Recent Biophysical Issues about the Preparation of Solute-Filled Lipid Vesicles

Mechanics of Advanced Materials and Structures

Volumn 22, Issue 9, 2015, Pages 748-759

  Stano, Pasquale ^a   De Souza, Tereza Pereira ^b   Carrara, Paolo ^a   Altamura, Emiliano ^c   D'Aguanno, Erica ^b   Caputo, Margherita ^c   Luisi, Pier Luigi ^a   Mavelli, Fabio ^c  

^a ROMA TRE UNIVERSITY   (Italy)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c UNIVERSITY OF BARI   (Italy)

Author keywords

encapsulation; entrapment; liposomes; synthetic biology; synthetic cells

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; CELLS; ENCAPSULATION; LIPOSOMES; MOLECULAR BIOLOGY;

BIOLOGICAL FUNCTIONS; CELL POPULATIONS; CELL PREPARATION; ENTRAPMENT; LIPID VESICLES;

SYNTHETIC BIOLOGY;

EID: 84925009219     PISSN: 15376494     EISSN: 15376532     Source Type: Journal    
DOI: 10.1080/15376494.2013.857743     Document Type: Article

References (76)

1. D. Andy, Foundations for engineering biology, Nature, vol. 438, pp. 449-453, 2005.
2. P.L. Luisi, F. Ferri, and P. Stano, Approaches to semi-synthetic minimal cells: A review, Naturwissenschaften, vol. 93, pp. 1-13, 2006.
3. P. Stano, Synthetic biology of minimal living cells: Primitive cell models and semi-synthetic cells, Syst. Synth. Biol., vol. 4, pp. 149-156, 2010.
4. P. Stano, P. Carrara, Y. Kuruma, T. Souza, and P.L. Luisi, Compartmentalized reactions as a case of soft-matter biotechnology: Synthesis of proteins and nucleic acids inside lipid vesicles, J. Mater. Chem., vol. 21, pp. 18887-18902, 2011.
5. P. Stano, Minimal cells: Relevance and interplay of physical and biochemical factors, Biotechnol. J., vol. 6, pp. 850-859, 2011.
6. V. Noireaux and A. Libchaber, A vesicle bioreactor as a step toward an artificial cell assembly, Proc. Natl. Acad. Sci. USA, vol. 101, pp. 17669-17674, 2004.
7. K. Ishikawa, K. Sato, Y. Shima, I. Urabe, and T. Yomo, Expression of a cascading genetic network within liposomes, FEBS Lett., vol. 576, pp. 387-390, 2004.
8. H. Kita, T. Matsuura, T. Sunami, K. Hosoda, N. Ichihashi, K. Tsukada, I. Urabe, and T. Yomo, Replication of genetic information with self-encoded replicase in liposomes, ChemBioChem, vol. 9, pp. 2403-2410, 2008.
9. B.M. Discher, Y.Y. Won, D.S. Ege, J.C.M. Lee, F.S. Bates, D.E. Discher, and D.A. Hammer, Tough vesicles made from diblock copolymers, Science, vol. 284, pp. 1143-1146, 1999.
10. S. Rasmussen, L. Chen, D. Deamer, D.C. Krakauer, N.H. Packard, P.F. Stadler, and M.A. Bedau, Transitions from non-living to living matter, Science, vol. 303, pp. 963-965, 2004.
11. K. Kurihara, M. Tamura, K. Shohda, T. Toyota, K. Suzuki, and T. Sugawara, Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA, Nature Chem., vol. 3, pp. 775-781, 2011.
12. J.W. Szostak, D.P. Bartel, and P.L. Luisi, Synthesizing life, Nature, vol. 409, pp. 387-390, 2001.
13. S.S. Mansy, J.P. Schrum, M. Krishnamurthy, S. Tobé, D.A. Treco, and J.W. Szostak, Template-directed synthesis of a genetic polymer in a model protocell, Nature, vol. 454, pp. 122-125, 2008.
14. H.J. Morowitz, B. Heinz, and D. Deamer, Chemical logic of a minimum protocell, Orig. Life Evol. Biosph., vol. 18, pp. 281-287, 1988.
15. P.A. Bachmann, P.L. Luisi, and J. Lang, Autocatalytic self-replicating micelles as models for prebiotic structures, Nature, vol. 357, pp. 57-59, 1992.
16. P. Walde, A. Goto, P.A. Monnard, M. Wessicken, and P.L. Luisi, Oparin's reactions revisited: Enzymatic synthesis of poly(adenylic acid) in micelles and self-reproducing vesicles, J. Am. Chem. Soc., vol. 116, pp. 7541-7544, 1994.
17. T. Oberholzer, R. Wick, P.L. Luisi, and C.K. Biebricher, Enzymatic RNA replication in self-reproducing vesicles: An approach to a minimal cell, Biochem. Biophys. Res. Comm., vol. 207, pp. 250-257, 1995.
18. T. Oberholzer, M. Albrizio, and P.L. Luisi, Polymerase chain reaction in liposomes, Chem. & Biol., vol. 2, pp. 677-682, 1995.
19. P. Walde, R. Wick, M. Fresta, A. Mangone, and P.L. Luisi, Autopoietic self-reproduction of fatty acid vesicles, J. Am. Chem. Soc., vol. 116, pp. 11649-11654, 1994.
20. S.S. Mansy and J.W. Szostak, Reconstructing the emergence of cellular life through the synthesis of model protocells, Cold Spring Harb. Symp. Quant. Biol., vol. 74, pp. 47-54, 2009.
21. T. Oberholzer, K.H. Nierhaus, and P.L. Luisi, Protein expression in liposomes, Biochem. Biophys. Res. Comm., vol. 261, pp. 238-241, 1999.
22. W. Yu, K. Sato, M. Wakabayashi, T. Nakatshi, E.P. Ko-Mitamura, Y. Shima, I. Urabe, and T. Yomo, Synthesis of functional protein in liposome, J. Biosci. Bioeng., vol. 92, pp. 590-593, 2001.
23. P. Stano and P.L. Luisi, Semi-synthetic minimal cells: Origin and recent developments, Curr. Opin. Biotech., vol. 24, pp. 633-638, 2013.
24. Y. Kuruma, P. Stano, T. Ueda, and P.L. Luisi, A synthetic biology approach to the construction of membrane proteins in semi-synthetic minimal cells, Biochim. Biophys. Acta, vol. 1788, pp. 567-574, 2009.
25. S. Matosevic, Synthesizing artificial cells from giant unilamellar vesicles: State-of-the-art in the development of microfluidic technology, Bioessay, vol. 34, pp. 992-1001, 2012.
26. C. Martino, S.-H. Kim, L. Horsfall, A. Abbaspourrad, S.J. Rosser, J. Cooper, and D.A. Weitz, Protein expression, aggregation, and triggered release from polymersomes as artificial cell-like structures, Angew. Chem. Int. Ed., vol. 51, pp. 6416-6420, 2012.
27. P.L. Luisi, M. Allegretti, T. Souza, F. Steineger, A. Fahr, and P. Stano, Spontaneous protein crowding in liposomes: A new vista for the origin of cellular metabolism, ChemBioChem, vol. 11, pp. 1989-1992, 2010.
28. T. Souza, F. Steiniger, P. Stano, A. Fahr, and P.L. Luisi, Spontaneous crowding of ribosomes and proteins inside vesicles: A possible mechanism for the origin of cell metabolism, ChemBioChem, vol. 12, pp. 2325-2330, 2011.
29. P.L. Luisi, The synthetic approach in biology: epistemological notes for synthetic biology. In: Chemical Synthetic Biology, P.L. Luisi and C. Chiarabelli, Eds., Wiley, Chichester, pp. 343-362, 2011.
30. H.H. Zepik, P. Walde, E.L. Kostoryz, J. Code, and D.M. Yourtree, Lipid vesicles as membrane models for toxicological assessment of xenobiotics, Crit. Rev. Toxicol., vol. 38, pp. 1-11, 2008.
31. A.P. Liu and D.A. Fletcher, Biology under construction: In vitro reconstitution of cellular functions, Nat. Rev. Mol. Cell Biol., vol. 10, pp. 644-650, 2009.
32. C. Tan, S. Saurabh, M.P. Bruchez, R. Schwartz, and P. LeDuc, Molecular crowding shapes gene expression in synthetic cellular nanosystems, Nat. Nanotech., vol. 8, pp. 602-608, 2013.
33. T. Osaki, K. Kamiya, R. Kawano, H. Sasaki, and S. Takeuchi, Towards artificial cell array system: encapsulation and hydration technologies integrated in liposome array, IEEE International Conference on Micro Electro Mechanical Systems, January 29-February 2, Paris, France, 2012.
34. S. Matosevic and B.H. Paegel, Layer-by-layer cell membrane assembly, Nat. Chem., vol. 5, pp. 958-963, 2013.
35. S. Fujii, T. Matsuura, T. Sunami, Y. Kazuta, and T. Yomo, In vitro evolution of alpha-hemolysin using a liposome display, Proc. Natl. Acad. Sci. USA, vol. 110, pp. 16796-16801, 2013.
36. T. Nakano, M. Moore, A. Enomoto, and T. Suda, Molecular communication technology as a biological ICT. In: Sawai, H. (Ed.), Biological Functions for Information and Communication Technologies, Studies in Computational Intelligence, Springer-Verlag, Berlin Heidelberg, pp. 49-86, 2011.
37. P. Stano, G. Rampioni, P. Carrara, L. Damiano, L. Leoni, and P.L. Luisi, Semi-synthetic minimal cells as a tool for biochemical ICT, Biosystems, vol. 109, pp. 24-34, 2012.
38. G. Rampioni, L. Damiano, M. Messina, F. D'Angelo, L. Leoni, and P. Stano, Chemical communication between synthetic and natural cells: A possible experimental design, Electr. Proc. Theor. Comp. Sci., vol. 130, pp. 14-26, 2013.
39. M. Kaneda, S.M. Nomura, S. Ichinose, S. Kondo, K. Nakahama, K. Akiyoshi, and I. Morita, Direct formation of proteo-liposomes by in vitro synthesis and cellular cytosolic delivery with connexin-expressing liposomes, Biomaterials, vol. 30, pp. 3971-3977, 2009.
40. Y. Moritani, S.M. Nomura, I. Morita, and K. Akiyoshi, Direct integration of cell-free-synthesized connexin-43 into liposomes and hemichannel formation, FEBS J., vol. 277, pp. 3343-3352, 2010.
41. P.R. Leduc, M.S. Wong, P.M. Ferriera, R.E. Groff, K. Haslinger, M.P. Koonce, W.Y. Lee, J.C. Love, J.A. McCammon, N.A. Monteiro-Riviere, V.M. Rotello, G.W. Rubloff, R. Westervelt, and M. Yoda, Towards an in vivo biologically inspired nanofactory, Nat. Nanotechnol., vol. 2, pp. 3-7, 2007.
42. P. Bucher, A. Fischer, P.L. Luisi, T. Oberholzer, and P. Walde, Giant vesicles as biochemical compartments: The use of microinjection techniques, Langmuir, vol. 14, pp. 2712-2721, 1998.
43. S. Pautot, B.J. Frisken, and D.A. Weitz, Production of unilamellar vesicles using an inverted emulsion, Langmuir, vol. 19, pp. 2870-2879, 2003.
44. D. san Swaay and A. deMello, Microfluidic methods for forming liposomes, Lab on a Chip, vol. 13, pp. 752-767, 2013.
45. D. D. Lasic, The mechanism of vesicle formation, Biochem. J., vol. 256, pp. 1-11, 1988.
46. Y. Shimizu, A. Inoue, Y. Tomari, T. Suzuki, T. Yokogawa, K. Nishikawa, and T. Ueda, Cell-free translation reconstituted with purified components, Nat. Biotech., vol. 19, pp. 751-755, 2001.
47. T. Souza, P. Stano, and P.L. Luisi, The minimal size of liposome-based model cells brings about a remarkably enhanced entrapment and protein synthesis, ChemBioChem, vol. 10, pp. 1056-1063, 2009.
48. T. Souza, P. Stano, F. Steiniger, E. D'Aguanno, E. Altamura, A. Fahr, and P.L. Luisi, Encapsulation of ferritin, ribosomes, and ribo-peptidic complexes inside liposomes: Insights into the origin of metabolism, Orig. Life Evol. Biosph., vol. 42, pp. 421-428, 2012.
49. B. Lohse, P.-Y. Bolinger, and D. Stamou, Encapsulation efficiency measured on single small unilamellar vesicles, J. Am. Chem. Soc., vol. 130, pp. 14372-14373, 2008.
50. F. Mavelli and P. Stano, Kinetic models for autopoietic chemical systems: Role of fluctuations in homeostatic regime, Phys. Biol., vol. 7, p. 016010, 2010.
51. P.L. Luisi, An open question on the origin of life: The first forms of metabolism, Chem. & Biodiv., vol. 9, pp. 2635-2647, 2012.
52. P. Stano, E. D'Aguanno, J. Bolz, A. Fahr, and P.L. Luisi, A remarkable self-organization process as the origin of primitive functional cells, Angew. Chem. Int. Ed. Engl., vol. 52, pp. 13397-13400, 2013.
53. K. Cosentino, A. Beneduci, A. Ramundo-Orlando, and G. Chidichimo, The influence of millimeter waves on the physical properties of large and giant unilamellar vesicles, J. Biol. Phys., vol. 39, pp. 395-410, 2013.
54. K. Nishimura, H. Suzuki, T. Toyota, and T. Yomo, Size control of giant unilamellar vesicles prepared from inverted emulsion droplets, J. Coll. Inter. Sci., vol. 376, pp. 119-125, 2012.
55. J. Shin and V. Noireaux, An E. coli cell-free expression toolbox: Application to synthetic gene circuits and artificial cells, ACS Synth. Biol., vol. 1, pp. 29-41, 2012.
56. P. Carrara, P. Stano, and P.L. Luisi, Giant vesicles 'colonies': A model for primitive cell communities, ChemBioChem, vol. 13, pp. 1497-1502, 2012.
57. L.M. Dominak and C.D. Keating, Polymer encapsulation within giant lipid vesicles, Langmuir, vol. 23, pp. 7148-7154, 2007.
58. D. Fiordemondo and P. Stano, Lecithin-based water-in-oil compartments as dividing bioreactors, ChemBioChem, vol. 8, pp. 1965-1973, 2007.
59. H. Saito, Y. Kato, M. LeBerre, A. Yamada, T. Inoue, K. Yoshikawa, and D. Baigl, Time-resolved tracking of aminimum gene expression system reconstituted in giant liposomes, ChemBioChem, vol. 10, pp. 1640-1643, 2009.
60. K. Yamaji, T. Kanai, S.M. Nomura, K. Akiyoshi, M. Negishi, Y. Chen, H. Atomi, K. Yoshikawa, and T. Imanaka, Protein synthesis in giant liposomes using the in vitro translation system of Thermococcus kodakaraensis, IEEE Trans Nanobiosci., vol. 8, pp. 325-331, 2009.
61. P. von Nies, Z. Nourian, M. Kok, R. van Vijk, J. Moeskops, I. Westerlaken, J.M. Poolman, R. Eelkema, J.H. van Esch, Y. Kuruma, T. Ueda, and C. Danelon, Unbiased tracking of the progression of mRNA and protein synthesis in bulk and in liposome-confined reactions, ChemBioChem, vol. 14, pp. 1963-1966, 2013.
62. A. Kato, M. Yanagisawa, Y.T. Sato, K. Fujiwara, and K. Yoshikawa, Cell-sized confinement in microspheres accelerates the reaction of gene expression, Sci. Rep., vol. 2, p. 283, 2012.
63. K. Vorauer-Uhl, A. Wagner, N. Borth, and H. Katinger, Determination of liposome size distribution by flow cytometry, Cytometry, vol. 39, pp. 166-171, 2000.
64. K. Nishimura, T. Hosoi, T. Sunami, T. Toyota, M. Fujinami, K. Oguma, T. Matsuura, H. Suzuki, and T. Yomo, Population analysis of structural properties of giant liposomes by flow cytometry, Langmuir, vol. 25, pp. 10439-10443, 2009.
65. T. Sunami, K. Hosoda, H. Suzuki, T. Matsuura, and T. Yomo, Cellular compartment model for exploring the effect of the lipidic membrane on the kinetics of encapsulated biochemical reactions, Langmuir, vol. 26, pp. 8544-8551, 2010.
66. K. Nishimura, T. Matsuura, K. Nishimura, T. Sunami, H. Suzuki, and T. Yomo, Cell-free protein synthesis inside giant unilamellar vesicles analyzed by flow cytometry, Langmuir, vol. 28, pp. 8426-8432, 2012.
67. P. Stano, New aspects of interactions among vesicles, Orig. Life Evol. Biosph., vol. 37, pp. 439-444, 2007.
68. C. Chiarabelli, J.W. Vrijbloed, D. De Lucrezia, R.M. Thomas, P. Stano, F. Polticelli, T. Ottone, E. Papa, and P.L. Luisi, Investigation of de novo totally random biosequences. Part II. On the folding frequency in a totally random library of de novo proteins obtained by phage display, Chem. & Biodiv., vol. 3, pp. 840-859, 2006.
69. Y. Hayashi, T. Aita, H. Toyota, Y. Husimi, I. Urabe, and T. Yomo, Experimental rugged fitness landscape in protein sequence space, PLoS One, vol. 1, p. e96, 2006.
70. B. Seelig and J. W. Szostak, Selection and evolution of enzymes from a partially randomized non-catalytic scaffold, Nature, vol. 448, pp. 828-831, 2007.
71. D. Segre, D. Lancet, O. Kedem, and Y. Pilpel, Graded autocatalysis replication domain (GARD): Kinetic analysis of self-replication in mutually catalytic sets, Orig. Life Evol. Biosph., vol. 28, pp. 501-514, 1998.
72. Z. Cheng and P.L. Luisi, Coexistence and mutual competition of vesicles with different size distributions, J. Phys. Chem. B, vol. 107, pp. 10940-10945, 2003.
73. I.A. Chen, R.W. Roberts, and J.W. Szostak, The emergence of competition between model protocells, Science, vol. 305, pp. 1474-1476, 2004.
74. M. Hadorn and P. Eggenberger Hotz, DNA-mediated self-assembly of artificial vesicles, PLoS One, vol. 26, p. e9886, 2010.
75. I. Budin and J.W. Szostak, Physical effects underlying the transition from primitive to modern cell membranes, Proc. Natl. Acad. Sci. USA, vol. 108, pp. 5249-5354, 2011.
76. L. Pontani, J. van der Gucht, G. Salbreux, J. Heuvingh, J.F. Joanny, and C. Sykes, Reconstitution of an actin cortex inside a liposome, Biophys. J., vol. 96, pp. 192-198, 2009.