Enzyme-free nucleic acid dynamical systems

Science

Volumn 358, Issue 6369, 2017, Pages

  Srinivas, Niranjan ^a   Parkin, James ^b   Seelig, Georg ^c   Winfree, Erik ^a,b   Soloveichik, David ^d  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b California Institute of Technology   (United States)

^c University of Washington   (United States)

^d The University of Texas at Austin   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ENZYME FREE NUCLEIC ACID; NUCLEIC ACID; OLIGONUCLEOTIDE; UNCLASSIFIED DRUG;

BIOTECHNOLOGY; CHEMICAL REACTION; DNA; ENZYME ACTIVITY; MOLECULAR ANALYSIS; NETWORK ANALYSIS; NUCLEIC ACID;

ARTICLE; BASE PAIRING; DNA STRAND; EQUIPMENT DESIGN; GENE STRUCTURE; GENETIC CODE; LABORATORY AUTOMATION; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR SYSTEMATICS; MOLECULE; NANOTECHNOLOGY; NETWORK LEARNING; NUCLEIC ACID ANALYSIS; PRIORITY JOURNAL; SEQUENCE ANALYSIS; CHEMISTRY; COMPUTER LANGUAGE; NUCLEOTIDE SEQUENCE;

BASE PAIRING; BASE SEQUENCE; DNA; PROGRAMMING LANGUAGES;

EID: 85040180009     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aal2052     Document Type: Article

References (82)

1. W. C. Bray, A periodic reaction in homogeneous solution and its relation to catalysis. J. Am. Chem. Soc. 43, 1262-1267 (1921). doi: 10.1021/ja01439a007
2. B. P. Belousov, Collection of Abstracts on Radiation Medicine (Medgiz, 1959), pp. 145-147.
3. I. R. Epstein, J. A. Pojman, An Introduction to Nonlinear Chemical Dynamics: Oscillations, Waves, Patterns, and Chaos (Oxford Univ. Press, 1998).
4. T. S. Gardner, C. R. Cantor, J. J. Collins, Construction of a genetic toggle switch in Escherichia coli. Nature 403, 339-342 (2000). doi: 10.1038/35002131; pmid: 10659857
5. M. B. Elowitz, S. Leibler, A synthetic oscillatory network of transcriptional regulators. Nature 403, 335-338 (2000). doi: 10.1038/35002125; pmid: 10659856
6. M. R. Atkinson, M. A. Savageau, J. T. Myers, A. J. Ninfa, Development of genetic circuitry exhibiting toggle switch or oscillatory behavior in Escherichia coli. Cell 113, 597-607 (2003). doi: 10.1016/S0092-8674(03)00346-5; pmid: 12787501
7. J. Stricker et al., A fast, robust and tunable synthetic gene oscillator. Nature 456, 516-519 (2008). doi: 10.1038/nature07389; pmid: 18971928
8. B. Wlotzka, J. S. McCaskill, A molecular predator and its prey: Coupled isothermal amplification of nucleic acids. Chem. Biol. 4, 25-33 (1997). doi: 10.1016/S1074-5521(97) 90234-9; pmid: 9070425
9. J. Kim, K. S. White, E. Winfree, Construction of an in vitro bistable circuit from synthetic transcriptional switches. Mol. Syst. Biol. 2, 68 (2006). doi: 10.1038/msb4100099; pmid: 17170763
10. J. Kim, E. Winfree, Synthetic in vitro transcriptional oscillators. Mol. Syst. Biol. 7, 465 (2011). doi: 10.1038/msb.2010.119; pmid: 21283141
11. K. Montagne, R. Plasson, Y. Sakai, T. Fujii, Y. Rondelez, Programming an in vitro DNA oscillator using a molecular networking strategy. Mol. Syst. Biol. 7, 466 (2011). doi: 10.1038/msb.2010.120; pmid: 21283142
12. A. Padirac, T. Fujii, Y. Rondelez, Bottom-up construction of in vitro switchable memories. Proc. Natl. Acad. Sci. U.S.A. 109, E3212-E3220 (2012). doi: 10.1073/pnas.1212069109; pmid: 23112180
13. T. Fujii, Y. Rondelez, Predator-prey molecular ecosystems. ACS Nano 7, 27-34 (2013). doi: 10.1021/nn3043572; pmid: 23176248
14. S. N. Semenov et al., Rational design of functional and tunable oscillating enzymatic networks. Nat. Chem. 7, 160-165 (2015). doi: 10.1038/nchem.2142; pmid: 25615670
15. D. Bray, Protein molecules as computational elements in living cells. Nature 376, 307-312 (1995). doi: 10.1038/376307a0; pmid: 7630396
16. J. J. Tyson, K. C. Chen, B. Novak, Sniffers, buzzers, toggles and blinkers: Dynamics of regulatory and signaling pathways in the cell. Curr. Opin. Cell Biol. 15, 221-231 (2003). doi: 10.1016/S0955-0674(03)00017-6; pmid: 12648679
17. F. Horn, R. Jackson, General mass action kinetics. Arch. Ration. Mech. Anal. 47, 81-116 (1972). doi: 10.1007/BF00251225
18. P. Érdi, J. Tóth, Mathematical Models of Chemical Reactions: Theory and Applications of Deterministic and Stochastic Models (Princeton University Press, 1989).
19. M. Korzuhin, Oscillatory Processes in Biological and Chemical Systems (Nauka, 1967), pp. 231-251.
20. W. Klonowski, Simplifying principles for chemical and enzyme reaction kinetics. Biophys. Chem. 18, 73-87 (1983). doi: 10.1016/0301-4622(83)85001-7; pmid: 6626688
21. K. Oishi, E. Klavins, Biomolecular implementation of linear I/O systems. IET Syst. Biol. 5, 252-260 (2011). doi: 10.1049/iet-syb.2010.0056; pmid: 21823756
22. A. Hjelmfelt, J. Ross, Implementation of logic functions and computations by chemical kinetics. Physica D 84, 180-193 (1995). doi: 10.1016/0167-2789(95)00014-U
23. A. Hjelmfelt, E. D. Weinberger, J. Ross, Chemical implementation of neural networks and Turing machines. Proc. Natl. Acad. Sci. U.S.A. 88, 10983-10987 (1991). doi: 10.1073/pnas.88.24.10983; pmid: 1763012
24. J. Aspnes, E. Ruppert, An introduction to population protocols, in Middleware for Network Eccentric and Mobile Applications, B. Garbinato, H. Miranda, L. Rodrigues, Eds. (Springer-Verlag, 2009), pp. 97-120.
25. A. Hjelmfelt, E. D. Weinberger, J. Ross, Chemical implementation of finite-state machines. Proc. Natl. Acad. Sci. U.S.A. 89, 383-387 (1992). doi: 10.1073/pnas.89.1.383; pmid: 11607249
26. D. Y. Zhang, G. Seelig, Dynamic DNA nanotechnology using strand-displacement reactions. Nat. Chem. 3, 103-113 (2011). doi: 10.1038/nchem.957; pmid: 21258382
27. J. SantaLucia Jr., D. Hicks, The thermodynamics of DNA structural motifs. Annu. Rev. Biophys. Biomol. Struct. 33, 415-440 (2004). doi: 10.1146/annurev. biophys.32.110601.141800; pmid: 15139820
28. J. N. Zadeh et al., NUPACK: Analysis and design of nucleic acid systems. J. Comput. Chem. 32, 170-173 (2011). doi: 10.1002/jcc.v32:1; pmid: 20645303
29. N. C. Seeman, De novo design of sequences for nucleic acid structural engineering. J. Biomol. Struct. Dyn. 8, 573-581 (1990). doi: 10.1080/07391102.1990.10507829; pmid: 2100519
30. R. M. Dirks, M. Lin, E. Winfree, N. A. Pierce, Paradigms for computational nucleic acid design. Nucleic Acids Res. 32, 1392-1403 (2004). doi: 10.1093/nar/gkh291; pmid: 14990744
31. J. N. Zadeh, B. R. Wolfe, N. A. Pierce, Nucleic acid sequence design via efficient ensemble defect optimization. J. Comput. Chem. 32, 439-452 (2011). doi: 10.1002/jcc.21633; pmid: 20717905
32. B. R. Wolfe, N. A. Pierce, Sequence design for a test tube of interacting nucleic acid strands. ACS Synth. Biol. 4, 1086-1100 (2015). doi: 10.1021/sb5002196; pmid: 25329866
33. B. R. Wolfe, N. J. Porubsky, J. N. Zadeh, R. M. Dirks, N. A. Pierce, Constrained multistate sequence design for nucleic acid reaction pathway engineering. J. Am. Chem. Soc. 139, 3134-3144 (2017). doi: 10.1021/jacs.6b12693; pmid: 28191938
34. B. Yurke, A. P. Mills Jr., Using DNA to power nanostructures. Genet. Program. Evolvable Mach. 4, 111-122 (2003). doi: 10.1023/A:1023928811651
35. D. Y. Zhang, E. Winfree, Control of DNA strand displacement kinetics using toehold exchange. J. Am. Chem. Soc. 131, 17303-17314 (2009). doi: 10.1021/ja906987s; pmid: 19894722
36. N. Srinivas et al., On the biophysics and kinetics of toeholdmediated DNA strand displacement. Nucleic Acids Res. 41, 10641-10658 (2013). doi: 10.1093/nar/gkt801; pmid: 24019238
37. B. Yurke, A. J. Turberfield, A. P. Mills Jr., F. C. Simmel, J. L. Neumann, A DNA-fuelled molecular machine made of DNA. Nature 406, 605-608 (2000). doi: 10.1038/35020524; pmid: 10949296
38. G. Seelig, D. Soloveichik, D. Y. Zhang, E. Winfree, Enzyme-free nucleic acid logic circuits. Science 314, 1585-1588 (2006). doi: 10.1126/science.1132493; pmid: 17158324
39. L. Qian, E. Winfree, Scaling up digital circuit computation with DNA strand displacement cascades. Science 332, 1196-1201 (2011). doi: 10.1126/science.1200520; pmid: 21636773
40. D. Y. Zhang, A. J. Turberfield, B. Yurke, E. Winfree, Engineering entropy-driven reactions and networks catalyzed by DNA. Science 318, 1121-1125 (2007). doi: 10.1126/science.1148532; pmid: 18006742
41. P. Yin, H. M. T. Choi, C. R. Calvert, N. A. Pierce, Programming biomolecular self-assembly pathways. Nature 451, 318-322 (2008). doi: 10.1038/nature06451; pmid: 18202654
42. J. P. Sadowski, C. R. Calvert, D. Y. Zhang, N. A. Pierce, P. Yin, Developmental self-assembly of a DNA tetrahedron. ACS Nano 8, 3251-3259 (2014). doi: 10.1021/nn4038223; pmid: 24720462
43. D. Soloveichik, G. Seelig, E. Winfree, DNA as a universal substrate for chemical kinetics. Proc. Natl. Acad. Sci. U.S.A. 107, 5393-5398 (2010). doi: 10.1073/pnas.0909380107; pmid: 20203007
44. L. Cardelli, Two-domain DNA strand displacement. Math. Struct. Comput. Sci. 23, 247-271 (2013). doi: 10.1017/S0960129512000102
45. Y.-J. Chen et al., Programmable chemical controllers made from DNA. Nat. Nanotechnol. 8, 755-762 (2013). doi: 10.1038/nnano.2013.189; pmid: 24077029
46. M. Lachmann, G. Sella, The computationally complete ant colony: global coordination in a system with no hierarchy, in Advances in Artificial Life (Lecture Notes in Computer Science), F. Morán, A. Moreno, J. J. Merelo, P. Chacón, Eds. (Springer, 1995), pp. 784-800.
47. L. Cardelli, Artificial biochemistry, in Algorithmic Bioprocesses, A. Condon, D. Harel, J. N. Kok, A. Salomaa, E. Winfree, Eds. (Springer, 2009), pp. 429-462.
48. T. Reichenbach, M. Mobilia, E. Frey, Coexistence versus extinction in the stochastic cyclic Lotka-Volterra model. Phys. Rev. E 74, 051907 (2006). doi: 10.1103/PhysRevE.74.051907; pmid: 17279939
49. A. Dobrinevski, E. Frey, Extinction in neutrally stable stochastic Lotka-Volterra models. Phys. Rev. E 85, 051903 (2012). doi: 10.1103/PhysRevE.85.051903; pmid: 23004784
50. M. R. Lakin, S. Youssef, L. Cardelli, A. Phillips, Abstractions for DNA circuit design. J. R. Soc. Interface 9, 470-486 (2012). doi: 10.1098/rsif.2011.0343; pmid: 21775321
51. L. P. Reynaldo, A. V. Vologodskii, B. P. Neri, V. I. Lyamichev, The kinetics of oligonucleotide replacements. J. Mol. Biol. 297, 511-520 (2000). doi: 10.1006/jmbi.2000.3573; pmid: 10715217
52. A. J. Genot, D. Y. Zhang, J. Bath, A. J. Turberfield, Remote toehold: A mechanism for flexible control of DNA hybridization kinetics. J. Am. Chem. Soc. 133, 2177-2182 (2011). doi: 10.1021/ja1073239; pmid: 21268641
53. D. Y. Zhang, E. Winfree, Robustness and modularity properties of a non-covalent DNA catalytic reaction. Nucleic Acids Res. 38, 4182-4197 (2010). doi: 10.1093/nar/gkq088; pmid: 20194118
54. DNA and Natural Algorithms Group github page, https://github.com/DNA-and-Natural-Algorithms-Group
55. C. G. Evans, E. Winfree, in DNA Computing and Molecular Programming, vol. 8141, Lecture Notes in Computer Science, D. Soloveichik, B. Yurke, Eds. (Springer, 2013), pp. 61-75.
56. L. Cardelli, Strand algebras for DNA computing. Nat. Comput. 10, 407-428 (2011). doi: 10.1007/s11047-010-9236-7
57. L. Qian, D. Soloveichik, E. Winfree, Turing-universal computation with DNA polymers, in DNA Computing and Molecular Programming, vol 6518, Lecture Notes in Computer Science, Y. Sakakibara, Y. Mi, Eds. (Springer, 2011), pp. 123-140.
58. H. Niederholtmeyer et al., Rapid cell-free forward engineering of novel genetic ring oscillators. eLife 4, e09771 (2015). doi: 10.7554/eLife.09771; pmid: 26430766
59. A. Baccouche, K. Montagne, A. Padirac, T. Fujii, Y. Rondelez, Dynamic DNA-toolbox reaction circuits: A walkthrough. Methods 67, 234-249 (2014). doi: 10.1016/j.ymeth.2014.01.015; pmid: 24495737
60. J. Garamella, R. Marshall, M. Rustad, V. Noireaux, The all E. coli TX-TL Toolbox 2.0: A platform for cell-free synthetic biology. ACS Synth. Biol. 5, 344-355 (2016). doi: 10.1021/acssynbio.5b00296; pmid: 26818434
61. J. Kim, J. J. Hopfield, E. Winfree, Neural network computation by in vitro transcriptional circuits, in Advances in Neural Information Processing Systems, L. K. Saul, Y. Weiss, L. Bottou, Eds. (MIT Press, 2004), pp. 681-688.
62. Y. Shimizu et al., Cell-free translation reconstituted with purified components. Nat. Biotechnol. 19, 751-755 (2001). doi: 10.1038/90802; pmid: 11479568
63. J. M. Schaeffer, C. Thachuk, E. Winfree, Stochastic simulation of the kinetics of multiple interacting nucleic acid strands, in DNA Computing and Molecular Programming, vol. 9211, Lecture Notes in Computer Science, A. Phillips, P. Yin, Eds. (Springer, 2015), pp. 194-211.
64. T. E. Ouldridge, P. Šulc, F. Romano, J. P. K. Doye, A. A. Louis, DNA hybridization kinetics: Zippering, internal displacement and sequence dependence. Nucleic Acids Res. 41, 8886-8895 (2013). doi: 10.1093/nar/gkt687; pmid: 23935069
65. C. Thachuk, E. Winfree, D. Soloveichik, in DNA Computing and Molecular Programming, vol 9211, Lecture Notes in Computer Science, A. Phillips, P. Yin, eds. (Springer, 2015), pp. 133-153.
66. I. R. Epstein, Complex dynamical behavior in "simple" chemical systems. J. Phys. Chem. 88, 187-198 (1984). doi: 10.1021/j150646a007
67. D. Y. Zhang, R. F. Hariadi, H. M. T. Choi, E. Winfree, Integrating DNA strand-displacement circuitry with DNA tile self-assembly. Nat. Commun. 4, 1965 (2013). doi: 10.1038/ncomms2965; pmid: 23756381
68. N. C. Seeman, Structural DNA Nanotechnology (Cambridge University Press, 2016).
69. M. N. Stojanovic, D. M. Kolpashchikov, Modular aptameric sensors. J. Am. Chem. Soc. 126, 9266-9270 (2004). doi: 10.1021/ja032013t; pmid: 15281816
70. E. J. Cho, J.-W. Lee, A. D. Ellington, Applications of aptamers as sensors. Annu. Rev. Anal. Chem. (Palo Alto Calif.) 2, 241-264 (2009). doi: 10.1146/annurev.anchem.1.031207.112851; pmid: 20636061
71. S. Liao, N. C. Seeman, Translation of DNA signals into polymer assembly instructions. Science 306, 2072-2074 (2004). doi: 10.1126/science.1104299; pmid: 15604403
72. Y. He, D. R. Liu, Autonomous multistep organic synthesis in a single isothermal solution mediated by a DNA walker. Nat. Nanotechnol. 5, 778-782 (2010). doi: 10.1038/nnano.2010.190; pmid: 20935654
73. W. Meng et al., An autonomous molecular assembler for programmable chemical synthesis. Nat. Chem. 8, 542-548 (2016). doi: 10.1038/nchem.2495; pmid: 27219697
74. H. Gu, J. Chao, S.-J. Xiao, N. C. Seeman, A proximity-based programmable DNA nanoscale assembly line. Nature 465, 202-205 (2010). doi: 10.1038/nature09026; pmid: 20463734
75. J. Fu, M. Liu, Y. Liu, N. W. Woodbury, H. Yan, Interenzyme substrate diffusion for an enzyme cascade organized on spatially addressable DNA nanostructures. J. Am. Chem. Soc. 134, 5516-5519 (2012). doi: 10.1021/ja300897h; pmid: 22414276
76. S. M. Douglas, I. Bachelet, G. M. Church, A logic-gated nanorobot for targeted transport of molecular payloads. Science 335, 831-834 (2012). doi: 10.1126/science.1214081; pmid: 22344439
77. R. Schreiber et al., Hierarchical assembly of metal nanoparticles, quantum dots and organic dyes using DNA origami scaffolds. Nat. Nanotechnol. 9, 74-78 (2014). doi: 10.1038/nnano.2013.253; pmid: 24292513
78. C. Zhou, X. Duan, N. Liu, A plasmonic nanorod that walks on DNA origami. Nat. Commun. 6, 8102 (2015). doi: 10.1038/ncomms9102; pmid: 26303016
79. N. C. Gianneschi, M. R. Ghadiri, Design of molecular logic devices based on a programmable DNA-regulated semisynthetic enzyme. Angew. Chem. Int. Ed. 46, 3955-3958 (2007). doi: 10.1002/(ISSN)1521-3773; pmid: 17427900
80. M. Liu et al., A DNA tweezer-actuated enzyme nanoreactor. Nat. Commun. 4, 2127 (2013). doi: 10.1038/ncomms3127; pmid: 23820332
81. A. J. M. Wollman, C. Sanchez-Cano, H. M. J. Carstairs, R. A. Cross, A. J. Turberfield, Transport and self-organization across different length scales powered by motor proteins and programmed by DNA. Nat. Nanotechnol. 9, 44-47 (2014). doi: 10.1038/nnano.2013.230; pmid: 24213281
82. V. Noireaux, Y. T. Maeda, A. Libchaber, Development of an artificial cell, from self-organization to computation and selfreproduction. Proc. Natl. Acad. Sci. U.S.A. 108, 3473-3480 (2011). doi: 10.1073/pnas.1017075108; pmid: 21317359