A Three-Station DNA Catenane Rotary Motor with Controlled

Apr 4, 2013 - The fabrication of DNA machines attracts extensive research efforts,1 and such molecular devices have been used for controlled synthesis...
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Letter pubs.acs.org/NanoLett

A Three-Station DNA Catenane Rotary Motor with Controlled Directionality Chun-Hua Lu,† Alessandro Cecconello,† Johann Elbaz,† Alberto Credi,‡ and Itamar Willner*,† †

Institute of Chemistry and The Minerva Center for Biohybrid Complex Systems, The Hebrew University of Jerusalem, Jerusalem 91904, Israel ‡ Photochemical Nanosciences Laboratory, Dipartimento di Chimica “G. Ciamician”, Università di Bologna, via Selmi 2, 40126 Bologna, Italy S Supporting Information *

ABSTRACT: The assembly of DNA machines represents a central effort in DNA nanotechnology. We report on the first DNA rotor system composed of a two-ring catenane. The DNA rotor ring rotates in dictated directions along a wheel, and it occupies three distinct sites. Hg2+/cysteine or pH (H+/OH−) act as fuels or antifuels in positioning the rotor ring. Analysis of the kinetics reveals directional clockwise or anticlockwise population of the target-sites (>85%), and the rotor’s direction is controlled by the shortest path on the wheel.

KEYWORDS: DNA, machine, catenane, nanotechnology, fluorescence resonance energy transfer (FRET)

T

not established. Mechanical rotation was demonstrated in synthetic, stimuli-responsive supramolecular nanostructures, either with18 or without19 directional control. Although the motion dynamics in catenane motors was never investigated, these devices represent interesting models for understanding the operation of biomolecular machines. Here we report on the development of a DNA rotary motor that exhibits dictated (clockwise or anticlockwise) mechanical motion across three states, triggered by fuel/antifuel pairs (Hg2+/cysteine or H+/ OH−), and on the time-dependent probing of the rotary motor operation. It should be noted that the dynamic rotary motions within the present two-ring catenane system differ significantly from the dynamic transitions observed in the three-ring catenane system.15 (i) In the present device, the dynamic transitions occur across three states, whereas in the three-ring catenane system the dynamic transitions proceed between two states. (ii) In the present study, H+/OH− and Hg2+/cysteine are used as fuels/antifuels, while the three-ring catenane was activated by fuel/antifuel single strands. (iii) The directional dynamic transitions in the three-ring catenane system were dictated by blocker units associated with the central ring. In contrast, in the two-ring catenane system the directional motion of the translocating ring is dictated by the shortest path to reach the next state, and blocker units associated with the “track” have only a secondary effect on the directionality. (iv)

he fabrication of DNA machines attracts extensive research efforts,1 and such molecular devices have been used for controlled synthesis,2 carrying nanocargoes,3 or DNA computing.4 Molecular DNA machines undergoing reversible B-Z DNA transitions,5 acting as “shuttles”,6 “tweezers”,7 “walkers”,8 “cranes”,9 and “metronome”10 systems, were reported in solution and on surfaces.11 The directional, mechanical operation of the machines across programmed and defined states is, however, a major challenge in this field. Directional and reversible mechanical transitions between states were demonstrated by controlling the relative stabilization energy of the “moving” elements at the different states of the machines, using appropriate “fuels” or “antifuels”. Different fuels/antifuels were applied to trigger these molecular machines, including DNA strands,12 Hg2+/cysteine,13 H+/ OH−13, light6,14 or enzymatic reactions.11 Recently, the dictated and reversible structural transitions of a three-ring catenane system across programmed topologies using DNA strands as blocker/antiblocker and fuel/antifuel units were demonstrated.15 In all of these systems, the directed mechanical motion is controlled by the energetics of the different states16 or by the introduction of steric barriers into the molecular structure. Naturally, these vectorial motions proceed on linear scaffolds, where the right/left or top/bottom motions are controlled by the relative energetics/steric constraints of the system. Various DNA-based [2]catenanes were synthesized,17 but the predetermined and controlled mechanical interconversion among different relative configurations of the two interlocked rings was © 2013 American Chemical Society

Received: March 19, 2013 Published: April 4, 2013 2303

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energetically favored duplex domain characterized by cooperative T-Hg2+-T bridges that assist base-pairing. The proximity between Cy3 and BHQ-2 leads to the effective quenching of the fluorophore, while Cy5 becomes inefficiently quenched owing to its increased spatial separation from the quencher. Treatment of state II with cysteine releases the Hg2+-ions from the duplex, thus regenerating state I with its characteristic fluorescence features. Subjecting state I to pH = 5.2 causes the release of strand (6) from the catenane in the form of the imotif structure. This process unblocks a complementary domain for ring α on ring β, resulting in the motion of ring α from site I to site III due to enhanced base-pairing stability between the two rings. In state III, the two fluorophores Cy3 and Cy5 are spatially separated from the quencher BHQ-2, leading to their inefficient quenching. By adjusting the pH of the system to 7.2, the i-motif structure is disassembled, and consequently, the strand displacement of ring α in state III by (6) regenerates state I with its characteristic fluorescence features. Similarly, treatment of state II with cysteine at pH = 5.2 yields state III, while subjecting state III to pH = 7.2, in the presence of Hg2+ ions, restores state II. Figure S3 in Supporting Information shows the fluorescence spectra of Cy3 and Cy5 in the different states, demonstrating that the fluorescence quenching of the fluorophores, indeed, probes the state of the system. It should be noted that the fluorescence of Cy3 and Cy5 is pH-insensitive in the pH = 5.2−7.2 region. Figure 2A depicts the time-dependent fluorescence intensity changes of Cy3 and Cy5 upon the cyclic transformation between states I and II through the addition of Hg2+ and cysteine, respectively. As expected, the formation of state II is accompanied by the increase in the fluorescence of Cy5 and the decrease of the fluorescence of Cy3. The opposite timedependent fluorescence changes are observed while going from state II back to state I. Similarly, Figure 2B shows the timedependent fluorescence changes of the fluorophores upon the pH-induced transition of state I to state III and back. In agreement with Figure 1B, only the fluorescence of Cy5 is enhanced upon formation of state III, and it becomes quenched again upon restoring state I. The time-dependent fluorescence intensities of Cy3 and Cy5 upon cycling between states II and III, using the respective triggering inputs, are reported in Figure 2C. As expected, the formation of state III is accompanied by an increase in the fluorescence of Cy3 with no significant change in the fluorescence of Cy5, while the regeneration of state II causes a time-dependent decrease in the fluorescence of Cy3 to its original value. Figure 3 shows that the device can perform a dictated “anticlockwise” cycle or “clockwise” cycle, where the stimuli-controlled rotation of the ring across the three states proceeds, Figure 3A and B, respectively. Evidently, the fluorescence features of the two fluorophores provide effective optical labels to probe the state of the device. Figure 3C shows anticlockwise and clockwise cycles, where the stimulicontrolled rotation of the ring across the three states proceeds. Figure S4 in Supporting Information shows the repeated twocycle rotation of the ring in consecutive anticlockwise cycles. These results indicate control over the directionality of the rotation of the DNA motor. An important aspect to consider involves the evaluation of the overall percentage of the populations of the different states upon triggering of the rotary motor with the respective fuel/ antifuel. To reach this goal, each of the states was treated with the respective fuel/antifuel and the time-dependent fluorescence changes of the respective fluorophore were monitored.

In the three-ring catenane system, the dynamic transitions proceed on the exterior of the catenated template and yield different states through “kissing” complementary interactions. In the two-ring catenane system, the transitions between all three states proceed within an interlocked configuration. Figure 1A depicts the synthesis of the two-ring DNA catenane that provides the skeleton of the DNA rotary motor.

Figure 1. (A) Synthesis of the catenated DNA molecular rotor system. (B) Reversible signal-triggered translocation of the rotor ring α across three states (I, II, and III).

The nucleic acid (1) was first mixed with the cap (2). Upon its capping and ligation, the first ring α was generated. The resulting ring was then hybridized with the nucleic acid (3) that included a hybridization domain to ring α. The nucleic acid (3) includes two internal Cy3 and Cy5 fluorophores. The threaded strand (3) was further capped with the strand cap (4), ligated and purified by gel electrophoresis to form the two-ring catenane α/β with a yield of ca. 28% (see details in the Supporting Information, Figure S1). The resulting catenane did not separate upon heating to 65 °C. The rotary motor was then constructed, and its schematic operation is shown in Figure 1B. The two-ring catenane system is stabilized in state I via interring hybridization; a nucleic acid strand modified with the BHQ-2 black hole quencher, (5), was hybridized with ring α (for the absorbance features of BHQ-2 see Figure S2). The nucleic acid (6) includes a cytosine-rich sequence and, at neutral pH, it is hybridized to a complementary domain on ring β. Since at pH 5.2 (6) is capable of generating the i-motif structure, it constitutes a pH-sensitive domain. The fluorescence resonance energy transfer (FRET) quenching of the fluorophores Cy3 and Cy5, located on ring β, by BHQ-2, located on ring α, provides the readout signals for the rotary motion of the device, which is powered by Hg2+/cysteine or pH (H+/OH−) stimuli. In state I, the Cy5 reporter is strongly quenched, whereas Cy3 is less efficiently quenched, because of its larger distance from the BHQ-2 unit. Addition of Hg2+ to state I yields state II in which the two rings are stabilized by an 2304

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Figure 2. Time-dependent fluorescence changes of the fluorophore probes Cy3 and Cy5 upon the reversible transition of the device between the states. (A) I ⇆ II using Hg2+/cysteine as triggers. (B) I ⇆ III using H+/OH− as triggers. (C) II ⇆ III using pH = 5.2 + cysteine/ pH = 7.2 + Hg2+ as triggers.

Figure 3. Time-dependent fluorescence changes upon the activation of the DNA rotor, with the respective triggers, and the cycling of the rotor across the states. (A) I → II → III → I. (B) I → III → II → I. (C) I → II → III → I → III → II → I.

Subsequently, an appropriate nucleic acid strand that displaces any residual ring α associated with the source-site was added to the system, and the additional time-dependent fluorescence changes were monitored. Assuming that the fuel/antifueltriggered processes and the subsequent strand displacement reactions lead to complete translocation (100%) of the ring α from the respective source-site to the target-site, one may calculate the percentage of the ring being translocated only by fuels/antifuels (for a specific example, see Supporting Information Figure S5). Table 1 summarizes the percentage yields of the translocated ring α from any source-site to a target-site using the respective fuel/antifuel triggers. One may realize that the ring α is almost fully translocated between the respective sites (for a detailed discussion on the design and implementation of the fuel strand sequences see Supporting Information Section IV). We then attempted to probe the relative directionality of the motion of the molecular rotor ring α on ring β. This is exemplified in Figure 4 with the analysis of the dynamic transition of ring α from site I to site II upon addition of Hg2+. Figure 4A shows that the transition of ring α from site I to II may proceed along either clockwise or anticlockwise paths. We thought that hindering any of the paths with complementary nucleic acids could dictate a directional motion of ring α to yield state II. Figure 4B implements two blocker units

anticipated to favor the anticlockwise movement, whereas Figure 4C depicts the blocker configuration that is anticipated to enhance the clockwise translocation. Preventing translocation in both directions with appropriate blocker units is schematically presented in Figure 4D and is expected, in principle, to prohibit the rotary motion of the device. Note that the blocker units are extended with single-stranded tails to increase the steric hindrance and to enhance the electrostatic repulsion between the rotating ring and the respective rotation path. Figure 4, bottom, shows the time-dependent fluorescence changes of Cy3 upon following the dynamics corresponding to the transition of state I to II in all four configurations. Several conclusions may be derived from these results. (i) Even in the presence of all blocker units, state I is transformed into state II. The final population of state II is similar to that observed in the absence of blocker units (Figure 4A). This suggests that the ring α may overcome the duplex blocker units, and it can reach the energetically stabilized site II. (ii) The rate of formation of state II is, however, strongly affected by the blocker units, and while the formation of the saturated population of state II in the absence of blockers occurred within 10 min, blocking of the clockwise motion with blockers B1 and B2 or the anticlockwise motion with blocker B3, or blocking of the device with B1 + B2 + B3, prolonged the formation time of the equilibrium population of state II to 12.0, 25.8, and 54.6 min, respectively. 2305

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Table 1. Percentage Yields of the Ring α Occupying the Respective Target-Sites upon the Application of the Respective Fuel/ Anti-Fuel Triggers translocation path

I→II

II→I

I→III

III→I

II→III

III→II

yield (%)

88 ± 4

86 ± 3

85 ± 3

91 ± 2

86 ± 3

90 ± 4

Figure 4. Time-dependent fluorescence changes of Cy3 upon transition of the device from state I to state II, where (A) the ring β does not include blockers; (B) the long path on ring β is blocked by blockers B1 and B2; (C) the short path on ring β is blocked by blocker B3; and (D) the two paths on ring β are blocked with B1, B2, and B3.

Table 2. Percentages of Ring α Translocating Across the Different Sites and Proceeding in Clockwise/Anticlockwise Directions in the Different Blocked/Unblocked Systemsa systemb

F

L

S

B

translocation path

PR1 (%)

PR2 (%)

PR1 (%)

PR3 (%)

PR2 (%)

PR4 (%)

PR3 (%)

PR4 (%)

I→II II→I I→III III→I II→III III→II

76.4 84.5 75.2 73.5 81.1 84.0

23.6 15.5 24.8 26.5 18.9 16.0

78.3 67.3 43.9 45.1 63.8 86.7

4.5 0.7 0.5 0.7 0.5 2.5

24.2 12.4 14.5 16.2 14.9 16.6

14.5 3.6 1.6 1.9 2.1 13.0

14.0 4.6 2.8 3.2 2.7 12.6

4.3 0.8 0.9 1.1 0.6 2.4

Percentages of translocated ring α from one site to another, calculated according to the procedure detailed in the Supporting Information. Percentages are calculated at a fixed time-interval corresponding to the saturated translocation (100%) of the ring α to the respective state in the unblocked system (I→II, 10 min; II→I, 3.4 min; I→III, 2.0 min; III→I, 2.2 min; II→III, 1.8 min; III→II, 10.0 min). bF corresponds to the unblocked system; L corresponds to the long path blocked system; S corresponds to the short path blocked system; B corresponds to the long and short paths blocked system. a

fractions of the states generated by transition across all possible paths can be calculated, and the obtained values are reported in Table 2 (see detailed explanations in the Supporting Information ). For example, for the transition of the state I to state II, in the unblocked structure 76.4% of state II is generated by the motion of ring α across the anticlockwise path (PR1), while 23.6% of state II is formed by moving ring α across the clockwise path (PR2). In the presence of the blockers B1 and B2, 78.3% of state II is generated by the anticlockwise direction, whereas the formation of state II by translocating ring α across the blocked path is only 4.5%. Note that these fractions of state II are generated at the same time interval of 10 min, where the population of state II in the unblocked configuration reaches the saturation value of 100%. That is, blocking the device by B1 + B2 allowed the population of only 82.8% of state II on this time scale, mostly through moving ring α in the anticlockwise direction. Also, we note that for the device blocked by all three

Analyses similar to those shown in Figure 4 were performed for the reverse transformation of state II to I, as well as to the other possible transitions (state I ⇆ state III; state II ⇆ state III). The time-intervals required to generate the equilibrium population of the different states are summarized in Supporting Information Table S3. While the key conclusions summarized above in (i) and (ii) are valid, the specific time-intervals to generate the states differ and are characteristic to the specific transitions across the states. The final populations of states I, II, III are identical without the blocker or with the blocker systems and differ only in the rates of formation. This allows us to define the rates for the transitions between the states. For example, for the transition of state I to state II, in the presence of Hg2+ ions, the rates are R1, R2, R3, and R4 (Figure 4, see detailed explanations in the Supporting Information ). Since the time-intervals for the generation of the different states (in the different unblocked/blocked configurations) are known, the 2306

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ACKNOWLEDGMENTS Parts of this research were supported by the Israel Science Foundation, the EU MULTI project, and the Volkswagen Foundation.

blockers only a population of 18.3% in state II is formed on the time scale of 10 min, a value that is substantially lower than in the systems where only one path is blocked. Table 2 summarizes the fractions of populations that generate the different states in clockwise or anti-clockwise directions in the absence of the blocker or the presence of the blocker(s). Several important conclusions may be extracted from Table 2. (i) Upon triggering the translocation of the rotor to a specific state, the rotor “selects” the shortest path, clockwise or anticlockwise, to reach the state. Although this conclusion is intuitively reasonable, the quantitative analysis was feasible only upon analyzing the more complicated blocked systems. Nonetheless, the preference of the moving path is not precisely dictated by the relative lengths of the paths (the movement along the short path is overexpressed). Although the origin for this effect is at present unknown, electrostatic repulsive interactions along the long path might further inhibit the movement. (ii) By the selection of appropriate sets of inputs, the dictated, autonomous, enriched rotation of the rotor proceeds in clockwise or anticlockwise directions. The direction of rotation of the DNA rotor can be reversed at any state, by the introduction of appropriate trigger inputs. (iii) The hybridization of blocker units to the different rotating paths decreases the probabilities for translocation of the rotary motor through the blocked domains. Specifically, the hybridization of the blocker units to the longer paths enhances the selectivity for motion of the rotor along the dictated short path. For example, upon the Hg2+-triggered transition of the rotor from state I to II, 78.3% of the rotor moves across the short path and only 4.5% moves along the long path within the time-scale of 40 min (as compared to 76.4%:23.6% in the unblocked configuration). Similarly, triggering the reverse transition from state II to state I using cysteine leads to a 67.3%:0.7% transition along the short and long blocked paths (while the ratio in the unblocked system is 84.5%:15.5%). To conclude, the present study has introduced a three-state rotary motor that is triggered by Hg2+/cysteine and H+/OH− stimuli. The device exhibits dictated directional rotation and revealed reversible clockwise and anticlockwise rotation functions. The distinct states of the devices and the ability to probe the dynamics of motion enabled us to elucidate the composition of the system at each time interval. This establishes a finite-state logic device for multilevel parallel computing.

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REFERENCES

(1) (a) Bath, J.; Turberfield, A. J. Nat. Nanotechnol. 2007, 2, 275− 284. (b) Krishnan, Y.; Simmel, F. C. Angew. Chem., Int. Ed. 2011, 50, 3124−3156. (c) Beissenhirtz, M. K.; Willner, I. Org. Biomol. Chem. 2006, 4, 3392−3401. (2) (a) Gu, H.; Chao, J.; Xiao, S. J.; Seeman, N. C. Nature 2010, 465, 202−206. (b) Milnes, P. J.; McKee, M. L.; Bath, J.; Song, L.; Stulz, E.; Turberfield, A. J.; O’Reilly, R. K. Chem. Commun. 2012, 48, 5614− 5616. (c) McKee, M. L.; Milnes, P. J.; Stulz, J. E.; O’Reilly, R. K.; Turberfield, A. J. J. Am. Chem. Soc. 2012, 134, 1446−1449. (3) (a) Fu, J.; Yan, H. Nat. Biotechnol. 2012, 30, 407−408. (b) Muscat, R. A.; Bath, J.; Turberfield, A. J. Nano Lett. 2011, 11, 982−987. (c) Lund, K.; Manzo, A. J.; Dabby, N.; Michelotti, N.; Johnson-Buck, A.; Nangreave, J.; Taylor, S.; Pei, R.; Stojanovic, M. N.; Walter, N. G.; Winfree, E.; Yan, H. Nature 2010, 465, 206−210. (d) Lo, P. K.; Karam, P.; Aldaye, F. A.; McLaughlin, C. K.; Hamblin, G. D.; Cosa, G.; Sleiman, H. F. Nature Chem. 2010, 2, 319−328. (4) (a) Seelig, G.; Soloveichik, D.; Zhang, D. Y.; Winfree, E. Science 2006, 314, 1585−1588. (b) Elbaz, J.; Lioubashevski, O.; Wang, F.; Remacle, F.; Levine, R. D.; Willner, I. Nat. Nanotechnol. 2010, 5, 417− 422. (5) (a) Mao, C.; Sun, W.; Shen, Z.; Seeman, N. C. Nature 1999, 397, 144−146. (b) Rajendran, A.; Endo, M.; Hidaka, K.; Sugiyama, H. J. Am. Chem. Soc. 2013, 135, 1117−1123. (6) Lohmann, F.; Ackermann, D.; Famulok, M. J. Am. Chem. Soc. 2012, 134, 11884−11887. (7) (a) Yurke, B.; Turberfield, A. J.; Mills, A. P., Jr; Simmel, F. C.; Neumann, J. L. Nature 2000, 406, 605−608. (b) Elbaz, J.; Moshe, M.; Willner, I. Angew. Chem., Int. Ed. 2009, 48, 3834−3837. (8) (a) Shin, J. S.; Pierce, N. A. J. Am. Chem. Soc. 2004, 126, 10834− 10835. (b) Omabegho, T.; Sha, R.; Seeman, N. C. Science 2009, 324, 67−71. (c) Wang, C.; Ren, J.; Qu, X. Chem. Commun. 2010, 47, 1428− 1430. (d) Wang, Z. G.; Elbaz, J.; Willner, I. Nano Lett. 2011, 11, 304− 309. (9) Wang, Z. G.; Elbaz, J.; Willner, I. Angew. Chem., Int. Ed. 2012, 51, 4322−4326. (10) Buranachai, C.; McKinney, S.; Ha, T. Nano Lett. 2006, 6, 496− 500. (11) Elbaz, J.; Tel-Vered, R.; Freeman, R.; Yildiz, H. B.; Willner, I. Angew. Chem., Int. Ed. 2008, 48, 133−137. (12) (a) Yin, P.; Choi, H. M. T.; Calvert, C. R.; Pierce, N. A. Nature 2008, 451, 318−322. (b) Zhang, D. Y.; Seelig, G. Nature Chem. 2011, 3, 103−113. (13) Wang, Z. G.; Elbaz, J.; Remacle, F.; Levine, R. D.; Willner, I. Proc. Nat. Acad. Sci. U.S.A. 2010, 107, 21996−22001. (14) (a) You, M.; Chen, Y.; Zhang, X.; Liu, H.; Wang, R.; Wang, K.; Williams, K. R.; Tan, W. Angew. Chem., Int. Ed. 2012, 51, 2457−2460. (b) Kang, H.; Liu, H.; Phillips, J. A.; Cao, Z.; Kim, Y.; Chen, Y.; Yang, Z.; Li, J.; Tan, W. Nano Lett. 2009, 9, 2690−2696. (c) Zhou, M.; Liang, X.; Mochizuki, T.; Asanuma, H. Angew. Chem., Int. Ed. 2010, 49, 2167−2170. (15) Elbaz, J.; Wang, Z. G.; Wang, F.; Willner, I. Angew. Chem., Int. Ed. 2012, 51, 2349−2353. (16) Qian, L.; Winfree, E. Science 2011, 332, 1196−1201. (17) (a) Liu, Y.; Kuzuya, A.; Sha, R.; Guillaume, J.; Wang, R.; Canary, J. W.; Seeman, N. C. J. Am. Chem. Soc. 2008, 130, 10882−10883. (b) Han, D.; Pal, S.; Liu, Y.; Yan, H. Nat. Nanotechnol 2010, 5, 712− 717. (c) Schmidt, T. L.; Heckel, A. Nano Lett. 2011, 11, 1739−1742. (d) Olson, M. A.; Braunschweig, A. B.; Fang, L.; Ikeda, T.; Klajn, R.; Trabolsi, A.; Mirkin, C. A.; Gryzbowski, B. A.; Stoddart, J. F. Angew. Chem., Int. Ed. 2009, 48, 1792−1797. (18) (a) Leigh, D. A.; Wong, J. K. Y.; Dehez, F.; Zerbetto, F. Nature 2003, 424, 174−179. (b) Hernandez, J. V.; Kay, E. R.; Leigh, D. A.

ASSOCIATED CONTENT

S Supporting Information *

Experimental section, gel electrophoresis analysis, repeated two-cycle rotation of the ring in consecutive anticlockwise cycles, evaluation of the percentage yield of the translocation of the rotary motor from a source-site to a target-site, evaluating the percentages of ring α translocating across the different sites in the clockwise/anticlockwise rotation. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected].. Tel: 972-2-6585272. Fax: 9722-6527715. Notes

The authors declare no competing financial interest. 2307

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Science 2004, 306, 1532−1537. (c) Ruangsupapichat, N.; Pollard, M. M.; Harutyunyan, S. Z.; Feringa, B. L. Nature Chem 2011, 3, 53−60. (19) (a) Livoreil, A.; Dietrich-Buchecker, C.; Sauvage, J. P. J. Am. Chem. Soc. 1994, 116, 9399−9400. (b) Asakawa, M.; Ashton, P. R.; Balzani, V.; Credi, A.; Hamers, C.; Mattersteig, G.; Montalti, M.; Shipway, A. N.; Spencer, N.; Stoddart, J. F.; Tolley, M. S.; Venturi, M.; White, A. J. P.; Williams, D. J. Angew. Chem., Int. Ed. 1998, 37, 333− 337. (c) Ashton, P. R.; Baldoni, V.; Balzani, V.; Credi, A.; Hoffmann, H. D. A.; Martinez-Diaz, M. V.; Raymo, F. M.; Stoddart, J. F.; Venturi, M. Chem.Eur. J. 2001, 7, 3482−3493. (d) Cao, D.; Amelia, M.; Klivansky, L. M.; Koshkakaryan, G.; Khan, S. I.; Semeraro, M.; Venturi, M.; Credi, A.; Liu, Y. J. Am. Chem. Soc. 2010, 132, 1110−1122. (e) Leontiev, A. V.; Serpell, C. J.; White, N. G.; Beer, P. D. Chem. Sci. 2011, 2, 922−927. (f) Fang, L.; Wang, C.; Fahrenbach, A. C.; Trabolsi, A.; Botros, Y. Y.; Stoddart, J. F. Angew. Chem., Int. Ed. 2011, 50, 1805− 1809. (g) Zhu, L. L.; Li, X.; Ji, F. Y.; Ma, X.; Wang, Q. C.; Tian, H. Langmuir 2009, 25, 3482−3486.

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