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Peptide-Metal Organic Framework (P-MOF) Swimmers that Direct the Motion toward Chemical Targets Yasuhiro Ikezoe, Justin Fang, Tomasz L Wasik, Menglu Shi, Takashi Uemura, Susumu Kitagawa, and Hiroshi Matsui Nano Lett., Just Accepted Manuscript • DOI: 10.1021/acs.nanolett.5b00969 • Publication Date (Web): 26 May 2015 Downloaded from http://pubs.acs.org on May 31, 2015

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Peptide-Metal Organic Framework (P-MOF) Swimmers that Direct the Motion toward Chemical Targets Yasuhiro Ikezoe,a Justin Fang,a Tomasz L. Wasik,a Menglu Shi,a Takashi Uemura,c,d Susumu Kitagawa,c,e Hiroshi Matsui a,b* a

Department of Chemistry and Biochemistry, Hunter College and Graduate Center of the City University of New York, New York, NY 10065 b

Department of Biochemistry, Weill Medical College of Cornell University , 413 E69th street, New York, NY 10021 c

Department of Synthetic Chemistry and Biological Chemistry, Kyoto University, Katsura, Nishikyo-ku, 615-8510, Kyoto (Japan). d

CREST, Japan Science and Technology Agency (JST), 4-1-8 Honcho, Kawaguchi, Saitama 332-0012, Japan e

Institute for Integrated Cell-Material Sciences (iCeMS), Kyoto University, Yoshida, Sakyo-ku, Kyoto 606-8501 (Japan) * to whom correspondence should be sent. E-mail: [email protected] KEYWORDS: Swimmers, Motors, Biomimetics, Directed Motion, Peptide Assembly, Metalorganic framework (MOF).

ABSTRACT: Highly efficient and robust chemical motors are expected for the application in microbots that can selectively swim toward targets and accomplish their tasks in sensing, labeling, and delivering. However, one of major issues for such development is that current

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artificial swimmers have difficulty controlling their directional motion toward targets like bacterial chemotaxis. To program synthetic motors with sensing capability for the target-directed motion, we need to develop swimmers whose motions are sensitive to chemical gradients in environments. Here we create a new intelligent biochemical swimmer by integrating metal organic frameworks (MOFs) and peptides that can sense toxic heavy metals in solution and swim toward the targets. With the aid of Pb-binding enzymes, the peptide-MOF motor can directionally swim toward PbSe quantum dots (QD) by sensing pH gradient and eventually complete the motion as the swimmer reaches the highest gradient point at the target position in solution. This type of technology could be evolved to miniaturize chemical robotic systems that sense target chemicals and swim toward target locations.

TEXT: Micromotors have been attracting attentions from broad science communities in both fundamental and practical interests.1-4 For example, in protein synthesis, DNA replication, ATP synthesis, and cell motility, micromotors support these functions as a vital engine.1 Various chemical motors have been produced such as self-propelling swimmers (in solutions) 5-15and walkers (on substrates).16-18 The artificial walkers consisting of DNA and microtubule systems were demonstrated to be guided to specific locations along tracks pre-patterned on substrates and capture targets without sensing.19-22 Thus, these chemical walkers are limited to capture targets only when targets are deposited on the track of guided motion, which is not a practical condition for the detection of target molecules in unknown locations. Ideal chemical motors can freely move in solution and then sense and directionally swim toward targets.23 The chemical


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swimmers are mainly powered by surface tension gradients generated via the creation of two different domains around swimmers so that the motion is directed toward high surface tension side, as known as Marangoni effect.8 While these swimmers are robust to generate the motion in solution, most of artificial swimmers are still limited to move in one direction and their motion is not directed to the targets.24 Some of bimetallic nanorod motors are reported to recognize one another with the electrostatic interaction, however the swimming pathway is not directed by the interaction and the binding event requires the collision between nanorods.25 In nature, biological motors convert chemical free energy to mechanical power directly by creating isothermal and non-equilibrium conditions through biochemical reactions such as the metabolism of chemicals by cells to produce products that are simultaneously exploited as energy resources.7, 8, 26 For example, bacteria use transmembrane receptors to bind targets and control their directional motion by sensing the chemical gradient.27 Because bacteria swim toward the higher gradient, the direction of motion can be corrected to capture the target. Biomimetic swimmers could be designed if artificial motors create the non-equilibrium condition by releasing molecules to the interface and transfer this chemical change to the energy, and then the directional motion toward targets is accomplished by the chemical gradient of target in solution. Here we developed a new hybrid peptide-metal organic framework (MOF) motor system that can create motion by releasing diphenylalanine (DPA) peptides from highly organized pores and swim toward PbSe QDs as a target. The reconfiguration of peptide selfassembly at the MOF-water interface is a driving force for the motion by creating the surface tension gradient via the asymmetric hydrophobic domain distribution around MOFs.12 The sensing and directional motion of the peptide-MOF motor is programmed by the pH-sensitive assembly of DPA peptide; the pH gradient around targets generated by Pb-binding enzymes


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disassembles peptides on the MOF when the peptide-MOF motor moves across this targeted area. Then, the motion of MOF motor is slowed as the MOF moves closer to the area and eventually it stops at the highly Pb-concentrated location. This peptide-MOF motor system is one of the fine mimetic examples of chemotaxis that can direct the motion by sensing the location of target.28, 29 In this work, a MOF of CuJAST-1 ([Cu2L2ted]n where L is 1,4-benzenedicarboxylate) is used as a model motor system.12 This MOF is an excellent storage for the peptide fuel because of its function to assemble small molecules in highly ordered pore array of coordination framework and to release guest molecules in more isotropic direction.30-34 The robust self-assembling nature of DPA peptide35-44 is an important feature as a guest molecule to power the MOF motor because the re-assembly of released hydrophobic DPA peptides at the edge of MOF induces the asymmetric surface tension distribution to trigger the motion toward high surface tension side (left in Figure 1-(a)).8 While the DPA-CuJAST-1 motor can move in a radial direction, this swimmer is not designed suitably to control the direction of motion and thus it is difficult to redirect their motion toward certain targets. Chemotaxis systems in nature sense chemical gradients of environment and swim toward the highest spots. To mimic these systems, we need to reprogram the DPA-CuJAST-1 motor system to sense and stop their motion at the highest chemical gradient point. To accomplish this task, we designed a model system of the peptideMOF motor that senses and moves onto the location of PbSe QDs in solution by introducing Pbbinding enzymes for selectively generating the highest gradient around the targets. PbSe QDs are selected as a model target because they are stable in aqueous solutions and straightforward to synthesize in high volumes for the proposed experimental setup. In this system, peptide-MOF motors can swim toward the highest pH gradient (upper right in Figure 1-(a), high pH area is


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shown in a blue cloud) because DPAs are least soluble at pH 5 and increase the solubility toward the basic condition. (also see Movie #1 in Supplementary Information). The motion of MOF motor is triggered by partial dissolution of MOF at the interface with EDTA, where DPA is emitted slowly and continuously in a constant rate from inside pores of MOF. The MOF particle consists of multiple crystalline domains, however the partial destruction of MOF creates the releasing path of DPA and thus the point of DPA emission is localized on the MOF.12 Between pH 4 and pH 8, the solubility of DPA is the lowest at pH 4 and it increases as pH becomes higher. As the solubility of DPA is increased with higher pH, the lifetime of motion of DPAMOF motor becomes shorter due to the depletion of DPA domain on the MOF (Fig. S-1). After the completion of motion, the surface tension of solution decreases due to the release of DPAs to the water interface (details in Supplementary Information), leading to the loss of surface gradient and thus terminating the MOF motion. These results support the proposed motion mechanism that the motion of MOF is dependent on the assembled domain of DPA released from MOF, sensitive to pH, and the dissolution leads to terminate the MOF motion. To generate the pH gradient around the target of PbSe QDs, enzyme urease is conjugated with a Pb-binding peptide of DHHTQQHD45 so that the enzyme can selectively bind PbSe QDs (step (i) in Figure 1-(b)) to produce NH3 around the targeted area for the generation of pH gradient (step (ii) in Figure 1-(b)). PbSe QDs are also advantageous as targets because the peptide sequence for the high affinity with Pb is well established (see Fig. S-2 in Supplementary Information for the detailed structural analysis of PbSe QD target). After the disassembly of DPA peptides at the tip of MOF takes place in the basic area of solution, the peptide-MOF motors complete their motion near the target (step (iii) -> (iv) in Figure 1-(b)).


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Before examining the proposed directional motion control protocol in Figure 1, we studied the motion of DPA-CuJAST-1 motor in an EDTA solution where a basic post (pH = 8) and an acidic post (pH = 4) are contained. As shown in Figure 2, in the beginning the peptide-MOF motor was moving freely, however after 30 seconds the motor swam more closely around the basic post. After 35 seconds, the motion was completed on the top of base post (also see the Movie #2 in Supplementary Information). This result demonstrates that the motion of the DPA peptide-MOF motor system is directed toward the targeted area of high pH gradient. Interestingly, the direction of rotation is rarely changed in Movie #2, indicating that the release of peptides occurs preferentially in one direction around the MOF. The unidirectionality of swimming motion supports our hypothesis that first area on the MOF where the framework is destructed by EDTA seems to cascade the DPA emission in one direction. The velocity of MOF motor is independent of the diameter of MOF particle (Fig. S-3 in Supplementary Information), and the size of container for the swimmer also seems to have a relatively small effect on the velocity of DPAMOF (details in Supplementary Information). When the conversion efficiency of chemical energy to kinetic energy in the swimming motion is estimated from the chemical energy required for DPA peptide assembly via intermolecular hydrophobic interaction between aromatic rings of DPA and the kinetic energy consumed as frictional loss of the moving peptide-MOF particle at the water surface, the energy conversion efficiency is calculated as 1.5% (details in Supporting Information), which is 2 to 7 orders of magnitude higher than other synthetic motor systems but an order of magnitude lower than highly optimized natural biological motors such as myosins and kinesins.46-48 For the creation of basic environment around the target of PbSe QDs as illustrated in the step (ii) of Figure 1-(b), enzyme urease is applied because it can produce the basic environment as


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urea is incubated. To bind urease selectively to PbSe QDs, N-terminus of the Pb-binding peptide (DHHTQQHD) was conjugated at SH group of urease by a standard crosslinking agent (Thermo Scientific Inc., Sulfo-SMCC). As shown in Figure 3-(b), the area around the post where PbSe QDs were deposited has high contrast of a pink indicator after the Pb-binding urease and urea were incubated. The comparison between Figures 3-(a) and (b) clearly indicates that urease is attached to Pb and produces NH3 to build the highest pH gradient point around the PbSe area as urea is added. It is interesting that when the acidic post was replaced by a neat agarose gel post, the indicator was quickly diffused as shown in Figure 3-(c). Thus, to localize the basic pH gradient around the target of PbSe for the directed swimming of peptide-MOF motor, the acid post is necessary in the container. This result also indicates that Pb ions do not significantly poison the catalytic activity of urease49 and NH3 is certainly produced enough to create the pH gradient. Under the same configuration, the peptide-MOF motor was examined to swim and sense the location of PbSe QDs, as proposed in Figure 1 and Movie #1. After Pb-binding urease was incubated in solution containing the PbSe post in the petri dish for 2 minutes, sufficient to bind urease with Pb on the post, the peptide-MOF motor was dropped onto the solution. Urea was premixed with solution before mixing urease. Initially the peptide-MOF motor was moved in one direction (left in Figure 4 and Movie #3 in Supplementary Information), and then it started swimming directionally toward the target area of PbSe QDs after 15 seconds. Finally, after 20 seconds, the peptide-MOF motor completes the motion on the PbSe QDs (center in Figure 4, Movie #3 in Supplementary Information). It was also observed that this motion is controlled by the pH gradient as the targeted swimming is directed toward the high pH area around the PbSe QD post marked by the pink indicator (Movie #4).


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In conclusion, this new peptide-MOF motors could sense the location of PbSe targets and swim toward them with the aid of Pb-binding urease. The pH gradient created around the targets with the urease guides the motion of peptide-MOF motors and the chemical motor completes the movement as they reach to the targets. Such behavior resembles the movement of living organisms toward a chemical attractant. The chemotactic motor translating the chemical power of nanoscale self-assembly into the motion of macroscopic objects in a millimeter scale with high velocity over distance of several centimeters is an interesting system. In future, it is desirable to program peptide-MOF motor systems for directly sensing concentration gradient of chemicals like chemotaxis.


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Figure 1. (a) Design of the peptide-MOF motor to swim toward high pHs. (left) The robust reassembly of released hydrophobic DPA peptides at the edge of MOF creates the asymmetric surface tension distribution that can power the motion toward high surface tension side. (right) The change of pH gradient in environment triggers the completion of motion because higher pH condition disassembles DPA peptides on the MOF. (b) Scheme of directed motion of peptideMOF motors by sensing Pb with the aid of Pb-binding enzymes. After urease-conjugated Pbbinding DHHTQQHD are dropped in the solution, urease is bound to PbSe QDs (step (i)). Urea in the solution generates NH3 around the target (step (ii)), and then the dropped peptide-MOF motor starts swimming (step (iii)). After the motion is directed toward Pb target, the movement is completed at the target due to high pH gradient (step (iv)). See Movie #1 that animates this process.


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Figure 2. Optical snap shots of motion of peptide-MOF motor swimming in a solution where a basic post (pH = 8, left) and an acidic post (pH = 4, right) are contained. At first the peptideMOF motor is swimming around solution (left), and after 30 seconds the peptide-MOF motor senses the basic post and stays around the high pH area. The solution is adjusted as pH = 5 by mixing EDTA (1 mM) and NaOH (2 mM), yielding the environment for the best mobility of the peptide-MOF motor at pH 5. The right figure shows 3D trajectory of MOF motion with time. See Movie #2 for the complete motion of directed swimming toward the target.


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Figure 3. Optical images of (a) a container with a PbSe post after urea and basic pH color indicator are incubated, (b) a container with PbSe and acidic posts after Pb-binding urease, urea, and basic pH color indicator are incubated, (c) a container with only PbSe post after Pb-binding urease, urea, and basic pH color indicator are incubated. The pink color distributions show the area of basic pHs in solution.

Figure 4. Optical snap shots of motion of peptide-MOF motor swimming in a solution where a PdSe QD-deposited post (left) and an acidic post (right) are contained. The peptide-MOF motor moves freely in the first 15 seconds, and after 15 seconds the peptide-MOF motor swims more closely around the PbSe area. After 20 seconds, the directed motion of peptide-MOF motor is completed on the PbSe QD post (dark spots on the left post are QDs deposited on an agarose gel post). The acidic post to the right is at pH 4. The right figure shows 3D trajectory of MOF motion with time. See Movie #3 for the complete motion of directed swimming toward the target.


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ASSOCIATED CONTENT Supporting Information. Experimentals, Motion study of DPA-MOF motor in various pHs, TEM image of PbSe QDs, Velocity study of MOF motor in different sizes, Surface tension of solution, Energy conversion efficiency in the swimming motion of P-MOFs, movie #1 (animation of directed motion scheme), movie #2 (targeted motion of P-MOF toward high pH), movie #3 (targeted motion of P-MOF toward the PbSe QD post), movie #4 (targeted motion of P-MOF toward the PbSe QD post with a pH indicator in solution). These materials are available free of charge via the Internet at http://pubs.acs.org.” AUTHOR INFORMATION Corresponding Author Hiroshi Matsui a,b* Present Addresses a

Department of Chemistry and Biochemistry, Hunter College and Graduate Center of the City University of New York, New York, NY 10065 b

Department of Biochemistry, Weill Medical College of Cornell University , 413 E69th street, New York, NY 10021 Author Contributions The manuscript was written through contributions of all authors. Funding Sources The U.S. Department of Energy (DOE), The National Institute on Minority Health and Health Disparities (NIMHD) of the National Institutes of Health (NIH), The National Science Foundation (NSF).


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ACKNOWLEDGMENT All of works except MOF synthesis and analysis were supported by the U.S. Department of Energy, Office of Basic Energy Sciences, Division of Materials Sciences and Engineering under Award No. DE-FG-02-01ER45935. Hunter College infrastructure is supported by the National Institute on Minority Health and Health Disparities (NIMHD) of the National Institutes of Health (NIH) (MD007599). JF is supported by NSF-IGERT traineeship (DGS 0965983 at Hunter College). Chemical syntheses of MOFs, peptide incorporation study in MOFs, and structural analysis of peptide-MOF complexes in Kyoto were supported by Grant-in-Aids for challenging Exploratory Research and Scientific Research on Innovative Area “New Polymeric Materials Based on Element-Blocks” from MEXT. The authors declare no competing financial interest.

ABBREVIATIONS MOF, metal organic framework; peptide-MOF, P-MOF; QD, quantum dot; DPA, diphenylalanine, TEM, transmission electron microscope; EDTA, ethylenediaminetetraacetic acid.


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