Abstract
Biological systems illustrate how complex and dynamic physical and chemical interactions between many different components can produce organized structures across length scales, ranging from angstroms to hundreds of meters, and precise temporal control over diverse material dynamics. While mechanisms for pattern formation such as reaction-diffusion processes, message passing, or rule-based assembly have been studied extensively using mathematical models, it can be difficult to create synthetic materials that implement these mechanisms. Here, we describe how DNA nanotechnology techniques make it possible to systematically build systems capable of complex self-organization or pattern formation across scales. DNA-programmed short-range interactions can be used to build aperiodic crystals and assemblies with long-range order, form patterns using reaction-diffusion and chemical message passing, and create self-organizing or stimulus-responsive amorphous materials, including gels or cell-sized compartments. Exploiting principles from self-organization using DNA-based interactions makes it possible to build materials with complex long-range order and intelligent spatiotemporal responses to a variety of stimuli using relatively simple bottom-up methods.
Similar content being viewed by others
References
H. Valladas, J. Clottes, J.-M. Geneste, M.A. Garcia, M. Arnold, H. Cachier, N. Tisnérat-Laborde, Nature 413, 479 (2001).
E. Haeckel, Art Forms in Nature (Prestel, Munich, Germany, 2004).
D.A.W. Thompson, On Growth and Form (Cambridge University Press, Cambridge, UK, 2014).
E. Schrödinger, What Is Life? The Physical Aspect of the Living Cell (Cambridge University Press, Cambridge, UK, 1944).
J.H.E. Cartwright, A.L. Mackay, Philos. Trans. R. Soc. Lond. A 370, 2807 (2012).
A.M. Turing, Philos. Trans. R. Soc. Lond. B 237, 37 (1952).
J. Von Neumann, A.W. Burks, Theory of Self-Reproducing Automata (University of Illinois Press, Urbana, IL, 1966).
S. Wolfram, Nature 311, 419 (1984).
M.C. Cross, P.C. Hohenberg, Rev. Mod. Phys. 65, 851 (1993).
D. Soloveichik, G. Seelig, E. Winfree, Proc. Natl. Acad. Sci. U.S.A. 107, 5393 (2010).
E. Prince, A.J.C. Wilson, International Tables for Crystallography (Kluwer Academic Publishers, Dordrecht, 2004).
M. Baake, U. Grimm, Aperiodic Order, Volume 1: A Mathematical Invitation, Encyclopedia of Mathematics and Its Applications, Book 149 (Cambridge University Press, Cambridge, UK, 2013).
D. Levine, P.J. Steinhardt, Phys. Rev. Lett. 53, 2477 (1984).
G. Tikhomirov, P. Petersen, L. Qian, Nat. Nanotechnol. 12, 251 (2017).
E. Winfree, Algorithmic Self-Assembly of DNA (California Institute of Technology, Pasadena, CA, 1998).
P.W. Rothemund, N. Papadakis, E. Winfree, PLoS Biol. 2, e424 (2004).
R.D. Barish, R. Schulman, P.W. Rothemund, E. Winfree, Proc. Natl. Acad. Sci. U.S.A. 106, 6054 (2009).
M. Cook, P.W. Rothemund, E. Winfree, “Self-Assembled Circuit Patterns,” 9th Int. Workshop DNA-Based Comput., J. Chen. J. Reif, Eds. (Springer, Berlin, 2004), p. 91.
D. Soloveichik, E. Winfree, SIAM J. Comput. 36, 1544 (2007).
P.W. Rothemund, E. Winfree, “The Program-Size Complexity of Self-Assembled Squares,” Proc. 32nd Annu. ACM Symp. Theory Comput. (ACM, New York, 2000), p. 459.
M.F. Cohen, J. Shade, S. Hiller, O. Deussen, ACM Trans. Graph. 22, 287 (2003).
R. Schulman, B. Yurke, E. Winfree, Proc. Natl. Acad. Sci. U.S.A. 109, 6405 (2012).
E. Winfree, “Self-Healing Tile Sets,” in Nanotechnology: Science and Computation, Natural Computing Series (Springer, Berlin, Germany, 2006), p. 55.
J.E. Padilla, R. Sha, M. Kristiansen, J. Chen, N. Jonoska, N.C. Seeman, Angew. Chem. Int. Ed. 54, 5939 (2015).
A.J. Lotka, J. Am. Chem. Soc. 42, 1595 (1920).
A.T. Winfree, J. Chem. Educ. 61, 661 (1984).
P. Wang, G. Chatterjee, H. Tan, T.H. LaBean, A.J. Turberfield, C.E. Castro, G. Seelig, Y. Ke, MRS Bull. 42 (12), 889 (2017).
D.Y. Zhang, G. Seelig, Nat. Chem. 3, 103 (2011).
J. Kim, I. Khetarpal, S. Sen, R.M. Murray, Nucleic Acids Res. 42, 6078 (2014).
G. Seelig, D. Soloveichik, D.Y. Zhang, E. Winfree, Science 314, 1585 (2006).
L. Qian, E. Winfree, Science 332, 1196 (2011).
L. Qian, E. Winfree, J. Bruck, Nature 475, 368 (2011).
Y.J. Chen, N. Dalchau, N. Srinivas, A. Phillips, L. Cardelli, D. Soloveichik, G. Seelig, Nat. Nanotechnol. 8, 755 (2013).
J. Kim, E. Winfree, Mol. Syst. Biol. 7, 465 (2011).
K. Montagne, R. Plasson, Y. Sakai, T. Fujii, Y. Rondelez, Mol. Syst. Biol. 7, 466 (2011).
M. Schwarz-Schilling, J. Kim, C. Cuba, M. Weitz, E. Franco, F.C. Simmel, Methods Mol. Biol. 1342, 185 (2016).
T. Fuji, Y. Rondelez, ACS Nano 7, 27 (2013).
A. Padirac, T. Fuji, A. Estévez-Torres, Y. Rondelez, J. Am. Chem. Soc. 135, 14586 (2013).
A.S. Zadorin, Y. Rondelez, G. Gines, V. Dilhas, G. Urtel, A. Zambrano, J.-C. Galas, A. Estevez-Torres, Nat. Chem. 9, 990 (2017).
G. Gines, A.S. Zadorin, J.C. Galas, T. Fuji, A. Estevez-Torres, Y. Rondelez, Nat. Nanotechnol. 12, 351 (2017).
G. Grossi, A. Jaekel, E.S. Andersen, B. Saccà, MRS Bull. 42 (12), 920 (2017).
A.S. Zadorin, Y. Rondelez, J.C. Galas, A. Estevez-Torres, Phys. Rev. Lett. 114, 068301 (2015).
M. Weitz, J. Kim, K. Kapsner, E. Winfree, E. Franco, F.C. Simmel, Nat. Chem. 6, 295 (2014).
K. Hasatani, M. Leocmach, A.J. Genot, A. Estevez-Torres, T. Fujii, Y. Rondelez, Chem. Commun. 49, 8090 (2013).
M. Langecker, V. Arnaut, T.G. Martin, J. List, S. Renner, M. Mayer, H. Dietz, F.C. Simmel, Science 338, 932 (2012).
S. Krishnan, D. Ziegler, V. Arnaut, T.G. Martin, K. Kapsner, K. Henneberg, A.R. Bausch, H. Dietz, F.C. Simmel, Nat. Commun. 7, 12787 (2016).
C. Kurokawa, K. Fujiwara, M. Morita, I. Kawamata, Y. Kawagishi, A. Sakai, Y. Murayama, Shin-ichiro M. Nomura, S. Murata, M. Takinoue, “DNA Cytoskeleton for Stabilizing Artificial Cells,” Proc. Natl. Acad. Sci. U.S.A. 114, 7228 (2017).
Y. Sato, Y. Hiratsuka, I. Kawamata, S. Murata, Shin-ichiro M. Nomura, Sci. Rob. 2, eaal3735 (2017).
S.H. Um, J.B. Lee, N. Park, S.Y. Kwon, C.C. Umbach, D. Luo, Nat. Mater. 5, 797 (2006).
S.M. Douglas, J.J. Chou, W.M. Shih, Proc. Natl. Acad. Sci. U.S.A. 104, 6644 (2007).
M. Siavashpouri, C.H. Wachauf, M.J. Zakhary, F. Praetorius, H. Dietz, Z. Dogic, Nat. Mater. 16, 849 (2017).
A.M. Mohammed, P. Šulc, J. Zenk, R. Schulman, Nat. Nanotechnol. 12, 312 (2017).
J.S. Kahn, Y. Hu, I. Willner, Acc. Chem. Res. 50, 680 (2017).
T. Liedl, H. Dietz, B. Yurke, F. Simmel, Small 3, 1688 (2007).
A. Cangialosi, C. Yoon, J. Liu, Q. Huang, J. Guo, T.D. Nguyen, D.H. Gracias, R. Schulman, Science 357, 1126 (2017).
K. Gothelf, MRS Bull. 42 (12), 897 (2017).
Acknowledgements
F.C.S. acknowledges financial support for related work by the European Research Council (ERC Grant Agreement No. 694410). R.S. acknowledges financial support for related work from the National Science Foundation (NSF 1527377) and US Department of Energy (DE-SC0010426).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Simmel, F.C., Schulman, R. Self-organizing materials built with DNA. MRS Bulletin 42, 913–919 (2017). https://doi.org/10.1557/mrs.2017.271
Published:
Issue Date:
DOI: https://doi.org/10.1557/mrs.2017.271