Self-Assembly of DNA Arrays into Multilayer Stacks
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1 Article Subscriber access provided by HOUSTON ACADEMY OF MEDICINE Self-Assembly of DNA Arrays into Multilayer Stacks Alexey Y. Koyfman, Sergei N. Magonov, and Norbert O. Reich Langmuir, 2009, 25 (2), DOI: /la801306j Publication Date (Web): 11 July 2008 Downloaded from on January 15, 2009 More About This Article Additional resources and features associated with this article are available within the HTML version: Supporting Information Access to high resolution figures Links to articles and content related to this article Copyright permission to reproduce figures and/or text from this article Langmuir is published by the American Chemical Society Sixteenth Street N.W., Washington, DC 20036
2 Langmuir 2009, 25, Self-Assembly of DNA Arrays into Multilayer Stacks Alexey Y. Koyfman,, Sergei N. Magonov, and Norbert O. Reich*,, Department of Chemistry and Biochemistry, Biomolecular Science and Engineering Program, UniVersity of California - Santa Barbara, Santa Barbara, California , and Veeco Instruments, 112 Robin Hill Road, Goleta, California ReceiVed April 26, ReVised Manuscript ReceiVed May 21, 2008 We describe the self-assembly of multilayer hexagonal DNA arrays through highly regular interlayer packing. Slow cooling of a mixture of three single-stranded DNA sequences with various Mg 2+ concentrations leads to the selfassembly of diverse multilayer architectures. The self-assembled aggregates were deposited onto mica surfaces and examined with atomic force microscopy. The size of the two-dimensional arrays and subsequent stacking to form multilayer structures are highly dependent on Mg 2+ concentration. DNA bilayers and multilayers of defined shape are favored in 2-5 mmmg 2+ with an average lateral size of 700 nm. Arrays are much larger (up to 20 µm across) in mm Mg 2+, although multiple layers still make up 20-60% of the observed structures. Domains within single layer architectures were identified using Moiré pattern analysis. Distinct structural phases within the multilayer assemblies include two layers translated by 17.5 nm and interlayer rotations of 20 and 30. Three layer assemblies have cubic close packing and taller multilayer architectures of 2D DNA sheets were also identified. Introduction DNA is condensed in living organisms up to one million fold and is subsequently unwound during cell division and RNA transcription. Due to the highly negatively charged nature of the DNA backbone, this compaction is largely achieved through the use of positively charged histones and small molecules such as spermine. DNA and RNA have recently been used as materials to study the process of controlled self-assembly. A critical aspect of such efforts is the inclusion of rigid structural motifs such as double 1 and triple 2 crossovers in DNA, or 90 motifs 3 in RNA. Another essential feature is the incorporation of complementary overhangs to direct the desired assembly. 3 8 While the designed features form on the nanoscale, they have been largely limited to sizes below a micron. 3 5 By introducing symmetry into all complementary overhangs, much larger assemblies can be generated Such large two-dimensional arrays require building blocks that are sufficiently flexible to constrain all components * reich@chem.ucsb.edu. Department of Chemistry and Biochemistry, University of California - Santa Barbara. Biomolecular Science and Engineering Program, University of California - Santa Barbara. Veeco Instruments. Current affiliation - Agilent Technologies. (1) Li, X.; Yang, X.; Qi, J.; Seeman, N. C. J. Am. Chem. Soc. 1996, 118, (2) LaBean, T. H.; Yan, H.; Kopatsch, J.; Liu, F.; Winfree, E.; Reif, J. H.; Seeman, N. C. J. Am. Chem. Soc. 2000, 122, (3) Chworos, A.; Severcan, I.; Koyfman, A. Y.; Weinkam, P.; Oroudjev, E.; Hansma, H. G.; Jaeger, L. Science 2004, 306, (4) Ding, B.; Sha, R.; Seeman, N. C. J. Am. Chem. Soc. 2004, 126, (5) Chelyapov, N.; Brun, Y.; Gopalkrishnan, M.; Reishus, D.; Shaw, B.; Adleman, L. J. Am. Chem. Soc. 2004, 126, (6) Yan, H.; Park, S. H.; Finkelstein, G.; Reif, J. H.; LaBean, T. H. Science 2003, 301, (7) Park, S. H.; Pistol, C.; Ahn, S. J.; Reif, J. H.; Lebeck, A. R.; Dwyer, C.; LaBean, T. H. Angew. Chem., Int. Ed. 2006, 45, (8) Seeman, N. C. Nature 2003, 421, (9) He, Y.; Chen, Y.; Liu, H.; Ribbe, A. E.; Mao, C. J. Am. Chem. Soc. 2005, 127, (10) He, Y.; Tian, Y.; Chen, Y.; Deng, Z.; Ribbe, A. E.; Mao, C. Angew. Chem., Int. Ed. 2005, 44, (11) He, Y.; Tian, Y.; Ribbe, A. E.; Mao, C. J. Am. Chem. Soc. 2006, 128, (12) He, Y.; Mao, C. Chem. Commun. 2006, (13) He, Y.; Tian, Y.; Chen, Y.; Ribbe, A. E.; Mao, C. Chem. Commun. 2007, in one plane. A new three-point-star motif was recently determined to have the correct balance of flexibility and stress to generate rigid and well defined structures. 9,12 Systematic increases of the number of branches in the monomer unit (3 f 4 f 6) generated arrays which were still restricted to a plane One- and two-dimensional nucleic acid architectures have been used as scaffolds for positioning proteins and inorganic materials 6 8,14 17 and for macromolecule detection. 18,19 The assembly of such structures in three dimensions and their temporal control remain significant challenges. Three-dimensional architectures can increase the density of guest molecule packing for structure determination, high-density information storage, localization of functional proteins next to each other for catalysis, and electronic and optical applications. Nanometer-scale three-dimensional objects of defined size have been constructed from DNA and used to position a protein within the architecture. 25 Continuous three-dimensional DNA lattices with solvent channels that can accommodate small proteins have been crystallized and function as molecular sieves. 26,27 Enzyme-catalyzed DNA hydrogels assembled from short strands of cdna were used for controlled (14) He, Y.; Tian, Y.; Ribbe, A. E.; Mao, C. J. Am. Chem. Soc. 2006, 128, (15) Koyfman, A. Y.; Braun, G.; Magonov, S.; Chworos, A.; Reich, N. O.; Jaeger, L. J. Am. Chem. Soc. 2005, 127, (16) Le, J. D.; Pinto, Y.; Seeman, N. C.; Musier-Forsyth, K.; Taton, T. A.; Kiehl, R. A. Nano Lett. 2004, 4, (17) Zheng, J.; Constantinou, P. E.; Micheel, C.; Alivisatos, A. P.; Kiehl, R. A.; Seeman, N. C. Nano Lett. 2006, 6, (18) Lin, C.; Katilius, E.; Liu, Y.; Zhang, J.; Yan, H. Angew. Chem., Int. Ed. 2006, 45, (19) Lin, C.; Liu, Y.; Yan, H. Nano Lett. 2007, 7, (20) Shih, W. M.; Quispe, J. D.; Joyce, G. F. Nature 2004, 427, (21) He, Y.; Ye, T.; Su, M.; Zhang, C.; Ribbe, A. E.; Jiang, W.; Mao, C. D. Nature 2008, 452, (22) Rothemund, P. W. K. Nature 2006, 440, (23) Goodman, R. P.; Schaap, I. A. T.; Tardin, C. F.; Erben, C. M.; Berry, R. M.; Schmidt, C. F.; Turberfield, A. J. Science 2005, 310, (24) Erben, C. M.; Goodman, R. P.; Turberfield, A. J. J. Am. Chem. Soc. 2007, 129, (25) Erben, C. M.; Goodman, R. P.; Turberfield, A. J. Angew. Chem., Int. Ed. 2006, 45, (26) Paukstelis, P. J.; Nowakowski, J.; Birktoft, J. J.; Seeman, N. C. Chem. Biol. 2004, 11, (27) Paukstelis, P. J. J. Am. Chem. Soc. 2006, 128, /la801306j CCC: $ American Chemical Society Published on Web 07/11/2008
3 1092 Langmuir, Vol. 25, No. 2, 2009 Koyfman et al. Figure 1. Nucleic acid array formation at various Mg 2+ ion concentrations (A) Representative arrays formed at high (10 and 15 mm) Mg 2+ concentrations. (B-D) Representative arrays formed at low (2 and 5 mm) Mg 2+ concentrations. (E) Graphical representation of domain sizes formed at various Mg 2+ concentrations. Domain size (µm) was determined as the square root of the area occupied by the domain. drug release. 28 DNA has been covalently coupled to organic materials to produce novel optical, electronic, and mechanical properties. 29,30 An attractive goal with these three-dimensional architectures is the construction of objects on the micrometer to millimeter scale. Our interest lies in the directed incorporation of inorganic materials within nucleic acid architectures for fundamental studies as well as various applications. We previously incorporated 5 nm positively charged gold nanoparticles within RNA scaffolds. 15 Mao and colleagues 9 recently showed that DNA provides an excellent scaffold to increase the regularity and extent of nanoparticle assembly on a nucleic acid array. In our efforts to use this new assembly approach, 9 we identified novel architectures which depended on the assembly conditions. Herein we report on the formation of highly regular interarray multilayer packing from hexagonal two-dimensional arrays. The extent of array and multilayer formation is highly dependent on Mg 2+ concentration. Results and Discussion The dependence of nucleic acid array formation from three single-stranded DNA sequences on the concentration of Mg 2+ ions is illustrated in Figure 1. Slow cooling of a mixture of three single-stranded DNA sequences (see Supporting Information) in the presence of Mg 2+ results in formation of 3-point star motifs 9 (monomer units of a hexagonal DNA array shown in Figure 3A, bottom right) that self-assemble into 2D hexagonal DNA arrays which furthermore form diverse multilayer architectures. Prior work with the same DNA strands at 10 mm Mg 2+ using fluorescent microscopy showed millimeter long arrays. 9,10 This same work demonstrated that arrays observed by atomic force microscopy were generally smaller than arrays observed by fluorescent microscopy since the interaction with a mica surface is potentially destructive to extensive nucleic acid arrays Here we show that at high Mg 2+ concentrations of 10 and 15 mm (Figure 1A) DNA strands form micron-sized arrays, 40 ( 20% (28) Um, S. H.; Lee, J. B.; Park, N.; Kwon, S. Y.; Umbach, C. C.; Luo, D. Nat. Mater. 2006, 5, (29) Chenoweth, D. M.; Viger, A.; Dervan, P. B. J. Am. Chem. Soc. 2007, 129, (30) Janssen, P. G. A.; Vandenbergh, J.; van Dongen, J. L. J.; Meijer, E. W.; Schenning, A. P. H. J. J. Am. Chem. Soc. 2007, 129, Figure 2. Moiré pattern of a single layer array. (A) 5 5 µm 2 digital zoom in of a µm 2 scan depicting Moiré patterns. Fast Fourier transform of image (A) where peaks are outlined by blue, red, and green boxes (inset). (B) µm 2 scan of the area outlined within the white square in (A). Three domains within this scan are indicated by positioning parallel blue, red, and green lines over them. Inset: Color coded FFT back transform of the peaks outlined in the inset in (A). Note that the parallel lines, FFT peaks in inset (A), and domains in inset (B) are the same colors.
4 Self-Assembly of DNA Arrays into Multilayer Stacks Langmuir, Vol. 25, No. 2, Figure 3. Three predominant orientations of a bilayer assembly. (A) (Top) AFM image showing single and double layer of a DNA hexagonal array. Top layer of the double layer is translated 17.5 nm with respect to the bottom layer where the overlay of two 3-point star motifs is higher. The distance between the two adjacent overlays is 30 nm. (Bottom) A diagram representation of a 3-point star motif, two layer assembly, and a model depicting an overlay of two 3-point star motifs. One motif is rotated 180 with respect to another. (B) (Top) AFM image showing two layers of a DNA hexagonal array rotated 30 with respect to one another. (Inset) Fourier transform of the AFM image indicating that the rotation between the two layers is 30. (Bottom) A diagram representation of a two layer assembly rotated 30 with respect to one another. Blue, red, and black dots on the AFM image and the model correspond to provide the same pattern. (C) (Top) AFM image showing two layers of a DNA hexagonal array rotated 20 with respect to one another. (Inset) Fourier transform of the AFM image indicating that the rotation between the two layers is 20. (Bottom) A diagram representation of a two layer assembly rotated 20 with respect to one another. Blue and red dots on the AFM image and the model correspond to provide the same pattern. of the total area of which occurs in multiple layers. Moiré patterns discussed in Figure 2 are evident in Figure 1A at the scan size above 10 µm. Different nucleic acid architectures were observed at low (2 and 5 mm) Mg 2+ concentrations (Figure 1B-D). Under low Mg 2+ concentrations, DNA strands form predominantly submicron bilayer arrays of a defined geometrical shape resembling rhombuses, triangles, or rectangles with sharply defined edges. Arrays formed at low Mg 2+ concentrations are mostly composed of two DNA layers positioned on top of each other at well-defined orientations. Occasionally, pyramidal architectures composed of multiple layers are observed at low Mg 2+ concentrations (Figures 1B and 5). The array size at low Mg 2+ concentrations is not altered if the Mg 2+ is subsequently increased to 15 mm, suggesting that the arrays are not selectively bound to the mica surface at different Mg 2+ concentrations. It is interesting to note that the density of array occurrence on the mica surface is highly Mg 2+ dependent. At 2 mm Mg 2+ submicron bilayers are separated tens of microns away from one another (Supporting Information Figure S1A-C). The array density is increased when the Mg 2+ concentration is increased to 15 mm indicating a better binding of negatively charged DNA arrays and the mica surface through Mg 2+ ions (Supporting Information Figure S1D-F). To further quantify the size of the array surface, we determined the area of the array using Nanoscope software. Since most of the arrays have similar lateral dimensions, we assumed that arrays form perfect squares and estimated an array s size by taking the square root of the area. Figure 1E shows the distribution of array sizes depending on the concentration of Mg 2+ ions. Representative arrays (45) were imaged at each concentration of 2, 5, 10 and 15 mm Mg 2+. Under low Mg 2+ concentrations, DNA strands form 88% submicron arrays where sizes range from 230 nm to 6.6 µm. Average sizes are 730 nm at 2 mm and 680 nm at 5 mm Mg 2+. At high Mg 2+ concentrations, DNA strands form arrays that range from 390 nm to 20 µm and are 4.7 ( 4.2 µm at10 mm Mg 2+ and 7.0 ( 4.6 µm at15mmmg 2+. At high Mg 2+ concentrations, 63% of the arrays are above 3 µm in size. Since arrays at high Mg 2+ concentration are evenly distributed in size, the larger arrays most likely are formed from a number of smaller domains as Moiré patterns confirm (Figure 2) as well as from addition of monomer units. DNA domains are well-ordered isotropic assemblies of monomer subunits with minimal defects. The assembly melting temperature (T m ) of DNA is known to increase with increases in Mg 2+ concentration. 31,32 Since the extent of the DNA arrays is in part dependent on the melting temperature, it is likely that lower Mg 2+ concentrations should result in smaller assemblies. The array edges formed at high Mg 2+ concentrations are poorly defined, implying a constant addition of monomer units by addition polymerization 33 (polydispersity index at high Mg 2+ concentrations is close to 1) or other already formed domains, consistent with the Moiré patterns (Figure 2). At high Mg 2+, lateral extension of DNA arrays occurs along with the multilayer formation occupying about 40 ( 20% of the total array area. Multilayer formation could happen by several mechanisms. For example, the extended arrays could bend and collapse on the mica surface. Smaller arrays could form closed tubes and form bilayers once collapsed on the mica surface. Alternatively, domains could stack on top of each other during the cooling process with Mg 2+ ions counteracting negative phosphates. For example, at lower concentrations of Mg 2+ ions, the ions which may be limiting are more likely to interact between phosphates of adjacent domains to neutralize the charge. In contrast, at higher Mg 2+ concentrations, the charges are counteracted within the same DNA strand, therefore helping to form extended single arrays with millimeter long structures. It is interesting to note that the DNA arrays are rather stable. These arrays were imaged on mica surfaces in air before degradation becomes visible for up to a month (Supporting Information Figure S2), unlike RNA arrays where damage becomes apparent after one week. 15 No damage to the DNA (31) Schildkraut, C.; Lifson, S. Biopolymers 1965, 3, (32) Tan, Z.; Chen, S. Biophys. J. 2006, 90, (33) Rubinstein, M.; Colby, R. H. Polymer Physics; Oxford University Press: New York, 2003.
5 1094 Langmuir, Vol. 25, No. 2, 2009 Koyfman et al. Figure 4. Modeling and AFM of two- and three-layer assemblies. (A) Folding of a representative DNA sheet along the blue line (top) leads to dense packing in which three-point-star motifs are positioned on top of each other, rotated 180 and predicted to be separated by 30 nm (shown in red). Bottom shows a folded DNA sheet positioned on another DNA sheet to generate two- and three-layer assemblies. The distance between two three-point-star motifs is predicted to decrease to 15 nm. (B) AFM and cross sections of two- and three-layer assemblies. For the two-layer assembly, the spacing between adjacent three-point-star motifs varies between 30 and 32 nm and the heights are 1.2 and 2.3 nm for single and double layers respectively (blue line). For the three-layer assembly, spacing between two three-point-star motifs varies between 14 and 19 nm and the heights are 1.3 and 2.4 nm for the single and three-layer assemblies respectively (red line). Green triangles enclose six and ten three-point-star motifs for double and triple layers respectively; the corresponding models are discussed in the text. DNA is cubic close-packed within the triple-layer assemblies. (C) Distributions of distances separating adjacent locations of the two three-point-star motifs positioned on one another for the double layer (blue, n ) 276) and triple layer (red, n ) 291). Distance separating adjacent locations of the two three-point-star motifs positioned on one another is 16.2 nm for the triple layer and 32.2 nm for the double layer. (34) Hexemer, A.; Stein, G. E.; Kramer, E. J.; Magonov, S. Macromolecules 2005, 38, arrays is observed when an aliquot of the solution containing DNA arrays is placed on the mica surface and dried after being stored at 4 C for multiple months. Figure 2 shows a Moiré pattern of a single layer array where we observe distinct orientations of DNA domains within the single layer of a DNA sheet. Moiré pattern analysis provides a robust approach to identify long-range order as well as the size and orientation of domains. Moiré patterns are observed at the scan size of µm due to the interference between the AFM scan lines which act as a reference grating, and closely packed hexagonal array architectures which form the sample lattice grating 34 (Figure 1A). To obtain Moiré patterns, the AFM grating pitch P G should be similar to the integer multiple of the sample lattice pitch P L, P G np L. The 15 µm by15µm image was scanned at a sampling rate of 512 pixels. Therefore, the grating pitch was P G ) 15 µm/512 pixels ) 29.3 nm/pixel, very close to the 30.3 nm sample lattice pitch P L. Analysis of similar patterns was used to detect structural defects formed in the microphaseseparation pattern common for thin films of block copolymers. 34 Figure 2A is a 5 5 µm 2 digital magnification of a µm 2 scan of Moiré patterns. The inset in the bottom right corner is a fast Fourier transform (FFT) of the image in Figure 2A. The colored rectangles in Figure 2A were iteratively optimized (size and position) to maximize both the individual and overall coverage of oriented domains shown in Figure 2B. Three distinctive FFT peaks are outlined by blue, red, and green boxes and correspond to distinct orientations of DNA domains within the single layer of a DNA sheet. The inset at the top left corner of Figure 2B shows a color-coded inverse FFT of only the FFT peaks in which the peak outlines and domains have the same color. Figure 2B shows a µm 2 scan of the area outlined within the white square in Figure 2A. Three domains within this scan are indicated by positioning parallel blue, red, and green lines over them which correspond to the colors of the FFT peak outlines and domains in the inverse FFT. Figure 3 shows three predominant orientations of a two-layer assembly. Figure 3A (top) shows an AFM image of a single layer of a DNA hexagonal array in the bottom right corner. A
6 Self-Assembly of DNA Arrays into Multilayer Stacks Langmuir, Vol. 25, No. 2, Figure 5. AFM and cross section of two-layer and multilayer assemblies. Multilayer assemblies form at low Mg 2+ concentration. The cross section (black line) was shown to represent the height of a two-layer assembly (2.5 nm) rotated 30 with respect to one another and a taller multilayer assembly that is 8.8 nm in height. double layer is formed when a DNA sheet is folded on itself along the edge in the top left corner of the image. This is a face centered cubic orientation, 5 since a 3-point-star motif is located within the hexagon formed by other six 3-point-star motifs. This orientation results from the translation or 180 rotation of the top layer (blue) with respect to the bottom layer (green) (Figure 3A(bottom)). A model of the overlay of two 3-point-star motifs rotated 180 with respect to another is shown in Figure 3A (bottom). A zoom in of the overlay of two 3-point-star motifs rotated 180 with respect to another is shown in Figure 3A (bottom). The distance between the two opposite edges of a hexagon formed from six 3-point-star motifs is predicted to be 30.3 nm calculated by assuming 0.33 nm/base pair pitch and 2 nm diameter in a DNA helix. 9 Assuming a 30.3 nm distance between the two opposite edges of a hexagon, the top of the double layer is translated 17.5 nm (15.15 nm/cos 30) with respect to the bottom layer. The overlay of two 3-point-star motifs generates a double layer which is higher than a single layer. The distance between the two adjacent overlays of 3-point-star motifs of similar height (indicated in red on the model in Figure 3A bottom) overlays is predicted to be 30.3 nm. The actual distance between adjacent 3-point-star motifs is consistent with the model and was 32.1 ( 2.2 nm (N ) 130). Figure 3B (top) shows an AFM image of two layers of a DNA hexagonal array rotated 30 with respect to one another. The inset is a Fourier transform of the AFM image indicating that the rotation between the two layers is 30, since 12 dots are equidistant from one another. The bottom of Figure 3B shows a diagram of a two-layer assembly where two sheets are rotated 30 with respect to one another. Blue, red, and black dots on the AFM image and the model correspond and show the same pattern. The two sets of 12 red dots are enclosed within the two sets of 5 dots. The first set of 5 dots is colored blue and is indicated for the set of 12 red dots on the right. Only two members of the second set of 5 dots are indicated in black. Figure 3C (top) shows an AFM image of two layers of a DNA hexagonal array rotated 20 with respect to one another. The inset is a Fourier transform of the AFM image indicating that the rotation between the two layers is 20, since the two sets of six dots are separated by 20. The bottom diagram represents a two-layer assembly where the two layers are rotated 20 with respect to one another. Blue (12) and red (5) dots in the AFM image and the model reveal the same patterns. Figure 4A represents a model of two- and three-layer assemblies. The top part of Figure 4A depicts a model of a DNA sheet that is folded on itself along the blue line. Upon folding, DNA becomes more densely packed, where three-point-star motifs are positioned within hexagons and on top of other threepoint-star motifs and are separated by 30.3 nm. The overlay of two three-point-star motifs is indicated in red. The bottom of Figure 4A shows a model of a folded DNA sheet positioned on another DNA sheet to generate an assembly of two and three layers. The unoccupied three-point-star motif, located within formed hexagon, was positioned on another three-point-star motif of the third layer via a 180 rotation. Upon the formation of the third layer, the distance between the adjacent interactions of the two three-point-star motifs is predicted to be half as much at 15 nm. An AFM image and cross sections of a two- and three-layer assembly are shown in Figure 4B. The blue line crosses over a two-layer assembly to show the height of the DNA architectures. The spacing between adjacent locations of the two three-pointstar motifs is consistent with modeling and varies between 30 and 32 nm. The height of a single layer is 1.2 nm, while the height of the double layer is 2.3 nm. The red line crosses over a three-layer assembly and shows that the spacing between adjacent locations of the two three-point-star motifs is consistent with modeling and varies between 14 and 19 nm. The height of a single layer is 1.3 nm, while the height of the triple layer is 2.4 nm. Since the heights of double and triple layers are similar, we suggest that the third layer is packed within cavities of the bottom two layers. This arrangement of three DNA layers is similar to the cubic close-packing (CCP) of metal atoms since the third layer of the model indicated in black in the triangular inset is rotated 180 with respect to the first sheet (green). The top DNA sheet lies in a unique position different from the bottom two sheets creating an ABC close-packed layer sequence. Green triangles enclose six and ten three-point-star motifs positioned on one another for double and triple layers respectively. Furthermore, DNA height measurements of DNA helices by AFM often reveal values below 2 nm, presumably as a result of the forces exerted by the vibrating tip in tapping mode. To further quantify the distance separating adjacent locations of the two three-point-star motifs that occur in different layers, 276 and 291 measurements were taken along the double layer and triple layers respectively. The distribution of these distances is shown in Figure 4C. Adjacent locations of the two threepoint-star motifs in different layers but positioned on one another is 16.2 nm with a standard deviation of 2.0 nm for the triple layer. For the double layer, the distance was twice as much, 32.2 nm, with a standard deviation of 1.7 nm. The measured distances are in good agreement with the values of the model where the
7 1096 Langmuir, Vol. 25, No. 2, 2009 Koyfman et al. overlay of two three-point-star motifs are 30.3 and nm for the double and triple layers respectively. Figure 5 demonstrates the occurrence of pyramidal architectures containing more than two or three layers at low concentrations of Mg 2+ ions. These multilayer assemblies appear in about 3% of the total number of structures. The number of layers in such a multilayer structure cannot be determined due to compaction of the DNA sheets. Based on the height of two and three layer structure (Figure 4) we estimate the multilayer structures in Figures 5 and 1B to contain anywhere from 5 to 11 layers. Conclusions In conclusion, we describe the formation of multilayer DNA structures from three-point-star motifs which self-assemble into hexagons and hexagonal 2D sheets. The formation of smaller multilayer structures of a defined geometrical shape was observed at low Mg 2+ concentration while the formation of larger singlelayer and multilayer 2D sheets was observed at higher Mg 2+ concentration. Moiré patterns were observed when the images of single layer architectures were taken on the µm scan and were useful for determination of the domains within the architectures. The most predominant orientations of a two-layer assembly were determined to be translation of 17.5 nm of one layer with respect to another where 3-point-star motifs are positioned 30 nm with respect to one another, 30 and 20 rotations of the two layers. Three-layer assemblies with cubic close-packing are even more densely packed where 3-point-star motifs are separated by 15 nm. A small portion of assemblies at low Mg 2+ concentration form multilayer structures with more than three layers. High resolution visualization of these structures is beyond the capability of atomic force microscopy, but we believe threedimensional architectures to be one of the exciting directions of the nucleic acid nanotechnology. Unlike the formation of DNA crystals or DNA hydrogels, layer by layer assembly has an advantage as various layers can pack within three-dimensional structures, thereby providing different pore sizes for guest molecule incorporation. Acknowledgment. Funding for this work was provided by the Institute for Collaborative Biotechnologies (UCSB) to N. Reich. We wish to thank Gary Braun and Dr. Michael Rubinstein for helpful discussions and critical review of the manuscript, and Dr. Sergey Belikov for help with LabView for the Moiré pattern analysis. Supporting Information Available: Materials and Methods, density dependence of DNA arrays, and degradation of multilayer DNA arrays are presented. This material is available free of charge via the Internet at LA801306J
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