Partitioning Variability of a Compartmentalized in Vitro Transcriptional Thresholding Circuit

ACS Synthetic Biology

Volumn 4, Issue 10, 2015, Pages 1136-1143

  Kapsner, Korbinian ^a   Simmel, Friedrich C ^a,b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b NANOSYSTEMS INITIATIVE MUNICH NIM   (Germany)

Author keywords

emulsion droplets; genelet circuits; in vitro transcription; stochasticity

Indexed keywords

COMPLEMENTARY DNA; RNA;

ARTICLE; CELL COMPARTMENTALIZATION; ENCAPSULATION; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; MICROEMULSION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA TRANSCRIPTION; STOICHIOMETRY; CHEMISTRY; GENETICS; THEORETICAL MODEL;

MODELS, THEORETICAL; RNA;

EID: 84944727753     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.5b00051     Document Type: Article

References (54)

1. Theberge, A. B., Courtois, F., Schaerli, Y., Fischlechner, M., Abell, C., Hollfelder, F., and Huck, W. T. S. (2010) Microdroplets in microuidics: an evolving platform for discoveries in chemistry and biology Angew. Chem., Int. Ed. 49, 5846-5868
2. Tawfik, D. S. and Griffiths, A. D. (1998) Man-made cell-like compartments for molecular evolution Nat. Biotechnol. 16, 652-656
3. Griffiths, A. D. and Tawfik, D. S. (2003) Directed evolution of an extremely fast phosphotriesterase by in vitro compartmentalization EMBO J. 22, 24-35
4. Paegel, B. M. and Joyce, G. F. (2010) Microuidic compartmentalized directed evolution Chem. Biol. 17, 717-724
5. Agresti, J. J., Antipov, E., Abate, A. R., Ahn, K., Rowat, A. C., Baret, J.-C., Marquez, M., Klibanov, A. M., Griffiths, A. D., and Weitz, D. A. (2010) Ultrahigh-throughput screening in drop-based microfluidics for directed evolution Proc. Natl. Acad. Sci. U. S. A. 107, 4004-4009
6. Kintses, B., Hein, C., Mohamed, M. F., Fischlechner, M., Courtois, F., Lainé, C., and Hollfelder, F. (2012) Picoliter cell lysate assays in micro uidic droplet compartments for directed enzyme evolution Chem. Biol. 19, 1001-1009
7. Ellefson, J. W., Meyer, A. J., Hughes, R. A., Cannon, J. R., Brodbelt, J. S., and Ellington, A. D. (2013) Directed evolution of genetic parts and circuits by compartmentalized partnered replication Nat. Biotechnol. 32, 97-101
8. Nakano, M., Komatsu, J., Matsuura, S., and Takashima, K. et al. 2003, Single-molecule PCR using water-in-oil emulsion J. Biotechnol. 102, 117-124
9. Williams, R., Peisajovich, S. G., Miller, O. J., Magdassi, S., Tawfik, D. S., and Griffiths, A. D. (2006) Amplification of complex gene libraries by emulsion PCR Nat. Methods 3, 545-550
10. Schütze, T., Rubelt, F., Repkow, J., Greiner, N., Erdmann, V. A., Lehrach, H., Konthur, Z., and Glökler, J. (2011) A streamlined protocol for emulsion polymerase chain reaction and subsequent purification Anal. Biochem. 410, 155-157
11. Metzker, M. L. (2009) Sequencing technologies-the next generation Nat. Rev. Genet. 11, 31-46
12. Kalisky, T. and Quake, S. (2011) Single-cell genomics Nat. Methods 8, 311-314
13. Pohorille, A. and Deamer, D. (2002) Artificial cells: prospects for biotechnology Trends Biotechnol. 20, 123
14. Noireaux, V., Maeda, Y. T., and Libchaber, A. (2011) Development of an artificial cell, from selforganization to computation and self-reproduction Proc. Natl. Acad. Sci. U. S. A. 108, 3473-3480
15. Attwater, J. and Holliger, P. (2014) A synthetic approach to abiogenesis Nat. Methods 11, 495-498
16. Luisi, P. L., Ferri, F., and Stano, P. (2006) Approaches to semi-synthetic minimal cells: a review Naturwissenschaften 93, 1-13
17. Rasmussen, S. (2009) Protocells: Bridging Nonliving and Living Matter, MIT Press, Cambridge, MA.
18. Fischer, A., Franco, A., and Oberholzer, T. (2002) Giant vesicles as microreactors for enzymatic mRNA synthesis ChemBioChem 3, 409-417
19. Monnard, P. (2003) Liposome-entrapped polymerases as models for microscale/nanoscale bioreactors J. Membr. Biol. 191, 87-97
20. Hanczyc, M. M., Fujikawa, S. M., and Szostak, J. W. (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division Science 302, 618-22
21. Ishikawa, K., Sato, K., Shima, Y., Urabe, I., and Yomo, T. (2004) Expression of a cascading genetic network within liposomes FEBS Lett. 576, 387-390
22. Noireaux, V. and Libchaber, A. (2004) A vesicle bioreactor as a step toward an artificial cell assembly Proc. Natl. Acad. Sci. U. S. A. 101, 17669-17674
23. Nourian, Z., Roelofsen, W., and Danelon, C. (2012) Triggered gene expression in fed-vesicle microreactors with a multifunctional membrane Angew. Chem., Int. Ed. 51, 3114-3118
24. Nourian, Z. and Danelon, C. (2013) Linking genotype and phenotype in protein synthesizing liposomes with external supply of resources ACS Synth. Biol. 2, 186-93
25. Tan, C., Saurabh, S., Bruchez, M. P., Schwartz, R., and Leduc, P. (2013) Molecular crowding shapes gene expression in synthetic cellular nanosystems Nat. Nanotechnol. 1-7
26. Maeda, Y. T., Nakadai, T., Shin, J., Uryu, K., Noireaux, V., and Libchaber, A. (2012) Assembly of MreB filaments on liposome membranes: a synthetic biology approach ACS Synth. Biol. 1, 53-9
27. Shin, J. and Noireaux, V. (2012) An E. coli cell-free expression toolbox: application to synthetic gene circuits and artificial cells ACS Synth. Biol. 1, 29-41
28. Karzbrun, E., Tayar, A. M., Noireaux, V., and Bar-Ziv, R. H. (2014) Programmable on-chip DNA compartments as artificial cells Science 345, 829-832
29. Matsuura, T., Hosoda, K., Kazuta, Y., Ichihashi, N., Suzuki, H., and Yomo, T. (2012) Effects of compartment size on the kinetics of intracompartmental multimeric protein synthesis ACS Synth. Biol. 1, 431-437
30. Sokolova, E., Spruijt, E., Hansen, M. M. K., Dubuc, E., Groen, J., Chokkalingam, V., Piruska, A., Heus, H. A., and Huck, W. T. S. (2013) Enhanced transcription rates in membrane free protocells formed by coacervation of cell lysate Proc. Natl. Acad. Sci. U. S. A. 110, 11692-11697
31. Soga, H., Fujii, S., Yomo, T., Kato, Y., Watanabe, H., and Matsuura, T. (2013) In vitro membrane protein synthesis inside cell-sized vesicles reveals the dependence of membrane protein integration on vesicle volume ACS Synth. Biol. 3, 372-379
32. Gillespie, D. T. (1977) Exact stochastic simulation of coupled chemical-reactions J. Phys. Chem. 81, 2340-2361
33. Fallah-Araghi, A., Meguellati, K., Baret, J.-C., Harrak, A. E., Mangeat, T., Karplus, M., Ladame, S., Marques, C. M., and Griffiths, A. D. (2014) Enhanced chemical synthesis at soft interfaces: a universal reaction-adsorption mechanism in microcompartments Phys. Rev. Lett. 112, 028301
34. Zhou, H.-X., Rivas, G., and Minton, A. P. (2008) Macromolecular crowding and confinement: Biochemical, biophysical, and potential physiological consequences Annu. Rev. Biophys. 37, 375-397
35. Toiya, M., Vanag, V., and Epstein, I. (2008) Diffusively coupled chemical oscillators in a microfluidic assembly Angew. Chem., Int. Ed. 47, 7753-7755
36. Epstein, I., Vanag, V., Balazs, A., Kuksenok, O., Dayal, P., and Bhattacharya, A. (2011) Chemical oscillators in structured media Acc. Chem. Res. 45, 2160-2168
37. Vanag, V. and Epstein, I. (2001) Pattern formation in a tunable medium: the Belousov- Zhabotinsky reaction in an aerosol OT microemulsion Phys. Rev. Lett. 87, 228301
38. Tompkins, N., Li, N., Girabawe, C., Heymann, M., Ermentrout, G. B., Epstein, I. R., and Fraden, S. (2014) Testing Turing's theory of morphogenesis in chemical cells Proc. Natl. Acad. Sci. U. S. A. 111, 4397-4402
39. Hasatani, K., Leocmach, M., Genot, A. J., Estevez-Torres, A., Fujii, T., and Rondelez, Y. (2013) High-throughput and long-term observation of compartmentalized biochemical oscillators Chem. Commun. (Cambridge, U. K.) 49, 8090-8092
40. Weitz, M., Kim, J., Kapsner, K., Winfree, E., Franco, E., and Simmel, F. C. (2014) Diversity in the dynamical behaviour of a compartmentalized programmable biochemical oscillator Nat. Chem. 6, 295-302
41. Roach, L. S., Song, H., and Ismagilov, R. F. (2005) Controlling nonspecific protein adsorption in a plug-based microfluidic system by controlling interfacial chemistry using fluorous-phase surfactants Anal. Chem. 77, 785-796
42. Liu, Y., Jung, S.-Y., and Collier, C. P. (2009) Shear-driven redistribution of surfactant affects enzyme activity inwell-mixed femtoliter droplets Anal. Chem. 81, 4922-4928
43. Kim, J. and Winfree, E. (2011) Synthetic in vitro transcriptional oscillators Mol. Syst. Biol. 7, 465
44. Franco, E., Friedrichs, E., Kim, J., Murray, R., Winfree, E., and Simmel, F. C. (2011) Timing molecular motion and production with a synthetic transcriptional clock Proc. Natl. Acad. Sci. U. S. A. 108, E784-E793
45. Kim, J., White, K. S., and Winfree, E. (2006) Construction of an in vitro bistable circuit from synthetic transcriptional switches Mol. Syst. Biol. 1, 68
46. Kim, J., Khetarpal, I., Sen, S., and Murray, R. M. (2014) Synthetic circuit for exact adaptation and fold-change detection Nucleic Acids Res. 42, 6078-6089
47. Maslak, M. and Martin, C. T. (1994) Effects of solution conditions on the steady-state kinetics of initiation of transcription by T7 RNA polymerase Biochemistry 33, 6918-24
48. Tyagi, S. and Kramer, F. (1996) Molecular beacons: Probes that fluoresce upon hybridization Nat. Biotechnol. 14, 303-308
49. Holtze, C., Rowat, A. C., Agresti, J. J., Hutchison, J. B., Angile, F. E., Schmitz, C. H. J., Koster, S., Duan, H., Humphry, K. J., Scanga, R. A., Johnson, J. S., Pisignano, D., and Weitz, D. A. (2008) Biocompatible surfactants for water-in-fluorocarbon emulsions Lab Chip 8, 1632-1639
50. Karzbrun, E., Shin, J., Bar-Ziv, R., and Noireaux, V. (2011) Coarse-grained dynamics of protein synthesis in a cell-free system Phys. Rev. Lett. 106, 048104
51. Epstein, B. (1947) The mathematical description of certain breakage mechanisms leading to the logarithmico-normal distribution J. Franklin Inst. 244, 471-477
52. Koch, A. (1966) The logarithm in biology 1. Mechanisms generating the log-normal distribution exactly J. Theor. Biol. 12, 276-290
53. Thattai, M. and van Oudenaarden, A. (2001) Intrinsic noise in gene regulatory networks Proc. Natl. Acad. Sci. U. S. A. 98, 8614-8619
54. Edelstein, A., Amodaj, N., Hoover, K., Vale, R., and Stuurman, N. (2001) Current Protocols in Molecular Biology, John Wiley & Sons, Inc., New York.