Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-26T14:09:16.495Z Has data issue: false hasContentIssue false

RNA nanotechnology—The knots and folds of RNA nanoparticle engineering

Published online by Cambridge University Press:  08 December 2017

Yossi Weizmann
Affiliation:
Department of Chemistry, The University of Chicago, USA; [email protected]
Ebbe Sloth Andersen
Affiliation:
Interdisciplinary Nanoscience Center, Aarhus University, Denmark; [email protected]
Get access

Abstract

RNA nanotechnology seeks to exploit the structural and functional properties of the RNA molecule in order to rationally design RNA nanoparticles and devices for applications in biotechnology and medicine, among others. Compared to DNA, RNA can adopt a larger diversity of structural motifs that allows the construction of more complicated nanoparticles that can be self-assembled during synthesis by the RNA polymerase—a process called co-transcriptional folding. RNA nanostructures can be genetically encoded and co-transcriptionally folded in cells, which allows large-scale production of RNA nanoparticles for therapeutic use or the application as scaffolds in cells for manipulating cellular components for use in synthetic biology. In this article, we describe the origins of the RNA nanotechnology research field and how it has been inspired by DNA nanotechnology. Recent developments of co-transcriptionally folded RNA nanostructures and the construction of RNA knots are discussed in relation to design principles and challenges, and speculations about future directions of the field are provided.

Type
Research Article
Copyright
Copyright © Materials Research Society 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Tinoco, I., Bustamante, C., J. Mol. Biol. 293, 271 (1999).Google Scholar
Leontis, N.B., Westhof, E., RNA 7, 499 (2001).Google Scholar
Kebbekus, P., Draper, D.E., Hagerman, P., Biochemistry 34, 4354 (1995).CrossRefGoogle Scholar
Seeman, N.C., J. Theor. Biol. 99, 237 (1982).Google Scholar
Wang, H., Di Gate, R.J., Seeman, N.C., Proc. Natl. Acad. Sci. U.S.A. 93, 9477 (1996).CrossRefGoogle Scholar
Westhof, E., Masquida, B., Jaeger, L., Fold. Des. 1, R78 (1996).Google Scholar
Jaeger, L., Leontis, N.B., Angew. Chem. Int. Ed. Engl. 39, 2521 (2000).3.0.CO;2-P>CrossRefGoogle Scholar
Jaeger, L., Westhof, E., Leontis, N.B., Nucleic Acids Res. 29, 455 (2001).CrossRefGoogle Scholar
Skripkin, E., Paillart, J.C., Marquet, R., Ehresmann, B., Ehresmann, C., Proc. Natl. Acad. Sci. U.S.A. 91, 4945 (1994).Google Scholar
Guo, P., Zhang, C., Chen, C., Garver, K., Trottier, M., Mol. Cell. 2, 149 (1998).CrossRefGoogle Scholar
Shu, D., Moll, W.D., Deng, Z., Mao, C., Guo, P., Nano Lett. 4, 1717 (2004).CrossRefGoogle Scholar
Chworos, A., Severcan, I., Koyfman, A.Y., Weinkam, P., Oroudjev, E., Hansma, H.G., Jaeger, L., Science 306, 2068 (2004).Google Scholar
Nissen, P., Hansen, J., Ban, N., Moore, P.B., Steitz, T.A., Science 289, 920 (2000).Google Scholar
Wimberly, B.T., Brodersen, D.E., Clemons, W.M. Jr., Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., Hartsch, T., Ramakrishnan, V., Nature 407, 327 (2000).CrossRefGoogle Scholar
Boerneke, M.A., Dibrov, S.M., Hermann, T., Angew. Chem. Int. Ed. Engl. 55, 4097 (2016).CrossRefGoogle Scholar
Ohno, H., Kobayashi, T., Kabata, R., Endo, K., Iwasa, T., Yoshimura, S.H., Takeyasu, K., Inoue, T., Saito, H., Nat. Nanotechnol. 6, 116 (2011).CrossRefGoogle Scholar
Afonin, K.A., Viard, M., Koyfman, A.Y., Martins, A.N., Kasprzak, W.K., Panigaj, M., Desai, R., Santhanam, A., Grabow, W.W., Jaeger, L., Heldman, E., Reiser, J., Chiu, W., Freed, E.O., Shapiro, B.A., Nano Lett. 14, 5662 (2014).Google Scholar
Grabow, W.W., Jaeger, L., Acc. Chem. Res. 47, 1871 (2014).CrossRefGoogle Scholar
Jasinski, D., Haque, F., Binzel, D.W., Guo, P., ACS Nano 11, 1142 (2017).CrossRefGoogle Scholar
Myhrvold, C., Silver, P.A., Nat. Struct. Mol. Biol. 22, 8 (2015).CrossRefGoogle Scholar
Stewar, J.M., Franco, E., DNA RNA Nanotechnol. 2, 23 (2016).Google Scholar
Geary, C.W., Andersen, E.S., Proc. 20th Int. Conf. DNA Comput. Mol. Program. DNA 20, Murata, S., Kobayashi, S., Eds. (Springer International Publishing, London, 2014), pp. 119.Google Scholar
Yurke, B., Turberfield, A.J., Mills, A.P. Jr., Simmeld, F.C., Neumann, J.L., Nature 406, 605 (2000).Google Scholar
Afonin, K.A., Viard, M., Martins, A.N., Lockett, S.J., Maciag, A.E., Freed, E.O., Heldman, E., Jaeger, L., Blumenthal, R., Shapiro, B.A., Nat. Nanotechnol. 8, 296 (2013).CrossRefGoogle Scholar
Sulc, P., Ouldridge, T.E., Romano, F., Doye, J.P., Louis, A.A., Biophys. J. 108, 1238 (2015).CrossRefGoogle Scholar
Good, M.C., Zalatan, J.G., Lim, W.A., Science 332, 680 (2011).CrossRefGoogle Scholar
Delebecque, C.J., Lindner, A.B., Silver, P.A., Aldaye, F.A., Science 333, 470 (2011).CrossRefGoogle Scholar
Ko, S.H., Su, M., Zhang, C., Ribbe, A.E., Jiang, W., Mao, C., Nat. Chem. 2, 1050 (2010).Google Scholar
Stewart, J.M., Subramanian, H.K.K., Franco, E., Nucleic Acids Res. 45, 5449 (2017).CrossRefGoogle Scholar
Rothemund, P.W.K., Nature 440, 297 (2006).CrossRefGoogle Scholar
Endo, M., Yamamoto, S., Tatsumi, K., Emura, T., Hidaka, K., Sugiyama, H., Chem. Commun. (Camb.) 49, 2879 (2013).CrossRefGoogle Scholar
Wang, P., Ko, S.H., Tian, C., Hao, C., Mao, C., Chem. Commun. (Camb.) 49, 5462 (2013).CrossRefGoogle Scholar
Geary, C., Rothemund, P.W.K., Andersen, E.S., Science 345, 799 (2014).Google Scholar
Liu, D., Shao, Y., Chen, G., Tse-Dinh, Y.C., Piccirilli, J.A., Weizmann, Y., Nat. Commun. 8, 14936 (2017).CrossRefGoogle Scholar
Cruz, J.A., Westhof, E., Cell 136, 604 (2009).CrossRefGoogle Scholar
Woodson, S.A., Acc. Chem. Res. 44, 1312 (2011).Google Scholar
Afonin, K.A., Bindewald, E., Yaghoubian, A.J., Voss, N., Jacovetty, E., Shapiro, B.A., Jaeger, L., Nat. Nanotechnol. 5, 676 (2010).Google Scholar
Afonin, K.A., Desai, R., Viard, M., Kireeva, M.L., Bindewald, E., Case, C.L., Maciag, A.E., Kasprzak, W.K., Kim, T., Sappe, A., Stepler, M., Kewalramani, V.N., Kashlev, M., Blumenthal, R., Shapiro, B.A., Nucleic Acids Res. 42, 2085 (2014).CrossRefGoogle Scholar
Afonin, K.A., Kireeva, M., Grabow, W.W., Kashlev, M., Jaeger, L., Shapiro, B.A., Nano Lett. 12, 5192 (2012).Google Scholar
Geary, C., Chworos, A., Verzemnieks, E., Voss, N.R., Jaeger, L., Nano Lett. (2017), doi: 10.1021/acs.nanolett.7b03842.Google Scholar
Lee, J.B., Hong, J., Bonner, D.K., Poon, Z., Hammond, P.T., Nat. Mater. 11, 316 (2012).Google Scholar
Sparvath, S.L., Geary, C.W., Andersen, E.S., Methods Mol. Biol. 1500, 51 (2017).CrossRefGoogle Scholar
Du, S.M., Stollar, B.D., Seeman, N.C., J. Am. Chem. Soc. 117, 1194 (1995).CrossRefGoogle Scholar
Liu, D., Chen, G., Akhter, U., Cronin, T.M., Weizmann, Y., Nat. Chem. 8, 907 (2016).Google Scholar
Liu, D., Wang, M., Deng, Z., Walulu, R., Mao, C., J. Am. Chem. Soc. 126, 2324 (2004).Google Scholar
Avis, J.M., Conn, G.L., Walker, S.C., Methods Mol. Biol. 941, 83 (2012).CrossRefGoogle Scholar
Hartmann, R.K., Bindereif, A., Schon, A., Westhof, E., Handbook of RNA Biochemistry (Wiley-VCH, Weinheim, 2005).Google Scholar
Niu, J., Hili, R., Liu, D.R., Nat. Chem. 5, 282 (2013).Google Scholar