The engineering of artificial cellular nanosystems using synthetic biology approaches

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 6, Issue 4, 2014, Pages 369-383

  Wu, Fan ^a   Tan, Cheemeng ^a  

^a University of California   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGY; BIOMIMETICS; CELLS; DRUG DELIVERY; MACHINERY;

BIOMIMETIC SYSTEMS; CELL-FREE EXPRESSION; INHERENT COMPLEXITY; METABOLIC PATHWAYS; NUMBER OF COMPONENTS; PROTEIN EXPRESSION SYSTEMS; SIGNALING PATHWAYS; SYNTHETIC GENE CIRCUITS;

NANOSYSTEMS;

ALPHA HEMOLYSIN; AMINO ACID TRANSFER RNA LIGASE; AMPHOPHILE; BUTANOL; CREATINE PHOSPHATE; CYAN FLUORESCENT PROTEIN; ELONGATION FACTOR 3; FATTY ACID; INITIATION FACTOR 3; LIPOSOME; METHIONINE TRANSFER RNA; N ACYLHOMOSERINE LACTONE; OLIGONUCLEOTIDE; PHENYLALANINE AMMONIA LYASE; PHOSPHOLIPID; POLYPEPTIDE ANTIBIOTIC AGENT; RNA POLYMERASE;

ARTICLE; ARTIFICIAL CELL; ARTIFICIAL MEMBRANE; BACTERIOPHAGE T7; BIOFUEL PRODUCTION; BIOMIMETICS; BIOTECHNOLOGY; CELL DIVISION; CELL ENGINEERING; CELL FREE SYSTEM; CELL GROWTH; CELL MEMBRANE; CELL METABOLISM; DNA REPLICATION; DRUG DELIVERY SYSTEM; ENERGY CONSUMPTION; EXOCYTOSIS; GENE EXPRESSION; GENE EXPRESSION SYSTEM; IN VITRO STUDY; INTRACELLULAR SPACE; LIPID BILAYER; MACROMOLECULE; MATHEMATICAL MODEL; MOLECULAR CROWDING; NANOENGINEERING; NONHUMAN; OPEN READING FRAME; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RNA REPLICATION; RNA SYNTHESIS; SURFACE TENSION; SYNTHETIC BIOLOGY; SYSTEMS BIOLOGY; CHEMISTRY; TRENDS;

ARTIFICIAL CELLS; BIOMIMETICS; SYNTHETIC BIOLOGY;

EID: 84902367870     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1265     Document Type: Article

References (106)

1. Miller SL. A production of amino acids under possible primitive earth conditions. Science 1953, 117:528-529.
2. Rudnick G, Schildiner S, Kaback HR. Equilibrium between two forms of the lac carrier protein in energized and nonenergized membrane vesicles from Escherichia coli. Biochemistry 1976, 15:5126-5131.
3. Kim J, White KS, Winfree E. Construction of an in vitro bistable circuit from synthetic transcriptional switches. Mol Syst Biol 2006, 2:68.
4. Mills DR, Peterson RL, Spiegelman S. An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. Proc Natl Acad Sci U S A 1967, 58:217-224.
5. Chen HZ, Zubay G. Prokaryotic coupled transcription-translation. Methods Enzymol 1983, 101:674-690.
6. Jewett MC, Calhoun KA, Voloshin A, Wuu JJ, Swartz JR. An integrated cell-free metabolic platform for protein production and synthetic biology. Mol Syst Biol 2008, 4:220.
7. Kikuchi H, Suzuki N, Ebihara K, Morita H, Ishii Y, Kikuchi A, Sugaya S, Serikawa T, Tanaka K. Gene delivery using liposome technology. J Control Release 1999, 62:269-277.
8. LaVan DA, McGuire T, Langer R. Small-scale systems for in vivo drug delivery. Nat Biotechnol 2003, 21:1184-1191.
9. Chang TM. Therapeutic applications of polymeric artificial cells. Nat Rev Drug Discov 2005, 4:221-235.
10. Tan C, Saurabh S, Bruchez MP, Schwartz R, Leduc P. Molecular crowding shapes gene expression in synthetic cellular nanosystems. Nat Nanotechnol 2013, 8:602-608.
11. Martino C, Horsfall L, Chen Y, Chanasakulniyom M, Paterson D, Brunet A, Rosser S, Yuan YJ, Cooper JM. Cytoskeletal protein expression and its association within the hydrophobic membrane of artificial cell models. Chembiochem 2012, 13:792-795.
12. Martino C, Kim SH, Horsfall L, Abbaspourrad A, Rosser SJ, Cooper J, Weitz DA. Protein expression, aggregation, and triggered release from polymersomes as artificial cell-like structures. Angew Chem Int Ed Engl 2012, 51:6416-6420.
13. Matsuura T, Hosoda K, Kazuta Y, Ichihashi N, Suzuki H, Yomo T. Effects of compartment size on the kinetics of intracompartmental multimeric protein synthesis. ACS Synth Biol 2012, 1:431-437.
14. Noireaux V, Bar-Ziv R, Godefroy J, Salman H, Libchaber A. Toward an artificial cell based on gene expression in vesicles. Phys Biol 2005, 2:P1-8.
15. Long MS, Jones CD, Helfrich MR, Mangeney-Slavin LK, Keating CD. Dynamic microcompartmentation in synthetic cells. Proc Natl Acad Sci U S A 2005, 102:5920-5925.
16. Ishikawa K, Sato K, Shima Y, Urabe I, Yomo T. Expression of a cascading genetic network within liposomes. FEBS Lett 2004, 576:387-390.
17. LeDuc PR, Messner WC, Wikswo JP. How do control-based approaches enter into biology? Annu Rev Biomed Eng 2011, 13:369-396.
18. Mansy SS, Schrum JP, Krishnamurthy M, Tobe S, Treco DA, Szostak JW. Template-directed synthesis of a genetic polymer in a model protocell. Nature 2008, 454:122-125.
19. Hanczyc MM, Fujikawa SM, Szostak JW. Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 2003, 302:618-622.
20. Monnard PA, Apel CL, Kanavarioti A, Deamer DW. Influence of ionic inorganic solutes on self-assembly and polymerization processes related to early forms of life: implications for a prebiotic aqueous medium. Astrobiology 2002, 2:139-152.
21. Bui HT, Umakoshi H, Ngo KX, Nishida M, Shimanouchi T, Kuboi R. Liposome membrane itself can affect gene expression in the Escherichia coli cell-free translation system. Langmuir 2008, 24:10537-10542.
22. Kazuta Y, Adachi J, Matsuura T, Ono N, Mori H, Yomo T. Comprehensive analysis of the effects of Escherichia coli ORFs on protein translation reaction. Mol Cell Proteomics 2008, 7:1530-1540.
23. Cans AS, Wittenberg N, Karlsson R, Sombers L, Karlsson M, Orwar O, Ewing A. Artificial cells: unique insights into exocytosis using liposomes and lipid nanotubes. Proc Natl Acad Sci U S A 2003, 100:400-404.
24. Pereira de Souza T, Stano P, Luisi PL. The minimal size of liposome-based model cells brings about a remarkably enhanced entrapment and protein synthesis. Chembiochem 2009, 10:1056-1063.
25. Kawarasaki Y, Nakano H, Yamane T. Prolonged cell-free protein synthesis in a batch system using wheat germ extract. Biosci Biotechnol Biochem, 1994, 58:1911-1913
26. Nakano H, Tanaka T, Kawarasaki Y, Yamane T. An increased rate of cell-free protein synthesis by condensing wheat-germ extract with ultrafiltration membranes. Biosci Biotechnol Biochem 1994, 58:631-634.
27. Zawada JF, Yin G, Steiner AR, Yang J, Naresh A, Roy SM, Gold DS, Heinsohn HG, Murray CJ. Microscale to manufacturing scale-up of cell-free cytokine production--a new approach for shortening protein production development timelines. Biotechnol Bioeng 2011, 108:1570-1578.
28. Tsuboi T, Takeo S, Iriko H, Jin L, Tsuchimochi M, Matsuda S, Han E-T, Otsuki H, Kaneko O, Sattabongkot J, et al. Wheat germ cell-free system-based production of malaria proteins for discovery of novel vaccine candidates. Infect Immun 2008, 76:1702-1708.
29. Jewett MC, Fritz BR, Timmerman LE, Church GM. In vitro integration of ribosomal RNA synthesis, ribosome assembly, and translation. Mol Syst Biol 2013, 9:678.
30. Monnard PA, Deamer DW. Membrane self-assembly processes: steps toward the first cellular life. Anat Rec 2002, 268:196-207.
31. Apel CL, Deamer DW, Mautner MN. Self-assembled vesicles of monocarboxylic acids and alcohols: conditions for stability and for the encapsulation of biopolymers. Biochim Biophys Acta 2002, 1559:1-9.
32. Sunami T, Matsuura T, Suzuki H, Yomo T. Synthesis of functional proteins within liposomes. Methods Mol Biol 2010, 607:243-256.
33. Harada T, Discher DE. Materials science: bubble wrap of cell-like aggregates. Nature 2011, 471:172-173.
34. Oberholzer T, Albrizio M, Luisi PL. Polymerase chain reaction in liposomes. Chem Biol 1995, 2:677-682.
35. Lande MB, Donovan JM, Zeidel ML. The relationship between membrane fluidity and permeabilities to water, solutes, ammonia, and protons. J Gen Physiol 1995, 106:67-84.
36. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 1996, 274:1859-1866.
37. Gardner PM, Winzer K, Davis BG. Sugar synthesis in a protocellular model leads to a cell signalling response in bacteria. Nat Chem 2009, 1:377-383.
38. Noireaux V, Libchaber A. A vesicle bioreactor as a step toward an artificial cell assembly. Proc Natl Acad Sci U S A 2004, 101:17669-17674.
39. Girsch SJ, Peracchia C. Lens cell-to-cell channel protein: I. Self-assembly into liposomes and permeability regulation by calmodulin. J Membr Biol 1985, 83:217-225.
40. Nikaido H, Rosenberg EY. Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins. J Bacteriol 1983, 153:241-252.
41. Zeidel ML, Ambudkar SV, Smith BL, Agre P. Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 1992, 31:7436-7440.
42. Karlsson M, Sott K, Davidson M, Cans AS, Linderholm P, Chiu D, Orwar O. Formation of geometrically complex lipid nanotube-vesicle networks of higher-order topologies. Proc Natl Acad Sci U S A 2002, 99:11573-11578.
43. Terasawa H, Nishimura K, Suzuki H, Matsuura T, Yomo T. Coupling of the fusion and budding of giant phospholipid vesicles containing macromolecules. Proc Natl Acad Sci U S A 2012, 109:5942-5947.
44. Szostak JW, Bartel DP, Luisi PL. Synthesizing life. Nature 2001, 409:387-390.
45. Hanczyc MM, Szostak JW. Replicating vesicles as models of primitive cell growth and division. Curr Opin Chem Biol 2004, 8:660-664.
46. Walde P, Wick R, Fresta M, Mangone A, Luisi PL. Autopoietic self-reproduction of fatty acid vesicles. J Am Chem Soc 1994, 116:11649-11654.
47. Kurihara K, Tamura M, Shohda K, Toyota T, Suzuki K, Sugawara T. Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nat Chem 2011, 3:775-781.
48. Caschera F, Sunami T, Matsuura T, Suzuki H, Hanczyc MM, Yomo T. Programmed vesicle fusion triggers gene expression. Langmuir 2011, 27:13082-13090.
49. Zan GH, Tan CM, Deserno M, Lanni F, Losche M. Hemifusion of giant unilamellar vesicles with planar hydrophobic surfaces: a fluorescence microscopy study. Soft Matter 2012, 8:10877-10886.
50. Zimmerman SB, Trach SO. Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 1991, 222:599-620.
51. Minton AP. The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 2001, 276:10577-10580.
52. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, Sasaki DY, Sherman MB, Geissler PL, Fletcher DA, Hayden CC. Membrane bending by protein-protein crowding. Nat Cell Biol 2012, 14:944-949.
53. Hosoda K, Sunami T, Kazuta Y, Matsuura T, Suzuki H, Yomo T. Quantitative study of the structure of multilamellar giant liposomes as a container of protein synthesis reaction. Langmuir 2008, 24:13540-13548.
54. Leduc PR, Wong MS, Ferreira PM, Groff RE, Haslinger K, Koonce MP, Lee WY, Love JC, McCammon JA, Monteiro-Riviere NA, et al. Towards an in vivo biologically inspired nanofactory. Nat Nanotechnol 2007, 2:3-7.
55. Bourget L, Chang TM. Phenylalanine ammonia-lyase immobilized in microcapsules for the depletion of phenylalanine in plasma in phenylketonuric rat model. Biochim Biophys Acta 1986, 883:432-438.
56. Fernandes R, Roy V, Wu HC, Bentley WE. Engineered biological nanofactories trigger quorum sensing response in targeted bacteria. Nat Nanotechnol 2010, 5:213-217.
57. Noireaux V, Maeda YT, Libchaber A. Development of an artificial cell, from self-organization to computation and self-reproduction. Proc Natl Acad Sci U S A 2011, 108:3473-3480.
58. Karzbrun E, Shin J, Bar-Ziv RH, Noireaux V. Coarse-grained dynamics of protein synthesis in a cell-free system. Phys Rev Lett 2011, 106:048104.
59. Shimizu Y, Inoue A, Tomari Y, Suzuki T, Yokogawa T, Nishikawa K, Ueda T. Cell-free translation reconstituted with purified components. Nat Biotechnol 2001, 19:751-755.
60. Matsuura T, Kazuta Y, Aita T, Adachi J, Yomo T. Quantifying epistatic interactions among the components constituting the protein translation system. Mol Syst Biol 2009, 5:297.
61. Shin J, Noireaux V. Efficient cell-free expression with the endogenous E. coli RNA polymerase and sigma factor 70. J Biol Eng 2010, 4:8.
62. Liu DV, Zawada JF, Swartz JR. Streamlining Escherichia coli S30 extract preparation for economical cell-free protein synthesis. Biotechnol Prog 2005, 21:460-465.
63. Martin CT, Coleman JE. Kinetic analysis of T7 RNA polymerase-promoter interactions with small synthetic promoters. Biochemistry 1987, 26:2690-2696.
64. Studier FW, Moffatt BA. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 1986, 189:113-130.
65. Jewett MC, Forster AC. Update on designing and building minimal cells. Curr Opin Biotechnol 2010, 21:697-703.
66. Kim DM, Swartz JR. Prolonging cell-free protein synthesis with a novel ATP regeneration system. Biotechnol Bioeng 1999, 66:180-188.
67. Spirin AS, Baranov VI, Ryabova LA, Ovodov SY, Alakhov YB. A continuous cell-free translation system capable of producing polypeptides in high yield. Science 1988, 242:1162-1164.
68. Yu W, Sato K, Wakabayashi M, Nakaishi T, Ko-Mitamura EP, Shima Y, Urabe I, Yomo T. Synthesis of functional protein in liposome. J Biosci Bioeng 2001, 92:590-593.
69. Murtas G, Kuruma Y, Bianchini P, Diaspro A, Luisi PL. Protein synthesis in liposomes with a minimal set of enzymes. Biochem Biophys Res Commun 2007, 363:12-17.
70. Kuruma Y, Stano P, Ueda T, Luisi PL. A synthetic biology approach to the construction of membrane proteins in semi-synthetic minimal cells. Biochim Biophys Acta 2009, 1788:567-574.
71. Sunami T, Kita H, Hosoda K, Matsuura T, Suzuki H, Yomo T. Chapter 2 - Detection and analysis of protein synthesis and RNA replication in giant liposomes. Methods Enzymol 2009, 464:19-30.
72. Sunami T, Hosoda K, Suzuki H, Matsuura T, Yomo T. Cellular compartment model for exploring the effect of the lipidic membrane on the kinetics of encapsulated biochemical reactions. Langmuir 2010, 26:8544-8551.
73. Ramachandran N, Hainsworth E, Bhullar B, Eisenstein S, Rosen B, Lau AY, Walter JC, LaBaer J. Self-assembling protein microarrays. Science 2004, 305:86-90.
74. Traub P, Nomura M. Structure and function of E. coli ribosomes. V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. Proc Natl Acad Sci U S A 1968, 59:777-784.
75. Maki JA, Culver GM. Recent developments in factor-facilitated ribosome assembly. Methods 2005, 36:313-320.
76. Nierhaus KH, Dohme F. Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc Natl Acad Sci U S A 1974, 71:4713-4717.
77. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415:389-395.
78. Hancock RE, Chapple DS. Peptide antibiotics. Antimicrob Agents Chemother 1999, 43:1317-1323.
79. Loose C, Jensen K, Rigoutsos I, Stephanopoulos G. A linguistic model for the rational design of antimicrobial peptides. Nature 2006, 443:867-869.
80. Jones DT, Woods DR. Acetone-butanol fermentation revisited. Microbiol Rev 1986, 50:484-524.
81. Zhang YH. Production of biocommodities and bioelectricity by cell-free synthetic enzymatic pathway biotransformations: challenges and opportunities. Biotechnol Bioeng 2010, 105:663-677.
82. Atkins JF, Gesteland RF, Cech T. RNA Worlds: From Life's Origins to Diversity in Gene Regulation. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2011.
83. Paul N, Joyce GF. A self-replicating ligase ribozyme. Proc Natl Acad Sci U S A 2002, 99:12733-12740.
84. Noireaux V, Bar-Ziv R, Libchaber A. Principles of cell-free genetic circuit assembly. Proc Natl Acad Sci U S A 2003, 100:12672-12677.
85. Lincoln TA, Joyce GF. Self-sustained replication of an RNA enzyme. Science 2009, 323:1229-1232.
86. Adamala K, Szostak JW. Nonenzymatic template-directed RNA synthesis inside model protocells. Science 2013, 342:1098-1100.
87. Ichihashi N, Matsuura T, Kita H, Sunami T, Suzuki H, Yomo T. Constructing partial models of cells. Cold Spring Harb Perspect Biol 2010, 2:a004945.
88. Pinheiro VB, Taylor AI, Cozens C, Abramov M, Renders M, Zhang S, Chaput JC, Wengel J, Peak-Chew SY, McLaughlin SH, et al. Synthetic genetic polymers capable of heredity and evolution. Science 2012, 336:341-344.
89. Nourian Z, Roelofsen W, Danelon C. Triggered gene expression in fed-vesicle microreactors with a multifunctional membrane. Angew Chem Int Ed Engl 2012, 51:3114-3118.
90. Schroeder A, Goldberg MS, Kastrup C, Wang YX, Jiang S, Joseph BJ, Levins CG, Kannan ST, Langer R, Anderson DG. Remotely activated protein-producing nanoparticles. Nano Lett 2012, 12:2685-2689.
91. Kobori S, Ichihashi N, Kazuta Y, Yomo T. A controllable gene expression system in liposomes that includes a positive feedback loop. Mol Biosyst 2013, 9:1282-1285.
92. Karig DK, Jung SY, Srijanto B, Collier CP, Simpson ML. Probing cell-free gene expression noise in femtoliter volumes. ACS Synth Biol 2013, 2:497-505.
93. Niederholtmeyer H, Stepanova V, Maerkl SJ. Implementation of cell-free biological networks at steady state. Proc Natl Acad Sci U S A 2013, 110:15985-15990.
94. Laurent TC. The interaction between polysaccharides and other macromolecules. 5. The solubility of proteins in the presence of dextran. Biochem J 1963, 89:253-257.
95. Wang Y, Guo L, Golding I, Cox EC, Ong NP. Quantitative transcription factor binding kinetics at the single-molecule level. Biophys J 2009, 96:609-620.
96. Friedman LJ, Gelles J. Mechanism of transcription initiation at an activator-dependent promoter defined by single-molecule observation. Cell 2012, 148:679-689.
97. Hammar P, Leroy P, Mahmutovic A, Marklund EG, Berg OG, Elf J. The lac repressor displays facilitated diffusion in living cells. Science 2012, 336:1595-1598.
98. Billerbeck S, Harle J, Panke S. The good of two worlds: increasing complexity in cell-free systems. Curr Opin Biotechnol 2013, 24:1037-1043.
99. Harris DC, Jewett MC. Cell-free biology: exploiting the interface between synthetic biology and synthetic chemistry. Curr Opin Biotechnol 2012, 23:672-678.
100. Forster AC, Church GM. Towards synthesis of a minimal cell. Mol Syst Biol 2006, 2:45.
101. Fujii S, Matsuura T, Sunami T, Kazuta Y, Yomo T. In vitro evolution of alpha-hemolysin using a liposome display. Proc Natl Acad Sci U S A 2013, 110:16796-16801.
102. Agresti JJ, Antipov E, Abate AR, Ahn K, Rowat AC, Baret JC, Marquez M, Klibanov AM, Griffiths AD, Weitz DA. Ultrahigh-throughput screening in drop-based microfluidics for directed evolution. Proc Natl Acad Sci U S A 2010, 107:4004-4009.
103. Lentini R, Forlin M, Martini L, Del Bianco C, Spencer AC, Torino D, Mansy SS. Fluorescent proteins and in vitro genetic organization for cell-free synthetic biology. ACS Synth Biol 2013, 2:482-489.
104. Chappell J, Jensen K, Freemont PS. Validation of an entirely in vitro approach for rapid prototyping of DNA regulatory elements for synthetic biology. Nucleic Acids Res 2013, 41:3471-3481.
105. Karig DK, Iyer S, Simpson ML, Doktycz MJ. Expression optimization and synthetic gene networks in cell-free systems. Nucleic Acids Res 2012, 40:3763-3774.
106. Shin J, Jardine P, Noireaux V. Genome replication, synthesis, and assembly of the bacteriophage T7 in a single cell-free reaction. ACS Synth Biol 2012, 1:408-413.