Triggering and visualizing the aggregation and fusion of lipid membranes in microfluidic chambers

Biophysical Journal

Volumn 91, Issue 1, 2006, Pages 233-243

  Estes, Daniel J ^a   Lopez, Santiago R ^a   Fuller, A Oveta ^a,b   Mayer, Michael ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; LIPOSOME; MACROGOL; PEPTIDE; RECEPTOR PROTEIN;

ARTICLE; CELL AGGREGATION; HERPES SIMPLEX VIRUS; HOST CELL; LIPID MEMBRANE; MEMBRANE FUSION; MICROFLUIDIC ANALYSIS; MICROMANIPULATOR; PEPTIDE ANALYSIS; PROTEIN AGGREGATION; TRIGGER POINT;

SIMPLEXVIRUS;

EID: 33745739450     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.076398     Document Type: Article

References (82)

1. Chen, E. H., and E. N. Olson. 2005. Unveiling the mechanisms of cell-cell fusion. Science. 308:369-373.
2. Fujii, G. 1999. To fuse or not to fuse: the effects of electrostatic interactions, hydrophobic forces, and structural amphiphilicity on protein-mediated membrane destabilization. Adv. Drug Deliv. Rev. 38:257-277.
3. Gennis, R. B. 1989. Biomembranes: molecular structure and function. C. R. Cantor, editor. Springer-Verlag, New York. 533.
4. Kemble, G. W., T. Danieli, and J. M. White. 1994. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell. 76:383-391.
5. Cevc, G., and H. Richardsen. 1999. Lipid vesicles and membrane fusion. Adv. Drug Deliv. Rev. 38:207-232.
6. Jahn, R., T. Lang, and T. C. Sudhof. 2003. Membrane fusion. Cell. 112:519-533.
7. Tamm, L. K., J. Crane, and V. Kiessling. 2003. Membrane fusion: a structural perspective on the interplay of lipids and proteins. Curr. Opin. Struct. Biol. 13:453-466.
8. Bentz, J. 2000. Membrane fusion mediated by coiled coils: a hypothesis. Biophys. J. 78:886-900.
9. Smith, A. E., and A. Helenius. 2004. How viruses enter animal cells. Science. 304:237-242.
10. Lee, J., and B. R. Lentz. 1997. Evolution of lipidic structures during model membrane fusion and the relation of this process to cell membrane fusion. Biochemistry. 36:6251-6259.
11. Lentz, B. R., and J. K. Lee. 1999. Poly(ethylene glycol) (PEG)-mediated fusion between pure lipid bilayers: a mechanism in common with viral fusion and secretory vesicle release? (Review). Mol. Membr. Biol. 16:279-296.
12. Chernomordik, L. V., G. B. Melikyan, and Y. A. Chizmadzhev. 1987. Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim. Biophys. Acta. 906:309-352.
13. Weber, T., B. V. Zemelman, J. A. McNew, B. Westermann, M. Gmachl, F. Parlati, T. H. Sollner, and J. E. Rothman. 1998. SNAREpins: minimal machinery for membrane fusion. Cell. 92:759-772.
14. Cohen, F. S., M. H. Akabas, and A. Finkelstein. 1982. Osmotic swelling of phospholipid-vesicles causes them to fuse with a planar phospholipid-bilayer membrane. Science. 217:458-460.
15. Cohen, F. S., J. Zimmerberg, and A. Finkelstein. 1980. Fusion of phospholipid-vesicles with planar phospholipid-bilayer membranes. 2. Incorporation of a vesicular membrane marker into the planar membrane. J. Gen. Physiol. 75:251-270.
16. Helm, C. A., J. N. Israelachvili, and P. M. McGuiggan. 1992. Role of hydrophobic forces in bilayer adhesion and fusion. Biochemistry. 31:1794-1805.
17. Tanaka, T., and M. Yamazaki. 2004. Membrane fusion of giant unilamellar vesicles of neutral phospholipid membranes induced by La3+. Langmuir. 20:5160-5164.
18. Nir, S., J. Bentz, J. Wilschut, and N. Duzgunes. 1983. Aggregation and fusion of phospholipid-vesicles. Prog. Surf. Sci. 13:1-124.
19. Bentz, J., D. Alford, J. Cohen, and N. Duzgunes. 1988. La-3+-induced fusion of phosphatidylserine liposomes-close approach, intermembrane intermediates, and the electrostatic surface-potential. Biophys. J. 53:593-607.
20. Lee, J., and B. R. Lentz. 1998. Secretory and viral fusion may share mechanistic events with fusion between curved lipid bilayers. Proc. Natl. Acad. Sci. USA. 95:9274-9279.
21. Munro, J. C., and C. W. Frank. 2004. In situ formation and characterization of poly(ethylene glycol)-supported lipid bilayers on gold surfaces. Langmuir. 20:10567-10575.
22. Zimmermann, U. 1982. Electric field-mediated fusion and related electrical phenomena. Biochim. Biophys. Acta. 694:227-277.
23. Bentz, J., and N. Duzgunes. 1985. Fusogenic capacities of divalent-cations and effect of liposome size. Biochemistry. 24:5436-5443.
24. Wilschut, J., N. Duzgunes, and D. Papahadjopoulos. 1981. Calcium-magnesium specificity in membrane-fusion - kinetics of aggregation and fusion of phosphatidylserine vesicles and the role of bilayer curvature. Biochemistry. 20:3126-3133.
25. Ohki, S. 1984. Effects of divalent-cations, temperature, osmotic-pressure gradient, and vesicle curvature on phosphatidylserine vesicle fusion. J. Membr. Biol. 77:265-275.
26. Lentz, B. R., G. F. McIntyre, D. J. Parks, J. C. Yates, and D. Massenburg. 1992. Bilayer Curvature and Certain Amphipaths promote poly(ethylene glycol)-induced fusion of dipalmitoylphosphatidylcholine unilamellar vesicles. Biochemistry. 31:2643-2653.
27. Evans, K. O., and B. R. Lentz. 2002. Kinetics of lipid rearrangements during poly(ethylene glycol)-mediated fusion of highly curved unilamellar vesicles. Biochemistry. 41:1241-1249.
28. Duzgunes, N., T. M. Allen, J. Fedor, and D. Papahadjopoulos. 1987. Lipid mixing during membrane aggregation and fusion - why fusion assays disagree. Biochemistry. 26:8435-8442.
29. Ellens, H., J. Bentz, and F. C. Szoka. 1985. H+-Induced and Ca-2+-induced fusion and destabilization of liposomes. Biochemistry. 24:3099-3106.
30. Wilschut, J., and D. Papahadjopoulos. 1979. Ca2+-induced fusion of phospholipid-vesicles monitored by mixing of aqueous contents. Nature. 281:690-692.
31. Trivedi, V. D., C. Yu, B. Veeramuthu, S. Francis, and D. K. Chang. 2000. Fusion induced aggregation of model vesicles studied by dynamic and static light scattering. Chem. Phys. Lipids. 107:99-106.
32. Murata, M., S. Takahashi, S. Kagiwada, A. Suzuki, and S. Ohnishi. 1992. Ph-dependent membrane-fusion and vesiculation of phospholipid large unilamellar vesicles induced by amphiphilic anionic and cationic peptides. Biochemistry. 31:1986-1992.
33. Siegel, D. P., J. L. Burns, M. H. Chestnut, and Y. Talmon. 1989. Intermediates in membrane-fusion and bilayer nonbilayer phase-transitions imaged by time-resolved cryo-transmission electron-microscopy. Biophys. J. 56:161-169.
34. Nomura, F., T. Inaba, S. Ishikawa, M. Nagata, S. Takahashi, H. Hotani, and K. Takiguchi. 2004. Microscopic observations reveal that fusogenic peptides induce liposome shrinkage prior to membrane fusion. Proc. Natl. Acad. Sci. USA. 101:3420-3425.
35. Soltesz, S. A., and D. A. Hammer. 1997. Lysis of large unilamellar vesicles induced by analogs of the fusion peptide of influenza virus hemagglutinin. J. Colloid Interface Sci. 186:399-409.
36. Soltesz, S. A., and D. A. Hammer. 1995. Micropipette manipulation technique for the monitoring of pH-dependent membrane lysis as induced by the fusion peptide of influenza-virus. Biophys. J. 68:315-325.
37. Akashi, K., H. Miyata, H. Itoh, and K. Kinosita. 1996. Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope. Biophys. J. 71:3242-3250.
38. Shoemaker, S. D., and T. K. Vanderlick. 2002. Intramembrane electrostatic interactions destabilize lipid vesicles. Biophys. J. 83:2007-2014.
39. Heuvingh, J., F. Pincet, and S. Cribier. 2004. Hemifusion and fusion of giant vesicles induced by reduction of inter-membrane distance. Eur. Phys. J. E. Soft Matter. 14:269-276.
40. Lei, G. H., and R. C. MacDonald. 2003. Lipid bilayer vesicle fusion: intermediates captured by high-speed microfluorescence spectroscopy. Biophys. J. 85:1585-1599.
41. Chiu, D. T. 2001. A microfluidics platform for cell fusion - commentary. Curr. Opin. Chem. Biol. 5:609-612.
42. Chiu, D. T., C. F. Wilson, F. Ryttsen, A. Stromberg, C. Farre, A. Karlsson, S. Nordholm, A. Gaggar, B. P. Modi, A. Moscho, R. A. Garza-Lopez, O. Orwar, and R. N. Zare. 1999. Chemical transformations in individual ultrasmall biomimetic containers. Science. 283:1892-1895.
43. Stromberg, A., A. Karlsson, F. Ryttsen, M. Davidson, D. T. Chiu, and O. Orwar. 2001. Microfluidic device for combinatorial fusion of liposomes and cells. Anal. Chem. 73:126-130.
44. Stromberg, A., F. Ryttsen, D. T. Chiu, M. Davidson, P. S. Eriksson, C. F. Wilson, O. Orwar, and R. N. Zare. 2000. Manipulating the genetic identity and biochemical surface properties of individual cells with electric-field-induced fusion. Proc. Natl. Acad. Sci. USA. 97:7-11.
45. Estes, D. J., and M. Mayer. 2005. Giant liposomes in physiological buffer using electroformation in a flow chamber. Biochim. Biophys. Acta. 1712:152-160.
46. Estes, D. J., and M. Mayer. 2005. Electroformation of giant liposomes from spin-coated films of lipids. Colloids Surf. B Biointerfaces. 42:115-123.
47. Lee, J. N., C. Park, and G. M. Whitesides. 2003. Solvent compatibility of poly(dimethylsiloxane)-based microfluidic devices. Anal. Chem. 75:6544-6554.
48. Angelova, M. I., and D. S. Dimitrov. 1986. Liposome electroformation. Faraday Discuss. Chem. Soc. 81:303-311.
49. Angelova, M., S. Soleau, P. Meleard, J. F. Faucon, and P. Bothorel. 1992. Preparation of giant vesicles by external AC electric fields. Kinetics and applications. Prog. Colloid Polym. Sci. 89:127-131.
50. Menger, F. M., and M. I. Angelova. 1998. Giant vesicles: imitating the cytological processes of cell membranes. Acc. Chem. Res. 31:789-797.
51. Bagatolli, L. A., T. Parasassi, and E. Gratton. 2000. Giant phospholipid vesicles: comparison among the whole lipid sample characteristics using different preparation methods - a two photon fluorescence microscopy study. Chem. Phys. Lipids. 105:135-147.
52. Perez, A., Q. X. Li, P. Perez-Romero, G. DeLassus, S. R. Lopez, S. Sutter, N. McLaren, and A. O. Fuller. 2005. A new class of receptor for herpes simplex virus has heptad repeat motifs that are common to membrane fusion proteins. J. Virol. 79:7419-7430.
53. Angelova, M. I. 2000. Liposome electroformation. In Giant Vesicles. P. L. Luisi, and P. Walde, editors. John Wiley & Sons, New York. 27-36.
54. Ohki, S., and N. Duzgunes. 1979. Divalent cation-induced interaction of phospholipid vesicle and monolayer membranes. Biochim. Biophys. Acta. 552:438-449.
55. Pincet, F., S. Cribier, and E. Perez. 1999. Bilayers of neutral lipids bear a small but significant charge. Eur. Phys. J. B. 11:127-130.
56. McLaughlin, A., C. Grathwohl, and S. McLaughlin. 1978. Adsorption of divalent-cations to phosphatidylcholine bilayer membranes. Biochim. Biophys. Acta. 513:338-357.
57. Papahadjopoulos, D., S. Nir, and N. Duzgunes. 1990. Molecular mechanisms of calcium-induced membrane-fusion. J. Bioenerg. Biomembr. 22:157-179.
58. Rand, R. P., B. Kachar, and T. S. Reese. 1985. Dynamic morphology of calcium-induced interactions between phosphatidylserine vesicles. Biophys. J. 47:483-489.
59. Fix, M., T. J. Melia, J. K. Jaiswal, J. Z. Rappoport, D. Q. You, T. H. Sollner, J. E. Rothman, and S. M. Simon. 2004. Imaging single membrane fusion events mediated by SNARE proteins. Proc. Natl. Acad. Sci. USA. 101:7311-7316.
60. Liu, T., W. C. Tucker, A. Bhalla, E. R. Chapman, and J. C. Weisshaar. 2005. SNARE-driven, 25-millisecond vesicle fusion in vitro. Biophys. J. biophysj.105.062539.
61. Akashi, K., H. Miyata, H. Itoh, and K. Kinosita. 1998. Formation of giant liposomes promoted by divalent cations: critical role of electrostatic repulsion. Biophys. J. 74:2973-2982.
62. Marra, J., and J. Israelachvili. 1985. Direct measurements of forces between phosphatidylcholine and phosphatidylethanolamine bilayers in aqueous-electrolyte solutions. Biochemistry. 24:4608-4618.
63. Wilschut, J., and D. Hoekstra. 1986. Membrane-fusion-lipid vesicles as a model system. Chem. Phys. Lipids. 40:145-166.
64. Lentz, B. R. 1994. Polymer-induced membrane-fusion-potential mechanism and relation to cell-fusion events. Chem. Phys. Lipids. 73:91-106.
65. Malinin, V. S., P. Frederik, and B. R. Lentz. 2002. Osmotic and curvature stress affect PEG-induced fusion of lipid vesicles but not mixing of their lipids. Biophys. J. 82:2090-2100.
66. Boni, L. T., T. P. Stewart, J. L. Alderfer, and S. W. Hui. 1981. Lipid-polyethylene glycol interactions.1. Induction of fusion between liposomes. J. Membr. Biol. 62:65-70.
67. Livnah, O., E. A. Bayer, M. Wilchek, and J. L. Sussman. 1993. Three-dimensional structures of avidin and the avidin-biotin complex. Proc. Natl. Acad. Sci. USA. 90:5076-5080.
68. Weber, P. C., D. H. Ohlendorf, J. J. Wendoloski, and F. R. Salemme. 1989. Structural origins of high-affinity biotin binding to streptavidin. Science. 243:85-88.
69. Vanroy, N., K. Mangelschots, and F. Speleman. 1993. Improved immunocytochemical detection of biotinylated probes with neutralite avidin. Trends Genet. 9:71-72.
70. Safran, S. A., T. L. Kuhl, and J. N. Israelachvili. 2001. Polymer-induced membrane contraction, phase separation, and fusion via Marangoni flow. Biophys. J. 81:659-666.
71. Helm, C. A., J. N. Israelachvili, and P. M. McGuiggan. 1989. Molecular mechanisms and forces involved in the adhesion and fusion of amphiphilic bilayers. Science. 246:919-922.
72. Tieleman, D. P., and J. Bentz. 2002. Molecular dynamics simulation of the evolution of hydrophobic defects in one monolayer of a phosphatidylcholine bilayer: relevance for membrane fusion mechanisms. Biophys. J. 83:1501-1510.
73. Stevens, M. J., J. H. Hoh, and T. B. Woolf. 2003. Insights into the molecular mechanism of membrane fusion from simulation: evidence for the association of splayed tails. Phys. Rev. Lett. 91:188102
74. Perez-Romero, P., and A. O. Fuller. 2005. The C terminus of the B5 receptor for herpes simplex virus contains a functional region important for infection. J. Virol. 79:7431-7437.
75. Gao, X. F., and T. C. Wong. 1998. Studies of the binding and structure of adrenocorticotropin peptides in membrane mimics by NMR spectroscopy and pulsed-field gradient diffusion. Biophys. J. 74:1871-1888.
76. Hawkins, B., K. Cross, and D. Craik. 1995. Solution structure of the B-chain of insulin as determined by 1H NMR spectroscopy. Comparison with the crystal structure of the insulin hexamer and with the solution structure of the insulin monomer. Int. J. Pept. Protein Res. 46:424-433.
77. Longo, M. L., A. J. Waring, and D. A. Hammer. 1997. Interaction of the influenza hemagglutinin fusion peptide with lipid bilayers: area expansion and permeation. Biophys. J. 73:1430-1439.
78. Bechinger, B. 1999. The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta. 1462:157-183.
79. Zuckermann, M. J., and T. Heimburg. 2001. Insertion and pore formation driven by adsorption of proteins onto lipid bilayer membrane-water interfaces. Biophys. J. 81:2458-2472.
80. Shai, Y. 1999. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta. 1462:55-70.
81. Papahadjopoulos, D., W. J. Vail, C. Newton, S. Nir, K. Jacobson, G. Poste, and R. Lazo. 1977. Studies on membrane-fusion. 3. Role of calcium-induced phase-changes. Biochim. Biophys. Acta. 465:579-598.
82. Brendel, V., P. Bucher, I. R. Nourbakhsh, B. E. Blaisdell, and S. Karlin. 1992. Methods and algorithms for statistical-analysis of protein sequences. Proc. Natl. Acad. Sci. USA. 89:2002-2006.