Methods 67 (2014) 103–104
Contents lists available at ScienceDirect
Methods journal homepage: www.elsevier.com/locate/ymeth
Guest Editor’s Introduction
Nucleic Acids Nanotechnology
It is unanimously recognized that the beginning of the Nanotechnology Era dates 29 December 1959, when the Nobel Laureate in Physics Richard Feynman gave his visionary talk at Caltech, entitled ‘‘There’s plenty of Room at the Bottom’’. In his revolutionary speech, he proposed for the first time the possibility to control matter at the nanoscale by direct manipulation of single atoms or molecules, thus laying the basis of a fundamental concept in nanotechnology, the merging of the top-down and bottom-up approach. Since then, many progresses have been made, such that nowadays self-organization of matter into supramolecular structures can be routinely achieved using a variety of chemical and bio-inspired strategies. Until now, probably one of the most robust and versatile approaches to reach the nanosized world from the molecular level takes advantage of the unique and programmable recognition properties of nucleic acids. Using a simple four bases code and applying predictable base pairing rules, one can in principle design and realize, in a relatively short time, two- and three-dimensional nucleic acids structures of almost any desired shape and pattern. The idea of using the DNA molecule as the fundamental building block of self-assembling nanomaterials was pioneered by Ned Seeman in the early ’80 [1] and since then structural DNA-nanotechnology has rapidly evolved, both in terms of design principles and applications [2]. A notable breakthrough in the field occurred in 2006, when Paul Rothemund first published his scaffolded DNA origami approach [3]. The self-assembly of a DNA origami basically relies on the folding of a long single stranded DNA (called ‘‘scaffold’’) into a desired shape by the help of hundreds of computer-designed synthetic oligonucleotides (normally referred to as ‘‘staples’’). The process normally occurs within a few hours and with astonishingly high yields. Most importantly, as the position of each nucleobase within the DNA nanostructure is exactly known, the method offers an extraordinary possibility: to organize matter in space with nanometer precision. This, together with the availability of user-friendly design tools and synthetic accessibility of oligonucleotides at relatively low costs, enabled the exponential growth of interest in this technology in the past few years [4]. Although initial efforts were mainly focused on solving design challenges, scientists rapidly succeeded in demonstrating the use of those structures for realistic applications. A comprehensive review on the use of DNA for the realization of functional devices is presented in this issue and covers different aspects of DNA nanotechnology, from the development of addressable molecular pegboards to optoelectronic hybrid materials and organic catalysts [5]. Of course, adding functionality to a nucleic acid structure normally requires its chemical modification with small molecules or proteins [6]. At this purpose, not only classical DNA-conjugation http://dx.doi.org/10.1016/j.ymeth.2014.04.018 1046-2023/Ó 2014 Elsevier Inc. All rights reserved.
strategies have been adopted and revisited [7], but other methods based on sequence-specificity recognition [8] and protein adaptors [9,10] have been also successfully applied. In addition, as shown by Sugimoto and coworkers in this issue [11], the molecular surrounding, e.g., cosolutes and crowding agents, may play a crucial role in controlling the stability and structure of nucleic acids. Typical examples of nucleic acids nanostructures, whose structural features are highly dependent on environmental conditions, are G-quadruplexes and G-wires [12]. One of the major advantages of being able to construct welldefined nanostructures in a predictable fashion is the possibility to address fundamental scientific questions at the single-molecule level [13]. The advancement of optical microscopy technologies and force-based instrumentations has made the study of single molecular events feasible, providing a way to ‘‘just look at the thing’’ as Feynman suggested. For example, single-molecule fluorescence microscopy has enabled the precise localization and counting of molecules in spatially distributed samples [14] or even allowed to reveal anomalous kinetic events occurring on a time scale normally not accessible by standard methods [15]. Besides being extremely valuable as biophysical tools, nucleic acids nanostructures have recently shown interesting properties in cells [16] and are currently explored as promising targeting and delivery systems [17,18]. Another interesting aspect of nucleic acids nanotechnology relates to the covalent modification of metal surfaces with DNA oligonucleotides, thus allowing to achieve control over the association of a distinct number of nanoparticles into well-ordered assemblies [19,20]. The strong electromagnetic field enhancement at the hot spot of two closely spaced metal surfaces has been then advantageously used to engineer nanoplasmonic materials with advanced optical properties [21]. DNA-guided assembly of metal nanoparticles is currently performed in two different ways. In a first approach, DNA-tagged nanoparticles are placed at predefined intermolecular distances through their arrangement onto a previously formed DNA template decorated with complementary single-stranded sequences [22]. In a second strategy, the DNA molecule is employed as a linker between desired nanoparticles, thus playing the double role of providing the structural framework while bringing the nanoparticles together. The extensive review from Wenlong and coauthors presented in this issue describes the basic principles, experimental procedures and applications currently in use for guiding the self-assembly of nanoparticles through DNA [23]. The ultimate goal of nucleic acids nanotechnology is the finest possible level of control over the spatial and temporal structure of matter. Thus, besides the use of DNA as a static framework to
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Guest Editor’s Introduction / Methods 67 (2014) 103–104
control the spatial arrangement of molecules, the programmability of nucleic acids structures can be conveniently employed to develop dynamic systems, whose interconversion between distinct species occurs in a predictable manner [24]. The conformational transition between one species and another is normally driven by the formation of thermodynamically more favored duplexes, through a mechanism of strand invasion and single strand displacement. This principle has been successfully employed to develop bioinspired DNA-nanomotors [25] and bioinformatic tools for emulating complex reaction circuits [26]. Recently, Kuzuya and coauthors also demonstrated that the structural reconfiguration of large DNA origami can be precisely controlled and directed to one of three different states [27], thus suggesting that more complex systems can be designed, in which the interplay between structural and dynamic properties of the DNA molecule offers enormous potential for future applications. Finally, it is worth noting that, although still at its infancy, fundamental research has been done on the rational design of nanoarchitectures made of RNA [28]. Despite its higher chemical lability as compared to its parent DNA molecule, RNA is more prone to fold into complex tertiary structures with catalytic and recognition properties, thus providing new possibilities for the design of complex and functional nanoarchitectures [29]. In conclusion, this issue nicely presents current state-of-the-art methodologies, design strategies and applications developed in the past decade by scientists worldwide in the continuously evolving field of nucleic acids nanotechnology. The exciting examples reported in this issue cover different aspects of the topic, ranging from the chemical approaches for functionalization of nanostructures, to formation of complex DNA or RNA architectures and their use as single-molecule or bioinformatic tools, cellular delivery systems, nanophotonic or biomimetic materials. Although many of Feynman’s predictions became a reality only decades later, one cannot but remain astonished by the enormous progresses made in the field and the rapid advancement of technologies and design strategies to approach the nanosized world with such a high control. In this sense, nucleic acids represent ideal candidates of those self-organizational systems initially envisaged in Feynman’s lecture, which can help us to manipulate nanosized matter and to understand the basic principles of self-assembly in natural and man-made systems, thus allowing us to emulate the genius famous words: ‘‘what I cannot create, I do not understand’’. I would like to deeply thank the authors of this issue of Methods for their high-quality and committed contributions, as well as the reviewers for their careful reviewing and precious suggestions. Finally, I am extremely thankful to the Editor, Prof. Jean-Louis Mergny, for inviting me to edit this collection, and the journal
manager, Mr. Don Prince, for his professional assistance in preparing the issue. References [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29]
N.C. Seeman, J. Theor. Biol. 99 (1982) 237. N.C. Seeman, Nature 421 (2003) 427. P.W. Rothemund, Nature 440 (2006) 297. B. Sacca, C.M. Niemeyer, Angew. Chem. Int. Ed. Engl. 51 (2012) 58. Y.C. Hung, D.M. Bauer, I. Ahmed, L. Fruk, Methods 67 (2014) 105–115. B. Sacca, C.M. Niemeyer, Chem. Soc. Rev. 40 (2011) 5910. Y. Dong, D. Liu, Z. Yang, Methods 67 (2014) 116–122. D.A. Rusling, K.R. Fox, Methods 67 (2014) 123–133. M.A. Koussa, M. Sotomayor, W.P. Wong, Methods 67 (2014) 134–141. T.A. Ngo, E. Nakata, M. Saimura, T. Kodaki, T. Morii, Methods 67 (2014) 142– 150. H. Tateishi-Karimta, N. Sugimoto, Methods 67 (2014) 151–158. J. Zhou, F. Rosu, S. Amrane, D.N. Korkut, V. Gabelica, J.L. Mergny, Methods 67 (2014) 159–168. N.G. Walter, C.Y. Huang, A.J. Manzo, M.A. Sobhy, Nat. Methods 5 (2008) 475. H. Zhang, P. Guo, Methods 67 (2014) 169–176. A. Johnson-Buck, N.G. Walter, Methods 67 (2014) 177–184. C. Bergamini, P. Angelini, K.J. Rhoden, A.M. Porcelli, R. Fato, G. Zuccheri, Methods 67 (2014) 185–192. A.H. Okholm, J.S. Nielsen, M. Vinther, R.S. Sorensen, D. Schaffert, J. Kjems, Methods 67 (2014) 193–197. X. Ouyang, J. Li, H. Liu, B. Zhao, J. Yan, D. He, C. Fan, J. Chao, Methods 67 (2014) 198–204. C.A. Mirkin, R.L. Letsinger, R.C. Mucic, J.J. Storhoff, Nature 382 (1996) 607. A.P. Alivisatos, K.P. Johnsson, X. Peng, T.E. Wilson, C.J. Loweth, M.P. Bruchez Jr., P.G. Schultz, Nature 382 (1996) 609. S.J. Tan, M.J. Campolongo, D. Luo, W. Cheng, Nat. Nanotechnol. 6 (2011) 268. Q. Liu, C. Song, Z.G. Wang, N. Li, B. Ding, Methods 67 (2014) 205–214. R.R. Mazid, K.J. Si, W. Cheng, Methods 67 (2014) 215–226. Y. Krishnan, F.C. Simmel, Angew. Chem. Int. Ed. Engl. 50 (2011) 3124. J. Cheng, S. Sreelatha, I.Y. Loh, M. Liu, Z. Wang, Methods 67 (2014) 227–233. A. Baccouche, K. Montagne, A. Padirac, T. Fujii, Y. Rondelez, Methods 67 (2014) 234–249. A. Kuzuya, R. Watanabe, M. Hashizume, M. Kaino, S. Minamida, K. Kameda, Y. Ohya, Methods 67 (2014) 250–255. A. Chworos, I. Severcan, A.Y. Koyfman, P. Weinkam, E. Oroudjev, H.G. Hansma, L. Jaeger, Science 306 (2004) 2068. K.A. Afonin, W. Kasprzak, E. Bindewald, P.S. Puppala, A.R. Diehl, K.T. Hall, T.J. Kim, M.T. Zimmermann, R.L. Jernigan, L. Jaeger, B.A. Shapiro, Methods 67 (2014) 256–265.
Barbara Saccà Center for Medical Biotechnology (ZMB), Universität Duisburg-Essen, Universitätstr. 2, 45117 Essen, Germany Center for Nanointegration Duisburg-Essen (CENIDE), Universität Duisburg-Essen, Universitätstr. 2, 45117 Essen, Germany E-mail address: [email protected]
Contents lists available at ScienceDirect
Methods journal homepage: www.elsevier.com/locate/ymeth
Guest Editor’s Introduction
Nucleic Acids Nanotechnology
It is unanimously recognized that the beginning of the Nanotechnology Era dates 29 December 1959, when the Nobel Laureate in Physics Richard Feynman gave his visionary talk at Caltech, entitled ‘‘There’s plenty of Room at the Bottom’’. In his revolutionary speech, he proposed for the first time the possibility to control matter at the nanoscale by direct manipulation of single atoms or molecules, thus laying the basis of a fundamental concept in nanotechnology, the merging of the top-down and bottom-up approach. Since then, many progresses have been made, such that nowadays self-organization of matter into supramolecular structures can be routinely achieved using a variety of chemical and bio-inspired strategies. Until now, probably one of the most robust and versatile approaches to reach the nanosized world from the molecular level takes advantage of the unique and programmable recognition properties of nucleic acids. Using a simple four bases code and applying predictable base pairing rules, one can in principle design and realize, in a relatively short time, two- and three-dimensional nucleic acids structures of almost any desired shape and pattern. The idea of using the DNA molecule as the fundamental building block of self-assembling nanomaterials was pioneered by Ned Seeman in the early ’80 [1] and since then structural DNA-nanotechnology has rapidly evolved, both in terms of design principles and applications [2]. A notable breakthrough in the field occurred in 2006, when Paul Rothemund first published his scaffolded DNA origami approach [3]. The self-assembly of a DNA origami basically relies on the folding of a long single stranded DNA (called ‘‘scaffold’’) into a desired shape by the help of hundreds of computer-designed synthetic oligonucleotides (normally referred to as ‘‘staples’’). The process normally occurs within a few hours and with astonishingly high yields. Most importantly, as the position of each nucleobase within the DNA nanostructure is exactly known, the method offers an extraordinary possibility: to organize matter in space with nanometer precision. This, together with the availability of user-friendly design tools and synthetic accessibility of oligonucleotides at relatively low costs, enabled the exponential growth of interest in this technology in the past few years [4]. Although initial efforts were mainly focused on solving design challenges, scientists rapidly succeeded in demonstrating the use of those structures for realistic applications. A comprehensive review on the use of DNA for the realization of functional devices is presented in this issue and covers different aspects of DNA nanotechnology, from the development of addressable molecular pegboards to optoelectronic hybrid materials and organic catalysts [5]. Of course, adding functionality to a nucleic acid structure normally requires its chemical modification with small molecules or proteins [6]. At this purpose, not only classical DNA-conjugation http://dx.doi.org/10.1016/j.ymeth.2014.04.018 1046-2023/Ó 2014 Elsevier Inc. All rights reserved.
strategies have been adopted and revisited [7], but other methods based on sequence-specificity recognition [8] and protein adaptors [9,10] have been also successfully applied. In addition, as shown by Sugimoto and coworkers in this issue [11], the molecular surrounding, e.g., cosolutes and crowding agents, may play a crucial role in controlling the stability and structure of nucleic acids. Typical examples of nucleic acids nanostructures, whose structural features are highly dependent on environmental conditions, are G-quadruplexes and G-wires [12]. One of the major advantages of being able to construct welldefined nanostructures in a predictable fashion is the possibility to address fundamental scientific questions at the single-molecule level [13]. The advancement of optical microscopy technologies and force-based instrumentations has made the study of single molecular events feasible, providing a way to ‘‘just look at the thing’’ as Feynman suggested. For example, single-molecule fluorescence microscopy has enabled the precise localization and counting of molecules in spatially distributed samples [14] or even allowed to reveal anomalous kinetic events occurring on a time scale normally not accessible by standard methods [15]. Besides being extremely valuable as biophysical tools, nucleic acids nanostructures have recently shown interesting properties in cells [16] and are currently explored as promising targeting and delivery systems [17,18]. Another interesting aspect of nucleic acids nanotechnology relates to the covalent modification of metal surfaces with DNA oligonucleotides, thus allowing to achieve control over the association of a distinct number of nanoparticles into well-ordered assemblies [19,20]. The strong electromagnetic field enhancement at the hot spot of two closely spaced metal surfaces has been then advantageously used to engineer nanoplasmonic materials with advanced optical properties [21]. DNA-guided assembly of metal nanoparticles is currently performed in two different ways. In a first approach, DNA-tagged nanoparticles are placed at predefined intermolecular distances through their arrangement onto a previously formed DNA template decorated with complementary single-stranded sequences [22]. In a second strategy, the DNA molecule is employed as a linker between desired nanoparticles, thus playing the double role of providing the structural framework while bringing the nanoparticles together. The extensive review from Wenlong and coauthors presented in this issue describes the basic principles, experimental procedures and applications currently in use for guiding the self-assembly of nanoparticles through DNA [23]. The ultimate goal of nucleic acids nanotechnology is the finest possible level of control over the spatial and temporal structure of matter. Thus, besides the use of DNA as a static framework to
104
Guest Editor’s Introduction / Methods 67 (2014) 103–104
control the spatial arrangement of molecules, the programmability of nucleic acids structures can be conveniently employed to develop dynamic systems, whose interconversion between distinct species occurs in a predictable manner [24]. The conformational transition between one species and another is normally driven by the formation of thermodynamically more favored duplexes, through a mechanism of strand invasion and single strand displacement. This principle has been successfully employed to develop bioinspired DNA-nanomotors [25] and bioinformatic tools for emulating complex reaction circuits [26]. Recently, Kuzuya and coauthors also demonstrated that the structural reconfiguration of large DNA origami can be precisely controlled and directed to one of three different states [27], thus suggesting that more complex systems can be designed, in which the interplay between structural and dynamic properties of the DNA molecule offers enormous potential for future applications. Finally, it is worth noting that, although still at its infancy, fundamental research has been done on the rational design of nanoarchitectures made of RNA [28]. Despite its higher chemical lability as compared to its parent DNA molecule, RNA is more prone to fold into complex tertiary structures with catalytic and recognition properties, thus providing new possibilities for the design of complex and functional nanoarchitectures [29]. In conclusion, this issue nicely presents current state-of-the-art methodologies, design strategies and applications developed in the past decade by scientists worldwide in the continuously evolving field of nucleic acids nanotechnology. The exciting examples reported in this issue cover different aspects of the topic, ranging from the chemical approaches for functionalization of nanostructures, to formation of complex DNA or RNA architectures and their use as single-molecule or bioinformatic tools, cellular delivery systems, nanophotonic or biomimetic materials. Although many of Feynman’s predictions became a reality only decades later, one cannot but remain astonished by the enormous progresses made in the field and the rapid advancement of technologies and design strategies to approach the nanosized world with such a high control. In this sense, nucleic acids represent ideal candidates of those self-organizational systems initially envisaged in Feynman’s lecture, which can help us to manipulate nanosized matter and to understand the basic principles of self-assembly in natural and man-made systems, thus allowing us to emulate the genius famous words: ‘‘what I cannot create, I do not understand’’. I would like to deeply thank the authors of this issue of Methods for their high-quality and committed contributions, as well as the reviewers for their careful reviewing and precious suggestions. Finally, I am extremely thankful to the Editor, Prof. Jean-Louis Mergny, for inviting me to edit this collection, and the journal
manager, Mr. Don Prince, for his professional assistance in preparing the issue. References [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29]
N.C. Seeman, J. Theor. Biol. 99 (1982) 237. N.C. Seeman, Nature 421 (2003) 427. P.W. Rothemund, Nature 440 (2006) 297. B. Sacca, C.M. Niemeyer, Angew. Chem. Int. Ed. Engl. 51 (2012) 58. Y.C. Hung, D.M. Bauer, I. Ahmed, L. Fruk, Methods 67 (2014) 105–115. B. Sacca, C.M. Niemeyer, Chem. Soc. Rev. 40 (2011) 5910. Y. Dong, D. Liu, Z. Yang, Methods 67 (2014) 116–122. D.A. Rusling, K.R. Fox, Methods 67 (2014) 123–133. M.A. Koussa, M. Sotomayor, W.P. Wong, Methods 67 (2014) 134–141. T.A. Ngo, E. Nakata, M. Saimura, T. Kodaki, T. Morii, Methods 67 (2014) 142– 150. H. Tateishi-Karimta, N. Sugimoto, Methods 67 (2014) 151–158. J. Zhou, F. Rosu, S. Amrane, D.N. Korkut, V. Gabelica, J.L. Mergny, Methods 67 (2014) 159–168. N.G. Walter, C.Y. Huang, A.J. Manzo, M.A. Sobhy, Nat. Methods 5 (2008) 475. H. Zhang, P. Guo, Methods 67 (2014) 169–176. A. Johnson-Buck, N.G. Walter, Methods 67 (2014) 177–184. C. Bergamini, P. Angelini, K.J. Rhoden, A.M. Porcelli, R. Fato, G. Zuccheri, Methods 67 (2014) 185–192. A.H. Okholm, J.S. Nielsen, M. Vinther, R.S. Sorensen, D. Schaffert, J. Kjems, Methods 67 (2014) 193–197. X. Ouyang, J. Li, H. Liu, B. Zhao, J. Yan, D. He, C. Fan, J. Chao, Methods 67 (2014) 198–204. C.A. Mirkin, R.L. Letsinger, R.C. Mucic, J.J. Storhoff, Nature 382 (1996) 607. A.P. Alivisatos, K.P. Johnsson, X. Peng, T.E. Wilson, C.J. Loweth, M.P. Bruchez Jr., P.G. Schultz, Nature 382 (1996) 609. S.J. Tan, M.J. Campolongo, D. Luo, W. Cheng, Nat. Nanotechnol. 6 (2011) 268. Q. Liu, C. Song, Z.G. Wang, N. Li, B. Ding, Methods 67 (2014) 205–214. R.R. Mazid, K.J. Si, W. Cheng, Methods 67 (2014) 215–226. Y. Krishnan, F.C. Simmel, Angew. Chem. Int. Ed. Engl. 50 (2011) 3124. J. Cheng, S. Sreelatha, I.Y. Loh, M. Liu, Z. Wang, Methods 67 (2014) 227–233. A. Baccouche, K. Montagne, A. Padirac, T. Fujii, Y. Rondelez, Methods 67 (2014) 234–249. A. Kuzuya, R. Watanabe, M. Hashizume, M. Kaino, S. Minamida, K. Kameda, Y. Ohya, Methods 67 (2014) 250–255. A. Chworos, I. Severcan, A.Y. Koyfman, P. Weinkam, E. Oroudjev, H.G. Hansma, L. Jaeger, Science 306 (2004) 2068. K.A. Afonin, W. Kasprzak, E. Bindewald, P.S. Puppala, A.R. Diehl, K.T. Hall, T.J. Kim, M.T. Zimmermann, R.L. Jernigan, L. Jaeger, B.A. Shapiro, Methods 67 (2014) 256–265.
Barbara Saccà Center for Medical Biotechnology (ZMB), Universität Duisburg-Essen, Universitätstr. 2, 45117 Essen, Germany Center for Nanointegration Duisburg-Essen (CENIDE), Universität Duisburg-Essen, Universitätstr. 2, 45117 Essen, Germany E-mail address: [email protected]
