids in lipid vesicles. Biochemistry 36, 8840-8848 (1997).
29. Kornberg, R. D. & McConnell, H. M. Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry 10, 1111-1120 (1971).
30. Qian, S. Structure and Mechanism of Peptide-induced Membrane Pores (ProQuest, UMI Dissertation Publishing, 2011).
31. Makino, A. et al. Cinnamycin (Ro 09-0198) promotes cell binding and toxicity by inducing transbilayer lipid movement. J. Biol. Chem. 278, 3204-3209 (2003).
32. Iwamoto, K. et al. Curvature-dependent recognition of ethanolamine phospholipids by duramycin and cinnamycin. Biophys. J. 93, 1608-1619 (2007).
33. Guder, A., Wiedemann, I. & Sahl, H. G. Posttranslationally modified bacteriocins-the lantibiotics. Biopolymers 55, 62-73 (2000).
34. Liu, Y. J., Hansen, G. P., Venancio-Marques, A. & Baigl, D. Cell-free preparation of functional and triggerable giant proteoliposomes. ChemBioChem 14, 2243-2247 (2013).
35. Kumar, N. M. & Gilula, N. B. The gap junction communication channel. Cell 84, 381-388 (1996).
36. John, S. A., Kondo, R., Wang, S. Y., Goldhaber, J. I. & Weiss, J. N. Connexin-43 hemichannels opened by metabolic inhibition. J. Biol. Chem. 274, 236-240 (1999).
37. Uhríková, D. et al. Small-angle neutron scattering study of n-decane effect on the bilayer thickness in extruded unilamellar dioleoylphosphatidylcholine liposomes. Biophys. Chem. 88, 165-170 (2000).
38. Sasanuma, Y. Conformational analysis of chain molecules in liquid crystalline phases by a rotational isomeric state scheme with maximum entropy method I. 1H-1H dipolar couplings from n-alkanes dissolved in a nematic solvent. Polymer J. 32, 883-889 (2000).
39. van Meer, G., Voelker, D R. & Feigenson, G. W. Membrane lipids: where they are and how they behave. Nature Rev. Mol. Cell Biol. 9, 112-124 (2008).
40. von Heijne, G. Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature 341, 456-458 (1989).
41. Hartmann, E., Rapoport, T. A. & Lodish, H. F. Predicting the orientation of eukaryotic membrane-spanning proteins. Proc. Natl Acad. Sci. USA 86, 5786-5790 (1989).
42. Dowhan, W. & Bogdanov, M. Lipid-dependent membrane protein topogenesis. Annu. Rev. Biochem. 78, 515-540 (2009).