Programmed ph-driven Reversible Association and Dissociation of Inter-Connected. Circular DNA Dimer Nanostructures
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1 Supporting information Programmed ph-driven Reversible Association and Dissociation of Inter-Connected Circular DNA Dimer Nanostructures Yuwei Hu, Jiangtao Ren, Chun-Hua Lu, and Itamar Willner* Institute of Chemistry and The Center for Nanoscience and Nanotechnology, The Hebrew University of Jerusalem, Jerusalem 91904, Israel *Address correspondence to: Tel: +972,2, Fax: +972,2,
2 Materials HEPES sodium salt, sodium chloride, ammonium acetate, magnesium chloride, dithiothreitol, acrylamide/bis-acrylamide (30%), bis(p-sulfonatophenyl)phenylphosphine dihydrate dipotassium salt (BSPP), ethylenediaminetetraacetic acid (EDTA), ammonia persulfide, N,N,N,N -Tetramethylethylenediamine (TEMED), sodium dodecyl sulfate (SDS) and tris(2-carboxyethyl)phosphine hydrochloride were purchased from Sigma Aldrich. Urea was purchased from J.T. Baker Chemical Co.. Ammonium hydroxide solution (25%) was purchased from Riedel-de Haën. Acetic acid glacial was purchased from Bio-Lab Ltd.. Gold colloid 5 nm and 10 nm were purchased from British Biocell. Metaphore agarose was purchased from Lonza. Dialysis tube 10 kda MWCO Snakeskin was purchased from Thermo Scientific. Amicon ultra 100 kda MWCO was purchased from Millipore. Disposable filter units 0.22 µm were purchased from Whateman GmbH. The T4 Polynucleotide Kinase and the Quick Ligation Kit were purchased from New England Biolabs Inc. (NEB). The gel extraction kit (QIAEX II) was purchased from QIAGEN. Ultrapure water from a NANOpure Diamond (Barnstead) source was used in all experiments. Nucleic acid loading dye and SYBR Gold nucleic acid gel stain were purchased from Invitrogen. All DNA oligonucleotides were purchased from Integrated DNA Technologies (Table 1). 2
3 Synthesis of the DNA rings The DNA sequence (R 1 ) was first phosphorylated by using T4 polynucleotide kinase. Then, the phosphorylated DNA (R 1 ) was mixed with the C 2 in the Quick Ligation Reaction Buffer. The resulting mixture was incubated at 90 C for 5 min, instantly cooled down to 25 C and then allowed to react for 40 min, resulting in the hybridization of C 2 with R 1. Then the ligase was added to solution of capped R 1, resulting in the ligation of the 3' and 5' ends of R 1 to form the DNA ring R 1. The volume of the reaction solution was 100 µl, and the concentrations of DNA (R 1 ) and cap (C 2 ) used in the reaction were 2 µm and 10 µm, respectively. The DNA phosphorylation and ligation processes followed the protocols provided by New England Biolabs. The same procedure was used to synthesize DNA ring R 2. Purification of the DNA rings The purification was conducted following the QIAGEN protocol. The solution that contained the DNA ring was loaded on a denatured polyacrylamide electrophoresis gel (9% polyacrylamide; acrylamide/bis-acrylamide 29:1, 7.0 M urea). After electrophoresis, the gel slice that included the DNA ring was excised. The excised gel slice was incubated in the diffusion buffer (0.5 M ammonium acetate; 10 mm magnesium acetate; 1 mm EDTA, ph 8.0; 0.1% SDS) at 50 C for 30 min. The diffusion buffer was then centrifuged, and the supernatant was collected. Buffer solutions QX1 and QIAEX II were added to the supernatant and incubated for 10 min. After centrifugation, the resulting pellet was washed with the PE buffer (20 mm NaCl, 2 mm Tris-HCl, ph=7.5, 80 vol% ethanol) twice. The pellet was air-dried to yield a white color. The DNA ring was extracted from the pellet with HEPES buffer (10 mm, ph 8.0), and its concentration was 3
4 determined spectroscopically. Pre-functionalization of the commercial Au NPs and preparation of the dithiol DNA stock solution The 5 or 10 nm Au NPs, as provided by the manufacturer, were mixed with an excess of bis(p-sulfonatophenyl)phenylphosphine dihydrate dipotassium salt (BSPP) and stirred for 8 hours. The resulting Au NPs were, then, concentrated using Amicon filtering tubes 100 kda MWCO, for 5 min under 3000 g to a final concentration of 1-10 µm (if necessary, a second concentration step was performed using Amicon filtering tubes). The concentration of the Au NPs was estimated by diluting the resulting solution (1:1000), recording the absorption spectrum, and using the respective extinction coefficient of the Au NPs. The concentration of the Au NPs was determined spectroscopically and was stored at +4 C for the further use. The dithiolated modified DNA A 1 and A 2 were diluted to a final concentrations of 15 µm with 15 mm Tris(2-carboxyethyl)phosphine hydrochloride (TCEP), respectively. The DNA solutions were stored at -20 C for the further use. Conjugation of the appropriate nucleic acid to the Au NPs 5 nm AuNPs (2.5 µm) were prepared in a solution that included 0.5 TBE, 0.44 mg/ml BSPP, 100 mm NaCl. The dithiolated DNA (A 1 ), 1.5 µm was mixed with the AuNPs. An auxiliary strand (Comp), 7.0 µm, was added to improve the subsequent separation of the modified AuNPs by gel electrophoresis. 10 nm AuNPs (0.45 µm) were prepared in a solution that included 0.5 TBE, 0.44 mg/ml BSPP, 100 mm NaCl. The dithiolated DNA (A 2 ), 1.2 µm, was mixed with the AuNPs. An auxiliary strand (Comp), 7 µm, was added to improve subsequent separation by gel electrophoresis. 4
5 It should be noted that the auxiliary strand (Comp) was designed to be partly complementary to the strands A 1 or A 2. Purification of the single strand DNA modified AuNPs The single strand-modified AuNPs functionalized with A 1 or A 2 were separated from the polyconjugated DNA-AuNPs existing in the mixture and from unreacted AuNPs on a 3% w/v agarose gel (MetaPhor). The different samples were mixed with 12% v/v glycerol (final concentration), and loaded in the wells of the gel. The gels were run at a constant voltage of 80 V. When satisfactory visual separation was observed, the respective bands were cut, and subjected to a voltage of 100 V inside a closed dialysis membrane filled with 0.5 TBE buffer (in order to release the desired modified NPs from the gel). Then, the solution trapped in the dialysis membrane was collected, filtered with a 0.22 µm syringe filter (Whatman), and concentrated with a 100 kda MWCO Amicon filtering tube. Stabilization of the single strand DNA modified AuNPs The separated single strand modified AuNPs with A 1 or A 2 revealed limited stability, and precipitated with time. To eliminate this difficulty, the different single strand-modified AuNPs were stabilized with an excess of a short thiolated DNA (Stab) in a solution that included 100 mm NaCl, 0.5 TBE and 0.44 mg/ml BSPP. Concomitantly, to the stabilization of the AuNPs, a complementary strand Comp*, to the auxiliary strand Comp, was added in excess to the solution in order to stimulate the stand displacement process of the auxiliary stand (Comp) from the single strand modified AuNPs. The resulting mixtures were incubated at 25 C for 48 h and then washed four times using 100 kda MWCO Amicon filtering tubes, in order to remove the strands Comp and Comp*. At the end, the concentrations of the stabilized-single strand modified-aunps of 5
6 DNA A 1 or A 2 were determined spectroscopically by using the appropriate extinction coefficient of the AuNPs. Tethering of the single strand-modified AuNPs to the DNA rings and reconfiguration of the nanostructures The stabilized-single strand-modified-aunps of DNA (A 1, A 2 ) and DNA rings (R 1, R 2 ) were added to a HEPES buffer solution (1 mm, ph 7.0, MgCl 2 20 mm) and incubated for a time interval of 12 hours to yield the appropriate nanostructures. Auxiliary strands C 2, L 10 or L 20 & L 3 were also added into the buffer to form the nanostructures shown in Figure 4A or 4C, respectively. The desired nanostructure was separated from the excess single strand modified AuNPs mixture in a 3% w/v agarose gel. 1 The ph-driven reconfigurations of the inter-connected circular DNA-AuNPs nanostructures were triggered by diluted acetic acid and ammonium hydroxide solution, to ph 5.0 and ph 10.0, respectively. STEM measurements The inter-connected or separated circular DNA-AuNPs nanostructures were diluted to a final concentration of 0.5 nm in the corresponding HEPES buffer solution (1 mm, ph 5.0/7.0/10.0, MgCl 2 20 mm), and deposited on the copper grids. The drop was dried in air at room temperature for two hours. Images were recorded with an Extra High Resolution Scanning Electron Microscope Magellan (TM) 400L. 6
7 Figure S1. Fluorescence intensities of AF488 (F 3 ) and AF647 (C 1 ) observed upon ph changes. I(pH 7.0) II(pH 10.0) III(pH 5.0) II(pH 10.0) III(pH 5.0) I(pH 7.0). 7
8 Figure S2. Native PAGE gels confirming the association of inter-connected circular DNA dimers at ph = 7.0 (A) and the dissociation of the inter-connected circular DNA dimers at ph = 5.0 (B) or ph = 10.0 (C). (A) Lane 1: L 1 crosslinked R 1 (rigidified by strands C 2, L 3 and F 1 ) and R 2 (rigidified by strands C 2, and F 2 ) dimers; Lane 2: R 1 (rigidified by strands C 2, L 3 and F 1 ); Lane 3: R 2 (rigidified by strands C 2, L 1 and F 2 ); Lane 4: R 2 ; Lane 5: R 1 ; Lane 6: R 2 (rigidified by strands C 2, L 2 and F 2 ); Lane 7: R 1 (rigidified by strands C 2, L 3 and F 1 ); Lane 8: L 2 crosslinked R 1 (rigidified by strands C 2 and F 1 ) and R 2 (rigidified by strands C 2 and F 2 ) dimers with the auxiliary strand L 3. (B) Lane 1: R 2 ; Lane 2: L 1 C-G C + triplex formation associated with R 2 (rigidified by strands F 2 and C 2 ); Lane 3: R 1 ; Lane 4: R 1 (rigidified by strands C 2, L 3 and F 1 ); Lane 5: L 1 C-G C + triplex formation associated with R 2 (rigidified by strands F 2 and C 2 ) leading to the separation of R 1 (rigidified by strands C 2, L 3 and F 1 ) and R 2 (rigidified by strands F 2 and C 2 ). (C) Lane 1: R 2 ; Lane 2: R 1 ; Lane 3: L 2 hybridized R 2 (rigidified by strands F 2 and C 2 ); Lane 4: R 1 (rigidified by strands C 2, L 3 and F 1 ); Lane 5: separation of interconnected dimers into R 1 (rigidified by strands C 2, L 3 and F 1 ) and R 2 (rigidified by strands L 2, F 2 and C 2 ). 8
9 Figure S3. Native PAGE gels confirming the association of inter-connected circular DNA dimers nanostrctures. Lane 1: R 2 ; Lane 2: R 1 ; Lane 3: R 1 (rigidified by strands C 2, L 3 and F 1 ); Lane 4: L 1 and L 2 hybridized R 2 (rigidified by strands C 2 and F 2 ); Lane 5: L 1 and L 2 crosslinked dimer R 1 (rigidified by strands C 2, L 3 and F 1 ) and R 2 (rigidified by strands C 2 and F 2 ). 9
10 Figure S4. Representative STEM images of the inter-connected circular DNA-AuNPs nanostructures shown in Figure 4(A). The imaged samples were purified by gel electrophoresis as described in the experimental section, Supporting Information. 10
11 Figure S5. Representative STEM images of the separated circular DNA-AuNPs nanostructures shown in Figure 4(A). 11
12 Figure S6. Representative STEM images of the inter-connected circular DNA-AuNPs nanostructures shown in Figure 4(C). 12
13 Figure S7. Representative STEM images of the separated circular DNA-AuNPs nanostructures shown in Figure 4(C). 13
14 Reference 1. Lu, C.-H.; Qi, X.-J.; Cecconello, A.; Jester, S. S.; Famulok, M.; Willner, I. Angew. Chem. Int. Ed. 2014, 53,
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