DNA Origami as Seeds for Promoting Protein Crystallization - ACS

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Biological and Medical Applications of Materials and Interfaces

DNA Origami as Seeds for Promoting Protein Crystallization Bo Zhang, Andy Ran Mei, Mark Antonin Isbell, Dianming Wang, Yiwei Wang, Suk Fun Tan, Xsu Li Teo, Li-Jin Xu, Zhongqiang Yang, and Jerry Y.Y. Heng ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.8b15629 • Publication Date (Web): 28 Nov 2018 Downloaded from http://pubs.acs.org on December 1, 2018

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ACS Applied Materials & Interfaces

DNA Origami as Seeds for Promoting Protein Crystallization Bo Zhang†,‡, Andy R. Mei‡,§, Mark Antonin Isbell‡,§, Dianming Wang‡, Yiwei Wang⊥, Suk F. Tan‡, Xsu L. Teo‡, Lijin Xu*,†, Zhongqiang Yang*,‡, Jerry Y. Y. Heng*,§ †

Department of Chemistry, Renmin University of China, Beijing 100872, PR China. Key Laboratory of Organic Optoelectronics & Molecular Engineering of the Ministry of Education, Department of Chemistry, Tsinghua University, Beijing 100084, PR China. § Surfaces and Particle Engineering Laboratory (SPEL), Department of Chemical Engineering, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom. ⊥ State Key Laboratory of Biomembrane, Center for Structural Biology School of Life Sciences and School of Medicine, Tsinghua University, Beijing 100084, PR China. ‡

Corresponding authors: Lijin Xu ([email protected]); Zhongqiang Yang ([email protected]); Jerry Y. Y. Heng ([email protected])

ABSTRACT: This study reports the first experimental evidence of DNA origami as a seed resulting in the increase in probability of protein crystallization. Using DNA origami constructed from long single-stranded M13 DNA scaffolds folded with short single-stranded DNA staples, it was found that the addition of the DNA origami in concentrations of 2-6 nM to mixtures of a well-characterized protein (Catalase) solution (1.0-7.0 mg/mL) resulted in a higher proportion of mixtures with successful crystallization, up to 11x greater. The improvement to crystallization is evident particularly for mixtures with low concentrations of Catalase (< 5 mg/mL). DNA origami in different conformations: a flat rectangular sheet and a tubular hollow cylinder, were examined. Both conformations improved crystallization as compared to control experiments without M13 DNA or non-folded M13 DNA, but exhibited little difference in the extent of protein crystallization improvement. This work confirms predictions of the potential use of DNA origami to promote protein crystallization, with potential application to systems with limited protein available or difficult to crystallize. KEYWORDS: DNA Nanotechnology, DNA origami, DNA nanostructure, protein crystallization, DNA-protein interaction. molecules at the nanometer length scale.4,20-24 The huge potential for DNA origami in the control of micromolecular assembly or macromolecular organization,25 along with the many underlying complexities, presents research significant opportunities.26,27 The powerful capabilities of DNA origami have already begun to be proven, such as its use as templates for the patterning of targeted proteins,28-32 organic or inorganic molecules33-36 and their synthesis.37,38 In addition to these applications, Professor Seeman proposed 30 years prior that protein crystallization could be attained for an array of molecules arranged in a highly ordered structure of DNA building blocks. Moreover, regardless of the fact that attempts of templating protein crystallization with DNA frameworks have thus far been unsuccessful, Seeman and his co-workers have crystallized a variety of self-assembling DNA crystals by designing periodic nucleic acid structures in one, two and three dimensions.39-43 Based on these researches, we proposed to apply DNA scaffold into protein crystallization.

Introduction DNA origami is one of the most promising materials in biotechnology with a plethora of wide-ranging applications, largely used as the primary building block for self-assembled structures.1 Since the time when DNA origami techniques were first put forward by Rothemund et al. in 2006,2 DNA origami has been applied in many fields including nanomaterials and nanomedicine.3-7 To create DNA origami, hundreds of short single strands of DNA (staples) are used to direct the folding of a long single strand of circular DNA (scaffold, ca. ~8000 bases), allowing for the building of highly customizable 2D and 3D nanostructures.8-12 The highly versatile nature of the size and molecular arrangement of DNA origami allow for its design into an enormous variety of geometric shapes.2,13-19 The ability to make precise individual molecule adjustments in the DNA origami structure along with its great biological compatibility makes DNA origami a powerful tool for the precise organization and manipulation of 1

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batch, such as physical and chemical property, which is unfavorable for repeating experiment and explaining the crystallization mechanism. Herein, we propose for the first time that DNA origami can be utilized as a seed to promote protein crystallization. With programmable property and precise recognition, we can accurately control size and morphology of DNA origami and ensure perfectly consistent performance of this material. In this study Catalase was used as a model protein, along with DNA origami constructed from M13 and staple strands.

The investigation of new methods to enhance and control protein crystallization is particularly valuable,44,45 especially for studies involving long nucleation times or the crystallization of target proteins that are difficult to obtain.46-53 Seeding method is an easy way to crystallize protein, especially heterogeneous nucleants. The main researches of nucleation agents have studied some natural surfaces such as horse tail hairs, minerals, fibers, lipid layers;54-57 fabricated surfaces like silicons and polymeric films, showing specific pores and wrinkles;58,59 epitaxic nucleants which require a correlation between the lattice of the heterogeneous nucleating agent and the nascent protein crystal;60 However, it is difficult to make these materials consistent in nanoscale from batch to

Scheme 1. Experimental setup of the hanging-drop vapor diffusion chamber, containing 5 droplets of different mixture types, with a reservoir of precipitant solution at the bottom.

2


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Figure 1. (a) Crystal percentage, the percentage of droplets with observable crystals in them, after 11 days with 6 nM DNA origami (triangle), unfolded M13rs with unfolded M13 plus random staple strands (pentagon) and Blank without any additives (five-pointed star) for Catalase （Cat） at 1.0 mg/mL at 4 °C, (b) crystal percentage with 6 nM DNA origami (triangle) and Blank without additives (five-pointed star) for Catalase (Cat) at 1.5 mg/mL (red line) and 7.0 mg/mL (pink line) at 4 °C, and (c) crystal percentage with 6 nM DNA origami (triangle) and Blank without additives (five-pointed star) for Catalase (Cat) at 3.0 mg/mL (blue line) and 5.0 mg/mL (orange line) at 4 °C

As illustrated in Scheme 1, we chose DNA origami with two conformations: ‘Rectangle’ which consists of rectangular-shaped DNA origami, ‘Tube’ which consists of tubular-shaped DNA origami (Dimeter = 11 nm) folded from Rectangle origami with the aid of staple strands at the sides. These origami structures have the same total surface area but different geometries. As control, we chose ‘M13rs’ which consists of the M13 framework and random non-binding staple strands, ‘M13’ which consists of the M13 framework, and ‘Blank’ which had no additives other than the precipitant solution. The crystallization was carried out using the hanging-drop vapor diffusion technique. This work would investigate how the addition of DNA origami in protein crystallization buffer would enhance the probability of crystallization and to demonstrate unequivocally that the structure of DNA origami as seeds is essential in promoting protein crystallization. The attempt to crystallize protein with DNA origami not only opens a new application of DNA

origami, but also provides a new platform for protein crystallization for isolation and purification. In the long term, with the advantage of precise control over DNA origami, this approach may reveal the fundamental protein nucleation process and generate a step change in development of biopharmaceutical products.

RESULTS AND DISCUSSION The influence of DNA origami on protein crystallization was first examined. As depicted in Scheme 1, the hanging-drop vapor diffusion technique was employed, with the arrangement of DNA origami in two conformations; M13rs and M13 with a further control experiment (Blank, without DNA present). Each mixture type was repeated 144 times. The degree of crystallization was evaluated with the quantity denoted as crystal percentage, i.e., the percentage of droplets with observable crystals present within them over a period of 3



time, usually when crystal growth reaches a plateau. Figures 1a, 1b and 1c show the increase in the number of droplets with crystals over a period of 11 days. Figure 1a demonstrates that 6 nM DNA origami (average value of Tube and Rectangle) had a clear effect on the crystallization probability of Catalase, where the presence of DNA origami resulted in a significant increase in crystal percentage, from 1% to 17%. The presence of M13rs provided a small improvement in crystallization but to a much smaller extent, suggesting that the ordered structure of the DNA origami is one of the main contributions to this effect. We believe that the nonspecific intermolecular interactions between the DNA origami and the protein molecules cause the protein molecules to adsorb onto the DNA nanostructure, resulting in an increase in the local protein concentration61-63 as well as potentially stabilizing the protein conformation. And also, DNA origami and Catalase both have overall negative charge47,64, remaining Mg2+ ions in DNA

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origami assemble process may act as salt bridge to link DNA origami and Catalase molecules, which possibly also facilitates protein molecules to interact with DNA origami. This ordered nanostructure may provide a significantly easier pathway to the super-saturation conditions required for crystal nucleation, compared to the disordered case for both M13rs and Blank. Figure 1b shows a comparison of the crystal percentage for two different protein concentrations (1.5 and 7.0 mg/mL) demonstrating that the effect of 6 nM DNA origami is reduced at higher protein concentrations. This is further demonstrated in Figure 1c where the other concentrations of Catalase (3.0 and 5.0 mg/mL) are displayed. From Figure 1, it is concluded that the extent to which 6 nM DNA origami promoted protein crystallization was proportionally greater at lower concentrations and smaller at higher concentrations of Catalase.

Figure 2. Crystal percentage with Blank without additives (five-pointed star), 6 nM M13rs with unfolded M13 plus random staple strands (pentagon) and unfolded M13 (rhombus) for Catalase (Cat) at 1.0 mg/mL (black line), 1.5 mg/mL (red line), 3.0 mg/mL (blue line), 5.0 mg/mL (orange line) and 7.0 mg/mL (pink line) at 4 °C.

At a Catalase concentration of 1.0 mg/mL, the crystal

super-saturation conditions because of the larger number of

percentage increased by more than 11 times from a success rate

protein molecules overcoming the energy barrier. The

of 1.4% for the Blank mixture to 16.3% for the DNA origami.

influence of DNA origami therefore became much smaller

For the 1.5 mg/mL Catalase concentration however, the crystal

since crystals could readily form, independently of the DNA

percentage, proportionally, increased by significantly less ~5

origami structure. At lower concentrations however, it seems

times from 4.2% for the Blank mixture to 24.7% for the DNA

the DNA origami provides an ordered framework on which

origami.

protein molecules can form clusters more easily. This aspect of

At higher protein concentrations, there is a greater

DNA origami’s influence on crystallization at low protein

probability of protein molecules aggregating together and

concentrations indicates the excellent potential of DNA

achieving the necessary critical size for nucleation. Therefore,

origami as a crystallization booster for systems with scarcer

crystallization generally occurs more readily with increasing

amounts of the protein. In addition to improving systems 4


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where the protein is difficult to crystallize, DNA origami could

solution without ordered structure, which is a likely cause for

significantly reduce the waste of valuable protein that may be

the distinction seen in Figure 1a between DNA origami and

difficult to acquire or synthesize and so maximize the efficient

M13rs. While the large M13 molecule plus random strands

use of protein resources.

might still have provided an aggregation site for the protein molecules

Figure 2 shows how both 6 nM M13 and M13rs did very

hence

the

small

improvement

in

protein

crystallization, its effect was not comparable to that of the

little to improve crystallization versus Blank consistently at all

highly structured DNA origami.

five protein concentrations ranging from 1.0 to 7.0 mg/mL. So while DNA origami is seen to significantly promoted protein

Additionally, the conformation of DNA origami, in the

crystallization, it is clear that its constituent components in

form of rectangular sheets or tubular hollow cylinders, was

M13rs on their own appear to have nowhere near the same

investigated. Figure 3 shows that 6 nM DNA origami in the

effect. In the ordered structure of DNA origami, all of the DNA

form of Rectangles or Tubes, unexpectedly, did not improve

strands are held tightly together within the M13 framework.

crystallization rates further. The structural differences between

We suspect that this results in a greater collection of elevated

the two are expected to have a noticeable impact on the

DNA concentration sites, allowing for stronger intermolecular

crystallization rates, given that the rectangular conformation

interactions between the DNA origami and the protein

has twice the exposed surface area versus the tubular

molecules. For the M13rs, which contains same amount of

configuration, and therefore would allow for double the

DNA as DNA origami, but with random sequence, therefore,

potential sites for intermolecular

the M13 and the staple strands are randomly dispersed in

Figure 3. Crystal percentage over a period of 11 days with 6 nM Rectangle conformation DNA origami (square) and Tube conformation DNA origami (circle) for Catalase (Cat) at 1.0 mg/mL (black line), 1.5 mg/mL (red line), 3.0 mg/mL (blue line), 5.0 mg/mL (orange line) and 7.0 mg/mL (pink line) at 4 °C.

5



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Figure 4. Crystal percentage for 5 mg/mL Catalase (Cat) over a period of 11 days with the Tube conformation DNA origami at different concentrations of 0 nM (black line), 2 nM (red line), 4 nM (blue line) and 6 nM (pink line) at 4°C. interactions with the protein molecules. On the other hand, the

exist a critical seed-loading amount, above which additional

tubular hollow cylinders may provide a confinement

DNA origami seeding has no effect on the amount of

effect.

47,65-67

As we know, only in pores with suitable size, can 65,67

crystallization rate. Within this system, the data in Figure 4

Here, it may be

suggests that this potential limit has been reached at a DNA

likely that the effects of point interactions are as effective as

origami concentration of 4 nM, with very little further

confinement, since trapping protein molecules in the

improvement in crystallization at 6 nM.

protein molecules accumulate efficiently.

pseudo-pores of the DNA origami would result in an increase

The many factors that affect DNA origami in promoting

in local protein concentration. And also, we designed different

protein crystallization, including the intermolecular forces, the

pore sizes of tubular DNA origami (diameter = 8, 11, 22 nm) at

structure of the DNA, potential artificial porosity and seeding

the same concentration to promote Catalase crystallization

effects, are all still relatively unexplored in terms of their

respectively. As a result (Figure S2), all the three pore sizes of

specific mechanics with crystallization and are areas for future

Tube can remarkably improve Catalase crystallization success

study. Future efforts in applying our methodology would focus

rate compared with Blank condition, but has little difference to

on more complicated structures of DNA origami with size

promote protein crystallization success rate among these DNA

tuned at 1 nm resolution, adapting it to fragile and difficult to

origami with various diameters. Figure 4 displays the crystal

crystallize proteins, in order to establish a general scheme for

percentage with increasing Tube conformation DNA origami

protein crystallization and separation.

concentration from 0 to 6 nM. From these results, Tube concentration was increased from 2 to 4 nM, but the

CONCLUSION

crystallization success rate respectively did not double in the

We report a new approach using DNA origami as seeds to

same way. This indicates a non-linear relationship between the

improve the crystallization probability of complex molecules

exposed surface area of the DNA origami and the rate of

such as proteins. The probability for protein crystallization was

crystallization, suggesting that other factors are behind the

enhanced with the presence of DNA origami, especially at low

Rectangle and Tube conformations having similar crystal

protein concentrations. The extent of this improvement was,

growth rates despite their shape difference. One possible

unexpectedly, similar for both rectangular and tubular

explanation is that beyond a certain concentration, there may 6


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conformations of DNA origami, suggesting that several

of the rectangular DNA origami (Rectangle) used was 35 nm ×

mechanisms may be involved in protein crystallization

100 nm. The diameter of the corresponding rolled-up tubular

promoted by DNA origami. Additionally, it was seen that there

DNA origami (Tube) was 11 nm × 100 nm with 2 nm in wall

exists a critical loading of the DNA origami, above which there

thickness. Atomic force microscopy (AFM) was employed to

was no improvement to the probability of crystallization. The

characterize the morphology of the rectangular and tubular

increase in crystallization was not observed in cases where the

structure (Supporting Information, Figure 1).

DNA was not ordered. We are trying to realize Seeman’s idea

As the protein crystallization required a precipitant

that protein can be crystallize within DNA scaffold. This may

solution of 25 mM HEPES (pH 7.0), 5% w/v PEG-4000 and 5%

be successful with DNA origami clusters with numerous pores

v/v MPD, the assembly buffer of the DNA origami needs to be

69,70

research which is on-going in

removed and replaced with said precipitant solution, using

our group. The ability to precisely manipulate DNA origami

buffer exchange.68 After removal of the assembly buffer, DNA

structure and chemistry will allow for the potential to finely

origami was dissolved in 25 mM HEPES (pH 7.0), 5% w/v

control macromolecular assembly such as nucleation and

PEG-4000 and 5% v/v MPD. The concentration of DNA

crystallization to a much greater extent.

origami after buffer exchange was 6 nM as determined with a

designed by Y. Ke’s group,

UV-Vis Spectrophotometer. The morphology of DNA origami was characterized by AFM. It was verified that DNA origami

MATERIALS AND METHODS

can stay intact for 15 days at least (Supporting Information,

Materials

Table S1). Therefore, we are certain that DNA origami remains

Catalase as lyophilized powders (C40) and 2-methyl-1,

undamaged over the crystallization period.

3-propanediol (MPD) were purchased from Sigma-Aldrich.

Three control conditions were made to compare to the

M13 was purchased from New England Biolabs. All staple

DNA origami mixtures: M13rs - M13 with random strands

strands purified by HPLC were purchased from Zixi Bio

incapable of hybridizing or assembly into DNA origami

(Beijing, China). HEPES was purchased from Xinjing

collectively dissolved in precipitant solution at 6 nM

Biological Science Technologies Co. (Beijing, China).

concentration, M13 - M13 dissolved in precipitant solution at 6

PEG-4000 was purchased from Alfa Aesar. CH3COOH was

nM concentration, Blank – precipitant solution with no

purchased from Guangfu (Tianjing, China). Mg(OAc)2, EDTA

additional chemicals.

and Tris were purchased from Tianjin Fuchen (Tianjing, China).

Protein crystallization experiment

For all reagents, analytical grade was purchased.

Protein crystallization was performed with custom-made

Protein samples

plates using the hanging-drop vapor-diffusion method.

Catalase was dissolved in 25 mM HEPES (pH 7.0).

Crystallization drops were made by mixing 1.5 μL of protein

Filtration of protein samples and all the solution for

solution and an equal volume of one of the five precipitant

crystallization through 0.22 µm mesh size filters was the

solution mixtures designated as: Rectangle, Tube, M13rs, M13,

standard procedure used before setting up trials for

and Blank. The drops were equilibrated against 333 μL of the

crystallization. The concentrations of Catalase were 1.0, 1.5,

precipitant solution in the reservoir well as shown in Scheme 1.

3.0, 5.0 and 7.0 mg/mL.

The precipitant solution for Catalase was comprised of 25 mM

DNA origami preparation

HEPES (pH 7.0), 5% w/v PEG-4000 and 5% v/v MPD. After

DNA origami was prepared using an established

the crystallization plates were sealed, the plates were set in an

procedure detailed in literature.68 The DNA origami was

incubator and incubated at 4 °C for two weeks with daily

prepared in an assembly buffer containing: 12.5 mM

examination. The effects of the DNA on the nucleation of

Mg(OAc)2, 20 mM CH3COOH, 40 mM Tris, 2 mM EDTA, pH

protein crystals were studied by counting the number of drops

8.0. It was annealed at 95 °C for 5 mins, then exposed to a

with crystals. Each drop type was repeated 144 times for one

temperature decrease at a rate of 1 °C/min until 4 °C. The size 7



Page 8 of 12

data set of all five mixtures at all five concentrations. The

Applications in Cancer Therapy. Cancer Sci. 2017, 108, 1535–

crystals in the crystallization solution were observed using an

1543.

optical microscope (SZM-T4).

(7)

Loescher, S.; Groeer, S.; Walther, A. 3D DNA Origami

Nanoparticles: From Basic Design Principles to Emerging Applications in Soft Matter and (Bio‐) Nanosciences. Angew. Chem. Int. Ed. 2018, 57, 10436–10448.

Supporting Information. AFM

pictures

of

DNA origami,

Figures

of

(8)

protein

Han, D.; Pal, S.; Nangreave, J.; Deng, Z.; Liu, Y.; Yan, H.

DNA Origami with Complex Curvatures in Three-Dimensional

crystallization success rate with 8, 11, 22 nm diameter, crystal

Space. Science 2011, 332, 342–347.

pictures of all the conditions and base sequence of DNA

(9)

origami.

Kauert, D. J.; Kurth, T.; Liedl, T.; Seidel, R. Direct

Mechanical Measurements Reveal the Material Properties of Three-Dimensional DNA Origami. Nano Lett. 2011, 11, 5558– 5563.

ACKNOWLEDGMENTS

(10) Liu, W.; Zhong, H.; Wang, R.; Seeman, N. C. Crystalline Two ‐ Dimensional DNA ‐ Origami Arrays. Angewandte

This work was supported by the National Natural Science Foundation of China (21474059, 21372258). ZY and JYYH

Chemie 2011, 123, 278-281.

acknowledge the Royal Academy of Engineering – Research

(11) Arbona, J. M.; Aimé, J. P.; Elezgaray, J. Cooperativity in

Exchange China and India (RECI) programme (Reference:

the Annealing of DNA Origamis. J. Chem. Phys. 2013, 138,

1314RECI047). JYYH also acknowledges the EPSRC

015105.

(EP/N015916/1) for funding. We acknowledge the Tsinghua

(12) Shen, H.; Wang, Y.; Wang, J.; Li, Z.; Yuan, Q. Emerging

University Branch of China National Center for Protein

Biomimetic Applications of DNA Nanotechnology. ACS Appl.

Sciences Beijing for technical support.

Mater. Interfaces 2018. (13) Liu X.; Zhang F.; Jing X.; Pan M.; Liu P.; Li W.; Zhu B.; Li J.; Chen H.; Wang L.; Lin J.; Liu Y.; Zhao D.; Yan H.; Fan C. Complex Silica Composite Nanomaterials Templated with

REFERENCES (1)

DNA Origami. Nature 2018, 559, 593.

Seeman, N. C. Nucleic Acid Junctions and Lattices. J.

(14) Andersen, E. S.; Dong, M.; Nielsen, M. M.; Jahn, K.;

Theor. Biol. 1982, 99, 237–247. (2)

Lind-Thomsen, A.; Mamdouh, W.; Gothelf, K. V.; Besenbacher,

Rothemund, P. W. K. Folding DNA to Create Nanoscale

F.; Kjems, J. DNA Origami Design of Dolphin-Shaped

Shapes and Patterns. Nature 2006, 440, 297–302. (3)

Structures with Flexible Tails. ACS Nano 2008, 2, 1213–1218.

Aldaye, F. A.; Palmer, A. L.; Sleiman, H. F. Assembling

(15) Andersen, E. S.; Dong, M.; Nielsen, M. M.; Jahn, K.;

Materials with DNA as the Guide. Science 2008, 321, 1795–

Subramani, R.; Mamdouh, W.; Golas, M. M.; Sander, B.; Stark,

1799. (4)

H.; Oliveira, C. L. P.; Pedersen J. S.; Birkedal V.; Besenbacher

Li, J.; Fan, C.; Pei, H.; Shi, J.; Huang, Q. Smart Drug

Delivery

Nanocarriers

with

Self-Assembled

F.; Gothelf K. V.; Kjems J. Self-Assembly of a Nanoscale DNA

DNA

Box with a Controllable Lid. Nature 2009, 459, 73–76.

Nanostructures. Adv. Mater. 2013, 25, 4386–4396. (5)

(16) Chen, Z.; Choi, C. K. K.; Wang, Q. Origin of the

Wu, N.; Czajkowsky, D. M.; Zhang, J.; Qu, J.; Ye, M.;

Plasmonic Chirality of Gold Nanorod Trimers Templated by

Zeng, D.; Zhou, X.; Hu, J.; Shao, Z.; Li, B.; Fan C. Molecular

DNA Origami. ACS Appl. Mater. Interfaces 2018, 10,

Threading and Tunable Molecular Recognition on DNA

26835−26840.

Origami Nanostructures. J. Am. Chem. Soc. 2013, 135, 12172–

(17) Song, J.; Li, Z.; Wang, P.; Meyer, T.; Mao, C.; Ke, Y.

12175. (6)

Reconfiguration of DNA Molecular Arrays Driven by

Udomprasert, A.; Kangsamaksin, T. DNA Origami 8


Page 9 of 12 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 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


Information relay. Science 2017, 357, eaan3377.

(29) Chhabra, R.; Sharma, J.; Ke, Y.; Liu, Y.; Rinker, S.;

(18) Chandrasekaran, A. R.; Levchenko, O. DNA Nanocages.

Lindsay, S.; Yan, H. Spatially Addressable Multi-Protein

Chem. Mater. 2016, 28, 5569–5581.

Nanoarrays

(19) Peng, Z.; Liu, H. Bottom-up Nanofabrication Using DNA

Nanoarchitectures. J. Am. Chem. Soc. 2007, 129, 10304–

Nanostructures. Chem. Mater. 2016, 28, 1012–1021.

10305.

(20) Williams, B. A. R.; Lund, K.; Liu, Y.; Yan, H.; Chaput, J.

(30) Fu, J.; Liu, M.; Liu, Y.; Woodbury, N. W.; Yan, H.

C. Self-Assembled Peptide Nanoarrays: An Approach to

Interenzyme Substrate Diffusion for an Enzyme Cascade

Studying Protein–Protein Interactions. Angew. Chem. Int. Ed.

Organized on Spatially Addressable DNA Nanostructures. J.

Templated

by

Aptamer

Tagged

DNA

2007, 119, 3111–3114.

Am. Chem. Soc. 2012, 134, 5516–5519.

(21) Lund, K.; Manzo, A. J.; Dabby, N.; Michelotti, N.;

(31) Hou, C.; Guan, S.; Wang, R.; Zhang, W.; Meng, F.; Zhao,

Johnson-Buck, A.; Nangreave, J.; Taylor, S.; Pei, R.;

L.; Xu, J.; Liu, J. Supramolecular Protein Assemblies Based on

Stojanovic, M. N.; Walter, N. G.; Winfree E.; Yan H.

DNA Templates. J. Phys. Chem. Lett. 2017, 8, 3970–3979.

Molecular Robots Guided by Prescriptive Landscapes. Nature

(32) Kurokawa, T.; Kiyonaka, S.; Nakata, E.; Endo, M.;

2010, 465, 206–210.

Koyama, S.; Mori, E.; Tran, N. H.; Dinh, H.; Suzuki, Y.;

(22) Diagne, C. T.; Brun, C.; Gasparutto, D.; Baillin, X.; Tiron,

Hidaka, K.; Kawata, M.; Sato, C.; Sugiyama, H.; Morii, T.;

R. DNA Origami Mask for Sub-Ten-Nanometer Lithography.

Mori, Y. DNA Origami Scaffolds as Templates for Functional

ACS Nano 2016, 10, 6458–6463.

Tetrameric Kir3 K+ Channels. Angew. Chem. Int. Ed. 2018, 130,

(23) Izabela, K.; Johann, B.; Sebastian, M.; Philip, T.;

2616-2621.

Guillermo, P. A. Strong Plasmonic Enhancement of a Single

(33)

Peridinin−Chlorophyll a−Protein Complex on

Nanomanufacturing with DNA Origami: Factors Affecting the

DNA Origami-Based Optical Antennas. ACS Nano 2018, 12,

Kinetics and Yield of Quantum Dot Binding. Adv. Funct. Mater.

1650−1655.

2012, 22, 1015–1023.

(24) Tokura, Y.; Jiang, Y.; Welle, A.; Stenzel, M. H.; Krzemien,

(34) Schreiber, R.; Do, J.; Roller, E.-M.; Zhang, T.; Schüller, V.

K. M.; Michaelis, J.; Berger, R.; Barner‐Kowollik, C.; Wu, Y.;

J.; Nickels, P. C.; Feldmann, J.; Liedl, T. Hierarchical

Weil, T. Bottom‐Up Fabrication of Nanopatterned Polymers

Assembly of Metal Nanoparticles, Quantum Dots and Organic

on DNA Origami by In Situ Atom ‐ Transfer Radical

Dyes using DNA Origami Scaffolds. Nat. Nanotechnol. 2014,

Polymerization. Angewandte Chemie 2016, 128, 5786-5791.

9, 74–78.

(25) Helmi, S.; Ziegler, C.; Kauert, D. J.; Seidel, R.

(35) Bui, H.; Shah, S.; Mokhtar, R.; Song, T.; Garg, S.; Reif, J.

Shape-Controlled Synthesis of Gold Nanostructures Using

Localized DNA Hybridization Chain Reactions on DNA

DNA Origami Molds. Nano letters 2014, 14, 6693-6698.

Origami. ACS Nano, 2018, 12, 1146–1155.

(26) Gür, F. N.; Schwarz, F. W.; Ye, J.; Diez, S.; Schmidt, T. L.

(36) Wang, Z. G.; Liu, Q.; Li, N.; Ding, B. DNA-Based

Toward Self-Assembled Plasmonic Devices: High-Yield

Nanotemplate

Directed

Arrangement of Gold Nanoparticles on DNA Origami

Nanoclusters

with

Templates. ACS Nano 2016, 10, 5374–5382.

Surface-Guided Chemical Reactions. Chem. Mater. 2016, 28,

(27) Krissanaprasit, A.; Madsen, M.; Knudsen, J. B.;

8834–8841.

Gudnason, D.; Surareungchai, W.; Birkedal, V.; Gothelf, K. V.

(37) Voigt, N. V; Tørring, T.; Rotaru, A.; Jacobsen, M. F.;

Programmed Switching of Single Polymer Conformation on

Ravnsbæk, J. B.; Subramani, R.; Mamdouh, W.; Kjems, J.;

DNA Origami. ACS Nano 2016, 10, 2243–2250.

Mokhir, A.; Besenbacher, F.; Gothelf K. V.; Single-Molecule

(28) Yan, H.; Park, S. H.; Finkelstein, G.; Reif, J. H.; Labean,

Chemical Reactions on DNA Origami. Nat. Nanotechnol. 2010,

T. H. DNA-Templated Self-Assembly of Protein Arrays and

5, 200–203.

Highly Conductive Nanowires. Science 2003, 301, 1882–1884.

(38) Bald, I.; Keller, A. Molecular Processes Studied at a

Ko,

S.

9


H.;

Gallatin,

in

G.

Situ

Specific

M.;

Liddle,

Synthesis Fluorescent

of

J.

A.

Silver

Emission:


Page 10 of 12

Single-Molecule Level using DNA Origami Nanostructures

(49) Hu, Y.; Chen, Z.; Fu, Y.; He, Q.; Jiang, L.; Zheng, J.; Gao,

and Atomic Force Microscopy. Molecules 2014, 19, 13803–

Y.; Mei, P.; Chen, Z.; Ren, X. The Amino-Terminal Structure

13823.

of Human Fragile X Mental Retardation Protein Obtained

(39) Zheng, J.; Birktoft, J. J.; Chen, Y.; Wang, T.; Sha, R.;

using Precipitant-Immobilized Imprinted Polymers. Nat.

Constantinou, P. E.; Ginell, S. L.; Mao, C.; Seeman, N. C.

Commun. 2015, 6, 6634.

From Molecular to Macroscopic via the Rational Design of a

(50) Kowacz, M.; Marchel, M.; Juknaite, L.; Esperanca, J. M.

Self-Assembled 3D DNA Crystal. Nature 2009, 461, 74–77.

S. S.; Romao, M. J.; Carvalho, A. L.; Rebelo, L. P. N.

(40) Hernandez,

C.;

Birktoft,

J.

J.;

Ohayon,

Y.

P.;

Ionic-Liquid-Functionalized Mineral Particles for Protein

Chandrasekaran, A. R.; Abdallah, H.; Sha, R.; Stojanoff, V.;

Crystallization. Cryst. Growth Des. 2015, 15, 2994–3003.

Mao, C.; Seeman, N. C. Self-Assembly of 3D DNA Crystals

(51) Xing, Y.; Hu, Y.; Jiang, L.; Gao, Z.; Chen, Z.; Chen, Z.;

Containing a Torsionally Stressed Component. Cell Chem. Biol.

Ren, X. Zwitterion-Immobilized Imprinted Polymers for

2017, 24, 1401–1406.

Promoting the Crystallization of Proteins. Cryst. Growth Des.

(41) Seeman, N. C.; Gang, O. Three-Dimensional Molecular

2015, 15, 4932–4937.

and Nanoparticle Crystallization by DNA Nanotechnology.

(52) Li, F.; Lakerveld, R. Influence of Alternating Electric

MRS Bull. 2017, 42, 904–912.

Fields on Protein Crystallization in Microfluidic Devices with

(42) Simmons, C. R.; Zhang, F.; MacCulloch, T.; Fahmi, N.;

Patterned Electrodes in a Parallel-Plate Configuration. Cryst.

Stephanopoulos, N.; Liu, Y.; Seeman, N. C.; Yan, H. Tuning

Growth Des. 2017, 17, 3062–3070.

the Cavity Size and Chirality of Self-Assembling 3D DNA

(53) de Poel, W.; Münninghoff, J. A.; Elemans, J. A.; van

Crystals. J. Am. Chem. Soc. 2017, 139, 11254–11260.

Enckevort, W. J.; Rowan, A. E.; Vlieg, E. Surfaces with

(43) Brady, R. A.; Brooks, N. J.; Cicuta, P.; Di Michele, L.

Controllable Topography and Chemistry Used as a Template

Crystallization of Amphiphilic DNA C-Stars. Nano Lett. 2017,

for Protein Crystallization. Cryst. Growth Des. 2018, 18, 763–

17, 3276–3281.

769.

(44) Drioli, E.; Di Profio, G.; Curcio, E. Membrane-Assisted

(54) Thakur, A. S.; Robin, G.; Guncar, G.; Saunders, N. F. W.;

Crystallization Technology. World Scientific 2015.

Newman, J.; Martin, J. L.; Kobe, B. Improved Success of

(45) Asanithi, P.; Saridakis, E.; Govada, L.; Jurewicz, I.;

Sparse

Brunner, E. W.; Ponnusamy, R.; Cleaver, J. A. S.; Dalton, A. B.;

Heterogeneous Nucleating Agents. PLoS One 2007, 2, e1091.

Chayen, N. E.; Sear, R. P. Carbon-Nanotube-Based Materials

(55) D’Arcy, A.; Mac Sweeney, A.; Haber, A. Using Natural

for Protein Crystallization. ACS Appl. Mater. Interfaces 2009,

Seeding

1, 1203–1210.

Crystallization Experiments. Acta Crystallogr. - Sect. D Biol.

(46) Saridakis, E.; Khurshid, S.; Govada, L.; Phan, Q.;

Crystallogr. 2003, 59, 1343–1346.

Hawkins, D.; Crichlow, G. V.; Lolis, E.; Reddy, S. M.; Chayen,

(56) Kimble, W. L.; Paxton, T. E.; Rousseau, R. W.; Sambanis,

N. E. Protein Crystallization Facilitated by Molecularly

A. The Effect of Mineral Substrates on the Crystallization of

Imprinted Polymers. PNAS 2011, 108, 11081-11086.

Lysozyme. J. Cryst. Growth 1998, 187, 268–276.

(47) Shah, U. V.; Allenby, M. C.; Williams, D. R.; Heng, J. Y.

(57) Edwards, A. M.; Darst, S. A.; Hemming, S. A.; Li, Y.;

Y. Crystallization of Proteins at Ultralow Supersaturations

Kornberg, R. D. Epitaxial Growth of Protein Crystals on Lipid

using Novel Three-Dimensional Nanotemplates. Cryst. Growth

Layers. Nature 1994, 1, 638–653.

Des. 2012, 12, 1772–1777.

(58) Chayen, N. E.; Saridakis, E.; El-Bahar, R.; Nemirovsky,

(48) Abdallah, B. G.; Kupitz, C.; Fromme, P.; Ros, A.

Y. Porous Silicon: An Effective Nucleation-Inducing Material

Crystallization of the Large Membrane Protein Complex

for Protein Crystallization. J. Mol. Biol. 2001, 312, 591–595.

Photosystem I in a Microfluidic Channel. ACS Nano 2013, 7,

(59) Fermani, S.; Falini, G.; Minnucci, M.; Ripamonti, A.

10534–10543.

Protein Crystallization on Polymeric Film Surfaces. J. Cryst.

Matrix

Protein

Material

10


to

Crystallization

Generate

Screening

Nucleation

in

with

Protein

Page 11 of 12 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 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


Growth 2001, 224, 327–334. (60) Mcpherson, A.; Shlichta, P. Epitaxial Nucleation of Protein Crystals. Science 1988, 239, 385–387. (61) Ten Wolde, P. R.; Frenkel, D. Enhancement of Protein Crystal Nucleation by Critical Density Fluctuations. Science 1997, 277, 1975-1978. (62) Galkin, O.; Vekilov, P. G. Are Nucleation Kinetics of Protein Crystals Similar to Those of Liquid Droplets? J. Am. Chem. Soc. 2000, 122, 156–163. (63) Vekilov, P. G. The Two-Step Mechanism of Nucleation of Crystals in Solution. Nanoscale 2010, 2, 2346–2357. (64) Lee B.; Kim S.; Cho J. Multi-Biocatalytic Properties of Layerby- Layer Assembled Lysozyme/Catalase Multilayers. J. Macromol. Res. 2011, 19, 635-638. (65) Chayen, N. E.; Saridakis, E.; Sear, R. P. Experiment and Theory for Heterogeneous Nucleation of Protein Crystals in a Porous Medium. PNAS. 2006, 103, 597–601. (66) Page, A. J.; Sear, R. P. Heterogeneous Nucleation in and out of Pores. Phys. Rev. Lett. 2006, 97, 065701. (67) Shah, U. V.; Williams, D. R.; Heng, J. Y. Y. Selective Crystallization of Proteins using Engineered Nanonucleants. Cryst. Growth Des. 2012, 12, 1362–1369. (68) Wang, D.; Da, Z.; Zhang, B.; Isbell, M. A.; Dong, Y.; Zhou, X.; Liu, H.; Heng, J. Y. Y.; Yang, Z.; Stability Study of Tubular

DNA

Origami

in

the

Presence

of

Protein

Crystallisation Buffer. RSC Adv. 2015, 5, 58734. (69) Ke, Y.; Ong, L. L.; Sun, W.; Song, J.; Dong, M.; Shih, W. M.; Yin, P. DNA Brick Crystals with Prescribed Depths. Nat. Chem. 2014, 6, 994–1002. (70) Tian, Y.; Wang, T.; Liu, W.; Xin, H. L.; Li, H.; Ke, Y.;

Shih, W. M.; Gang, O. Prescribed Nanoparticle Cluster Architectures and Low-Dimensional Arrays Built Using Octahedral DNA Origami Frames. Nat. Nanotechnol. 2015, 10, 637–644.

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