Synthesizing artificial cells from giant unilamellar vesicles: State-of-the art in the development of microfluidic technology

BioEssays

Volumn 34, Issue 11, 2012, Pages 992-1001

  Matosevic, Sandro ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Artificial cell; Giant unilamellar vesicle; Microfluidics; Synthetic biology

Indexed keywords

ARTICLE; ARTIFICIAL CELL; BIOENGINEERING; CELL DIVISION; CELL FUNCTION; CELL MEMBRANE; CELL SIZE; CELL STRUCTURE; CELL VACUOLE; EMULSION; FILM; GIANT UNILAMELLAR VESICLE; HYDRATION; HYDRODYNAMICS; LIPID MEMBRANE; LIPID VESICLE; MEMBRANE STRUCTURE; MICROFLUIDICS; PROTEIN SYNTHESIS;

ARTIFICIAL CELLS; HYDRODYNAMICS; MICROFLUIDICS; MODELS, BIOLOGICAL; PHASE TRANSITION; UNILAMELLAR LIPOSOMES;

EID: 84867438840     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201200105     Document Type: Article

References (88)

1. Andrianantoandro E, Basu S, Karig D, Weiss R. 2006. Synthetic biology: new engineering rules for an emerging discipline. Mol Syst Biol 2: 2006.0028.
2. Purnick P, Weiss R. 2009. The second wave of synthetic biology: from modules to systems. Nat Rev Mol Cell Biol 10: 410- 22.
3. Szostak J, Bartel D, Luisi P. 2001. Synthesizing life. Nature 409: 387- 90.
4. Liu A, Fletcher D. 2001. Biology under construction: in vitro reconstitution of cellular function. Nat Rev Mol Cell Biol 10: 644- 50.
5. Vinuselvi P, Park S, Kim M, Park JM, et al. 2011. Microfluidic technologies for synthetic biology. Int J Mol Sci 12: 3576- 93.
6. Szita N, Polizzi K, Jaccard N, Baganz F. 2010. Microfluidic approaches for systems and synthetic biology. Curr Opin Biotech 21: 517- 23.
7. Suzuki H, Takeuchi S. 2008. Microtechnologies for membrane protein studies. Anal Bioanal Chem 391: 2695- 702.
8. Stano P, Carrara P, Kuruma Y, de Souza T, et al. 2011. Compartmentalized reactions as a case of soft-matter biotechnology: synthesis of proteins and nucleic acids inside lipid vesicles. J Mater Chem 21: 18887- 902.
9. Carrara P, Stano P, Luisi P. 2011. Giant vesicle colonies: a moder for "primitive" cell communities. Chembiochem 13: 1497- 502.
10. Ikonen E. 2001. Roles of lipid rafts in membrane transport. Curr Opin Cell Biol 13: 470- 7.
11. Montessuit S, Somasekharan S, Terrones O, Lucken-Ardjomande S, et al. 2011. Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell 142: 889- 901.
12. Chernomordik L, Kozlov M. 2003. Protein-lipid interplay in fusion and fission of biological membranes. Annu Rev Biochem 72: 175- 207.
13. Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31- 9.
14. Singer S, Nicholson G. 1972. Fluid mosaic model of cell membranes. Science 175: 720- 31.
15. Walde P, Cosentino K, Engel H, Stano P. 2010. Giant vesicles: preparations and applications. Chembiochem 11: 848- 65.
16. Walde P. 2010. Building artificial cells and protocell models: experimental approaches with lipid vesicles. BioEssays 32: 296- 303.
17. Mansy SS, Schrum J, Krishnaurthy M, Tobé S, et al. 2008. Template-directed synthesis of a genetic polymer in a model protocell. Nature 454: 122- 5.
18. Hotani H, Nomura F, Suzuki Y. 2000. Giant liposomes: from membrane dynamics to cell morphogenesis. Curr Opin Colloid In 4: 358- 68.
19. Stano P. 2011. Minimal cells: relevance and interplay of physical and biochemical factors. Biotechnol J 6: 850- 9.
20. Deamer D. 2005. A giant step towards artificial life? Trends Biotechnol 23: 336- 8.
21. Cans A, Wittenberg N, Karlsson R, Sombers L, et al. 2002. Artificial cells: unique insights into exocytosis using liposomes and lipid nanotubes. Proc Natl Acad Sci USA 100: 400- 4.
22. Dimova R, Lipowsky R. 2012. Lipid membranes in contact with aqueous phases of polymer solutions. Soft Matter 8: 2409- 15.
23. Long M, Jones C, Helfrich M, Mangeney-Slavin L, et al. 2005. Dynamic microcompartmentation in synthetic cells. Proc Natl Acad Sci USA 102: 5920- 5.
24. Simons K, Vaz WL. 2004. Model systems, lipid rafts and cell membranes. Annu Rev Biophys Biomol Struct 33: 269- 95.
25. Ipsen J, Karlström G, Mourtisen O, Wennerström H, et al. 1987. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim Biophys Acta: Biomembr 905: 162- 72.
26. Korlach J, Schwille P, Webb W, Feigenson G. 1999. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc Natl Acad Sci USA 96: 8461- 6.
27. Li Y, Kusumaatmaja H, Lipowsky R, Dimova R. 2012. Wetting-induced budding of vesicles in contact with several aqueous phases. J Phys Chem B 116: 1819- 23.
28. Long M, Cans A, Keating C. 2008. Budding and asymmetric protein microcompartmentation in giant vesicles containing two aqueous phases. J Am Chem Soc 130: 756- 62.
29. Merkle D, Kahya N, Schwille P. 2008. Reconstitution and anchoring of cytoskeleton inside giant unilamellar vesicles. Chembiochem 9: 2673- 81.
30. Liu A, Richmond D, Maibaum L, Pronk S, et al. 2008. Membrane-induced bundling of actin filaments. Nat Phys 4: 789- 93.
31. Upadhyaya A, van Oudenaarden A. 2003. Biomimetic systems for studying actin-based motility. Curr Biol 13: R734- 44.
32. Heuvingh J, Franco M, Chavrier P, Sykes C. 2007. ARF1-mediated actin polymerization produces movement of artificial vesicles. Proc Natl Acad Sci USA 104: 16928- 33.
33. Whitesides G, Grzybowski B. 2002. Self-assembly at all scales. Science 295: 2418- 21.
34. Angelova MI, Soléau S, Méléard Ph, Faucon F, et al. 1992. Preparation of giant vesicles by external AC electric fields. Kinetics and applications. Trends Colloid Interface Sci 89: 127- 31.
35. Bangham AD, Standish MM, Watkins JC. 1965. Diffusion of univalent ions across the lamellae of swollen phospholipids. J Mol Biol 13: 238- 52.
36. Pautot S, Frisken BJ, Weitz DA. 2003. Engineering asymmetric vesicles. Proc Natl Acad Sci USA 100: 10718- 21.
37. Batzri S, Korn ED. 1973. Single bilayer liposomes prepared without sonication. Biochim Biophys Acta 298: 1015- 9.
38. Bagatolli L, Gratton E. 2000. Two photon fluorescence microscopy of coexisting lipid domains in giant unilamellar vesicles of binary phospholipid mixtures. Biophys J 78: 290- 305.
39. Veatch S, Keller S. 2003. Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys J 85: 3074- 83.
40. Takeuchi S. 2010. Formation of planar lipid bilayer membranes and vesicles using microfluidic technology. In Iglič A. ed; Advances in Planar Lipid Bilayers and Liposomes, Vol. 4. Amsterdam: Elsevier. p. 87- 100.
41. Whitesides GM. 2006. The origins and the future of microfluidics. Nature 442: 368- 73.
42. Di Carlo D. 2009. Inertial microfluidics. Lab Chip 9: 3038- 46.
43. Jahn A, Reiner J, Vreeland W, DeVoe D, et al. 2008. Preparation of nanoparticles by continuous-flow microfluidics. J Nanopart Res 10: 925- 34.
44. Solvas X, deMello A. 2011. Droplet microfluidics: recent developments and future applications. Chem Commun 47: 1936- 42.
45. Matosevic S, Szita N, Baganz F. 2011. Fundamentals and applications of immobilized microfluidic enzymatic reactors. J Chem Technol Biotechnol 86: 325- 34.
46. Angelova M, Dimitrov DS. 1986. Liposome electroformation. Faraday Discuss 81: 303- 11.
47. Montes L, Alonso A, Goni F, Bagatolli L. 2007. Giant unilamellar vesicles electroformed from native membranes and organic lipid mixtures under physiological conditions. Biophys J 93: 3548- 54.
48. Kuribayashi K, Tresset G, Coquet P, Fujita H, et al. 2006. Electroformation of giant liposomes in microfluidic channels. Meas Sci Technol 17: 3121- 6.
49. Kuribayashi K, Takeuchi S. 2008. Electroformation of solvent-free lipid membranes over microaperture array. Proc IEEE MEMS 296- 9.
50. Dittrich P, Heule M, Renaud P, Manz A. 2006. On-chip extrusion of lipid vesicles and tubes through microsized apertures. Lab Chip 6: 488- 93.
51. Funakoshi K, Suzuki H, Takeuchi S. 2007. Formation of giant lipid vesiclelike compartments from a planar lipid membrane by a pulsed jet flow. J Am Chem Soc 129: 12608- 9.
52. Stachowiak JC, Richmond DL, Li TH, Liu AP, et al. 2008. Unilamellar vesicle formation and encapsulation by microfluidic jetting. Proc Natl Acad Sci USA 105: 4697- 702.
53. Stachowiak JC, Richmond DL, Li TH, Brochard-Wyart F, et al. 2009. Inkjet formation of unilamellar lipid vesicles for cell-like encapsulation. Lab Chip 9: 2003- 9.
54. Richmond DL, Schmid EM, Martens S, Stachowiak JC, et al. 2011. Forming giant vesicles with controlled membrane composition, asymmetry, and contents. Proc Natl Acad Sci USA 108: 9431- 6.
55. Kirchner S, Ohlinger A, Pfeiffer T. 2012. Membrane composition of jetted lipid vesicles: a Raman spectroscopy study. J Biophotonics 5: 40- 6.
56. Ota S, Yoshizawa S, Takeuchi S. 2009. Microfluidic formation of monodisperse, cell-sized, and unilamellar vesicles. Angew Chem 48: 6533- 7.
57. Jahn A, Vreeland WN, Gaitan M, Locascio LE. 2004. Controlled vesicle self-assembly in microfluidic channels with hydrodynamic focusing. J Am Chem Soc 126: 2674- 5.
58. Jahn A, Vreeland WN, DeVoe DL, Locascio LE, et al. 2007. Microfluidic directed formation of liposomes of controlled size. Langmuir 23: 6289- 93.
59. Thiele J, Steinhauser D, Pfohl T, Forster S. 2010. Preparation of monodisperse block copolymer vesicles via flow focusing in microfluidics. Langmuir 26: 6860- 3.
60. Takinoue M, Takeuchi S. 2011. Droplet microfluidics for the study of artificial cells. Anal Bioanal Chem 400: 1705- 16.
61. Anna S, Bontoux N, Stone H. 2003. Formation of dispersions using "flow focusing" in microchannels. Appl Phys Lett 82: 364- 6.
62. Link D, Anna S, Weitz D, Stone H. 2004. Geometrically mediated breakup of drops in microfluidic devices. Phys Rev Lett 92: 054503.
63. Teh S, Lin R, Hung L, Lee A. 2008. Droplet microfluidics. Lab Chip 8: 198- 220.
64. Garstecki P, Fuerstman M, Stone H, Whitesides G. 2006. Formation of droplets and bubbles in a microfluidic T-junction. Lab Chip 6: 437- 46.
65. Tawfik D, Griffiths A. 1998. Man-made cell-like compartments for molecular evolution. Nat Biotechnol 16: 652- 6.
66. Dittrich P, Jahnz M, Schwille P. 2005. A new embedded process for compartmentalized cell-free protein expression and on-line detection in microfluidic devices. Chembiochem 6: 811- 4.
67. Paegel B, Joyce G. 2010. Microfluidic compartmentalized directed evolution. Chem Biol 17: 717- 24.
68. Utada A, Lorenceau E, Link D, Kaplan P, et al. 2005. Monodisperse double emulsions generated from a microcapillary device. Science 308: 537- 41.
69. Shum H, Lee D, Yoon I, Kodger T, et al. 2008. Double emulsion templated monodisperse phospholipid vesicles. Langmuir 24: 7651- 3.
70. Shum H, Kim J, Weitz D. 2008. Microfluidic fabrication of monodisperse biocompatible and biodegradable polymersomes with controlled permeability. J Am Chem Soc 130: 9543- 9.
71. Shum H, Zhao Y, Kim S, Weitz D. 2011. Multicompartment polymersomes from double emulsions. Angew Chem Int Ed 50: 1648- 51.
72. Sugiura S, Kuroiwa T, Kagota T, Nakajima M, et al. 2008. Novel method for obtaining homogeneous giant vesicles from a monodisperse water-in-oil emulsion prepared with a microfluidic device. Langmuir 24: 4581- 8.
73. Kuroiwa T, Kiuchi H, Noda K, Kobayashi I, et al. 2009. Controlled preparation of giant vesicles from uniform water droplets obtained by microchannel emulsification with bilayer-forming lipids as emulsifiers. Microfluid Nanofluid 6: 821.
74. Pautot S, Frisken BJ, Weitz DA. 2003. Production of unilamellar vesicles using an inverted emulsion. Langmuir 19: 2870- 9.
75. Noireaux V, Libchaber A. 2004. A vesicle bioreactor as a step toward an artificial cell assembly. Proc Natl Acad Sci USA 101: 17669- 74.
76. Nishimura K, Suzuki H, Toyota T, Yomo T. 2012. Size control of giant unilamellar vesicles prepared from inverted emulsion droplets. J Colloid Interface Sci 376: 125.
77. Hase M, Yamada A, Hamada T, Baigl D, et al. 2007. Manipulation of cell-sized phospholipid-coated microdroplets and their use as biochemical microreactors. Langmuir 23: 348- 52.
78. Matosevic S, Paegel BM. 2011. Stepwise synthesis of giant unilamellar vesicles on a microfluidic assembly line. J Am Chem Soc 133: 2798- 800.
79. Hu P, Li S, Malmstadt N. 2011. Microfluidic fabrication of asymmetric giant lipid vesicles. ACS Appl Mater Interfaces 3: 1434- 40.
80. Matosevic S, Paegel B. 2012. Layer-by-layer assembly of cellular structures. Biophys J 102: 28a.
81. Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31- 9.
82. van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9: 124.
83. Hannun YA, Obeid LM. 2008. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139- 50.
84. Holthuis JCM, Levine TP. 2005. Lipid traffic: floppy drives and a superhighway. Nat Rev Mol Cell Biol 6: 209- 20.
85. Seigneuret M, Devaux PF. 2012. ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc Natl Acad Sci USA 81: 3751- 5.
86. Cheng HT, Megha, London E. 2009. Preparation and properties of asymmetric vesicles that mimic cell membranes: effect upon lipid raft formation and transmembrane helix orientation. J Biol Chem 284: 6079- 92.
87. Luisi P, Ferri F, Stano P. 2003. Approaches to semi synthetic minimal cells: a review. Naturwissenschaften 93: 1- 13.
88. Stano P, Luisi PL. 2010. Achievements and open questions in the self-reproduction of vesicles and synthetic minimal cells. Chem Commun 46: 3639- 53.