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Transparent Protein Microtubule Motors with Controllable Velocity and Biodegradability Natsuho Sugai, Yoko Nakai, Yoshitsugu Morita, and Teruyuki Komatsu ACS Appl. Nano Mater., Just Accepted Manuscript • DOI: 10.1021/acsanm.8b00791 • Publication Date (Web): 11 Jun 2018 Downloaded from http://pubs.acs.org on June 12, 2018

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ACS Applied Nano Materials

Transparent Protein Microtubule Motors with Controllable Velocity and Biodegradability Natsuho Sugai,† Yoko Nakai,† Yoshitsugu Mororita,† and Teruyuki Komatsu*,†

†

Department of Applied Chemistry, Faculty of Science and Engineering, Chuo University, 1-1327 Kasuga, Bunkyo-ku, Tokyo 112-8551, Japan

Corresponding author: Prof. Teruyuki Komatsu Tel & Fax: +81-3-3817-1910, E-mail: [email protected]

ACS Paragon Plus Environment

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ABSTRACT: Slender protein microtube motors with a catalase interior surface are selfpropelled in aqueous H2O2 by jetting O2 microbubbles from the open-end terminus. The immobilization of catalase biocatalyst on the internal wall is achieved using avidin–biotin complexation. It is particularly interesting that the migration of O2 bubbles in the 1D-channel and their subsequent expulsions were clearly visible because the tube walls are transparent. The microtube motor velocity reached maximum at the optimum pH and temperature of the catalase. Furthermore, the microtubes were digested completely by proteases, showing sufficient biodegradability.

KEYWORDS: autonomous propulsion, avidin–biotin interaction, catalase, enzyme activity, layer-by-layer assembly


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Considerable interest has arisen recently in self-propelled microtube motors1–10 because of their potential applications as bacterium/cell removers,4,5 pollutant cleaners,6 separation devices,1,7–9 and analytical sensors.10 The propulsion is typically O2 microbubble ejection from the open-end terminus. Most microtubes comprise solid polymer-based and metal-based pipes with a Pt interior surface, where the O2 microbubbles are generated by the disproportionation of H2O2 fuel (2H2O2 → 2H2O + O2↑). Therefore, the fabrication processes of such hollow architectures must involve electrochemical deposition or magnetron sputtering of Pt. The obtained tubes are normally short and thick with a low aspect ratio of 2–4.2,3,5,6,8 Moreover, they are impenetrable to light. For those reasons, little information is available about bubble migration behavior in the tube. Wet template-synthesis using alternate layer-by-layer (LbL) assembly of biologically active proteins into the track-etched polycarbonate (PC) membrane is a beneficial technique to prepare smart nano/microtubes.11–16 We demonstrated earlier that various hollow cylinders made of protein multilayers exhibit versatile biofunctionalities, such as virus trapping,17,18 E. coli capture,19 and enzymatic polymerization.20 Furthermore, the deposition of Pt nanoparticle (PtNP) on the last layer of the cylindrical wall yielded protein–PtNP microtubes with autonomous propulsion.21 Hybrid microtubes, however, do not have sufficient biodegradability, which is the most important feature for biomedical applications. Recently, several research groups have reported biodegradable polymer-based and zinc-based motors with good biofriendly nature.22–26 Catalase (Cat, Mw: 240 kDa, pI: 5.5) is a common hemoprotein enzyme capable of decomposing H2O2 with high efficiency in antioxidant defense systems. Several successful achievements related to catalase-powered polymer/metal microtubes have been reported,27–30 although they still show poor biocompatibility. The obtained hollow cylinders can possess both self-propulsion capability and biocompatibility if one were able to immobilize Cat biocatalyst on the inner


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surface of the protein microtubes. He et al. synthesized unique protein microrockets incorporating gelatin hydrogel with Cat.31 Diffusion of H2O2 into the hydrogel engenders production of O2 bubbles to swim. Nevertheless, the conical rockets (5-µm outer diameter, 10µm length) display a limited lifetime for bubble propulsion at high concentration peroxide media. Here, we report the synthesis of slender protein microtube motors (outer diameter, 1.2 µm; aspect ratio, 20) comprising human serum albumin (HSA) as a wall material and Cat as an interior surface, and their controllable velocity of autonomous movement in water. Stable generation, migration, and expulsion of O2 bubbles were readily observable using optical microscopy because the tube walls are transparent. Moreover, perfect biodegradability of the microtubes is highlighted. An initial attempt to prepare the designed protein microtubules by electrostatic LbL build-up assembly14 using aqueous Cat solution unfortunately failed. We obtained hollow cylinders, but the Cat internal walls were denatured during the PC membrane dissolution process. The tubes did not swim at all in aqueous H2O2. Therefore, we used the avidin–biotin interaction. The avidin (Avi, Mw: 68 kDa, pI: 10.0–10.5) can bind four biotins with high specificity and degree of affinity (K > 1015 M-1). First, biotinylated catalase (bCat) was synthesized using a succinimidylarmed biotin reagent. The average number of biotin groups per Cat was determined as approximately 9.32 The H2O2 disproportionation capability of the enzyme remains unaltered after the biotin conjugation. Next, the HSA-based microtubes with an Avi interior surface, the precursor microtubes, were fabricated using template-assisted LbL assembly with microporous PC membrane (pore size: 1.2 µm). The positively charged poly-L-arginine (PLA) and negatively charged poly-L(glutamic acid) (PLG) were used as electrostatic glue. The obtained template membrane


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involving multilayers was immersed into N,N-dimethylformamide solution to dissolve the PC framework. The released microtubes were subsequently freeze-dried, yielding lyophilized powder of (PLA/HSA)7PLA/PLG/Avi microtubes (Avi microtubes). SEM images clearly showed the formation of uniform hollow cylinders with 1.16 ± 0.05 µm outer diameter and 146 ± 8 nm wall thickness (Figures 1A and 1B). The maximum length of the tubes (23.7 ± 0.7 µm) coincided well with the pore-depth of the PC template used. The aspect ratio of the Avi microtube is 20, signifying high inner pore surface area compared to same-diameter microtubes with a low aspect ratio. We proposed a 17-layer model in which the last Avi layer binds to the oppositely charged PLG layer with single-particle thickness. If we hypothesized that the dimensions of PLA, PLG, HSA, and Avi are, respectively, 8.7, 11.0, 8.0, and 6.0 nm from our previously reported results,14,15,21 then the total tube wall thickness is estimated as 143 nm (Figure 1C). This value is close to the observed width of the cylindrical wall. Low-cycle filtration was insufficient to obtain stable microtubes with good mechanical properties. For example, thin 11-layered microtubes were very fragile. The lyophilized powder of Avi microtubes was suspended in sodium phosphate buffered saline (PBS) solution (pH 7.4, +154 mM NaCl).33 Thereafter, bCat was added to the dispersion. Removing the unbound

bCat

by centrifugation

(1,500

× g,

10

min) conferred

(PLA/HSA)7PLA/PLG/Avi/bCat microtubes (Avi-bCat microtubes) as a precipitate. Later, the tubes were resuspended into the PB solution (pH 7.0). TEM measurements of the air-dried sample of the aqueous dispersion revealed that the microtubes swelled considerably in water. The wall thickness became 298 nm, although the outer diameter was unchanged (Figure 1D). Results show that the inner pore diameter diminished to ca. 560 nm. Under the assumption that the protein sizes are constant, the thickness of each polypeptide (PLA or PLG) layer might be 25


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nm, which is apparently greater than that of the dried state. We ascertained the swelling ratio of the polypeptide layer (αp) to be 2.4 (see Supporting Information). This value is almost equal to data reported in the literatures for general polyelectrolytes (1.2−4.0).34,35

Figure 1. (A, B) SEM images of slender Avi microtubes prepared using a 1.2 µm porous PC template (24 µm pore depth). The lyophilized powder comprises highly oriented microtubes. (C) Schematic illustration of 17-layer wall in Avi microtube. (D) TEM image of Avi-bCat microtube without staining. (E) CLSM image of Avi-FbCat microtube (excited at 488 nm).

To demonstrate the immobilization of bCat at the internal wall, we exploited fluoresceinlabeled bCat (FbCat) as well. Confocal laser scanning microscopy (CLSM) images of


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(PLA/HSA)7PLA/PLG/Avi/FbCat

microtubes

(Avi-FbCat

microtubes)

showed

strong

fluorescence, indicating that the FbCat molecules are accommodated in the tube (Figure 1E). We inferred that the homogeneous immobilization of bCat on the internal wall was accomplished by avidin–biotin linkage. Upon addition of H2O2 into the aliquot of the microtube dispersion, the tubes were immediately self-propelled by jetting O2 bubbles from the terminal opening with average velocity of 71 ± 20 µm/s (pH 7.0, [H2O2] = 5 wt%, [Triton X-100] = 0.2 wt%) (Figure 2A, Video S1A). Swimming behavior was observed using optical microscopy with a digital high-speed camera (200 frames/s). The continuous microbubble releases from one end induced a selfpumping of the H2O2 fuel in the 1D-channel. The resultant liquid flow propels the tubes. In marked contrast, the Avi microtubes without Cat layer did not move under the same conditions. Azide anion is known to coordinate to the heme groups of Cat and to inhibit enzyme activity. Actually, the addition of sodium azide (NaN3, 5 mM) stopped the moving of the tubes within 1 min. All these results demonstrate (i) that the disproportionation of H2O2 was catalyzed by the innermost bCat layer and (ii) that the subsequent O2 bubble expulsion is responsible for the autonomous propulsion (Figure 2B). The cylindrical wall of protein multilayers must be soft, although the microtube architecture was sufficiently robust to endure the bubble-propelled motion. The swimming trajectories of the PLA-bCat microtubes were mostly a turning motion, which probably arose from slight differences of the tube body symmetry and the opening shape. By addition of a magnetite layer in the tube wall, the direction of microtube movement would be manipulated to straight motion using magnetic field guidance.21,30


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Figure 2. Time-lapse images of microscopic observations of self-propelled Avi-bCat microtube by jetting O2 bubbles in PB solution (10 mM, 5 wt% H2O2, 0.2 wt% Triton X-100) at 25 °C. (A) In pH 7.0 (scale bar, 20 µm) (taken from Video SlA). The bottom image (enlarged image) portrays a line of moving O2 bubbles in the microtube capillary (orange arrow). (B) Schematic


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illustration of self-propulsion of Avi-bCat microtube by O2 bubble ejection from the terminal opening. (C) In pH 7.0 (scale bar, 10 µm) (taken from Video S1B). Slow motion images of O2 bubble migration in microtube and their expulsion from the tube mouth. Expulsion at 5 ms created one small bubble in the outer aqueous phase (orange arrow). The subsequent expulsion at 50 ms enlarged this bubble. The next expulsion at 90 ms generated a new bubble (light blue arrow). (D) In pH 6.0 (scale bar, 20 µm) (taken from Video S2B). The bottom image (enlarged image) portrays a line of moving O2 bubbles in the microtube capillary (orange arrow).

To our surprise, the migration of O2 bubbles was readily visible in the center of the tube because the protein walls are transparent and reasonably long (Figure 2A bottom, Video S1B). A line of moving bubbles was visible in the back half of the capillary. The nucleated nanobubbles in the front half of the tube might be too small to detect using optical microscopy (Figure 2B). We inferred that the O2 bubble size increases in the fast flow by increasing the number of tiny bubbles. Furthermore, careful inspections revealed that two expulsions every 45 ms (22.2 Hz) from the tube’s mouth create one bubble in the outer aqueous phase (Figure 2C, Video S1B). For instance, the first expulsion at 5 ms provides one small bubble of around 3 µm diameter (orange arrow). The second expulsion at 50 ms blows up this balloon to 5 µm. The next expulsion at 90 ms creates another new bubble (light blue arrow). He et al. reported that conical protein microbots encapsulating gelatin hydrogel with Cat are able to swim in aqueous H2O2 solution.31 Unfortunately, the rockets lose their bubble propulsion capability within 10 min at high peroxide concentration (> 5 wt%). That loss is likely to be attributed to the inactivation of Cat by the presence of a high gradient of hydroxyl radicals.31,36


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This inactivation contrasts significantly against the fact that our Avi-bCat microtube motors retain their bubble-ejection capability for over 3 hr at 5 wt% H2O2. One possible explanation is that the hydroxyl radicals and other enzyme inhibitors are always washed out from the channels of Avi-bCat microtubes with the water stream. We inferred that the cylindrical hollow structure is more preferred for biocatalytic O2 bubble propulsion for long periods. The Avi-bCat microtubes maintained their original morphology after 3 hr self-propelling experiment in the medium used. The pH and temperature, the main parameters of enzyme activity, strongly affect the protein microtube motor mobility. Indeed, the swimming speed of Avi-bCat microtubes was affected by pH (pH 6.0–9.0), for example 71 ± 20 µm/s (3.0 body-lengths/s) in pH 7.0 (Figure 2A, Video S1A) and 42 ± 12 µm/s (1.8 body-lengths/s) in pH 6.0 (Figure 2D, Video S2A). It is particularly interesting that the pH dependence of velocity exhibited a maximum peak at pH 7.0, which corresponds to the optimum pH of Cat (Figure 3A).37 It is noteworthy that slight back pressure in the capillary was observed before every expulsion at pH 6.0 (Video S2B). This back pressure might be caused by a weak pushing force of bubbles from the inside tube at low pH. Under constant pH 7.0, the Avi-bCat microtubes swim much faster at 35 °C (120 ± 23 µm/s, 5.1 bodylengths/s), which is almost the optimum temperature of the enzyme (37 °C). As expected, the temperature dependence of the tube (15–50 °C) coincided perfectly with the Cat activity curve (Figure 3B).37 Acceleration and deceleration by pH and temperature changes were fully reversible, signifying that bCat biocatalysts are bound tightly on the internal wall. We concluded that the Avi-bCat microtube motor velocity can be regulated by the modulation of enzyme activity with pH and temperature.


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Figure 3. (A) Influence of pH on average velocity of self-propelled Avi-bCat microtubes (5 wt% H2O2, 0.2 wt% Triton X-100) and on the Cat activity37 at 25 °C (n = 10). (B) Influence of temperature on the average velocity of self-propelled Avi-bCat microtubes (5 wt% H2O2, 0.2 wt% Triton X-100) and on the Cat activity37 in pH 7.0 (n = 10).


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Protein microtube motors have drawback in stabilities relative to inorganic tubules. However, disadvantage in long-term use could be replaced by advantage of biodegradability. The Avi-bCat microtubes consist only of proteins and polypeptides. Therefore, the tubular wall can be easily decomposed by acid and protease. After 6 hr incubation with acidic water (pH 3.0), the Avi-bCat microtubes were entirely degraded. Pronase, the cocktail of several proteases, digests the proteins into individual amino acids. Upon addition of Pronase into the Avi-bCat microtube dispersion, the hollow column morphology disappeared within 120 min (Figure S1). In conclusion, results demonstrate the two-step fabrication of self-propelled protein rolledsandwiches with a Cat innermost layer and their controllable velocity by the modulation of enzyme activity. The H2O2 diffused into the channel of “5.9 femtoliter” volume was decomposed to O2 bubbles by the Cat interior surface. The O2 bubble migration in the center of transparent microtube was observed clearly. The cylindrical wall was sufficiently stable to the bubblepropelled motion in water. The swimming speed of the tubes reached maximum at the optimum pH and temperature of Cat engines. Furthermore, the microtubes were degraded in acidic water and were digested completely by proteases. Compared to other biodegradable polymer-based and metal-based motors, the most important advantage of our “all protein” microtubes would be possible immobilization of different enzymes with desired arrangement in the stratiform wall, which can accomplish functional relay of sequential enzymatic reactions. For example, if we introduce glucoamylase and glucose oxidase as intermediate layers into the Avi-bCat microtube,38

a

starch

fuel-driven

motor

would

be

realized.

Combining

with

bionanoarchitectonics and bioassembly concepts39,40 would support creation of various tailormade microtube motors that move with a variety of biosubstances as power source.


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ASSOCIATED CONTENT Supporting Information. Supporting Information is available free of charge from the ACS Publication website at DOI:… Materials and detailed experimental procedures, morphology change of Avi-bCat microtube in Pronase solution (Figure S1) (PDF), self-propelled motion of Avi-bCat microtube in pH 7.0 at 25 °C (Video S1) (AVI), and in pH 6.0 at 25 °C (Video S2) (AVI).

AUTHOR INFORMATION Corresponding Author * E-mail: [email protected] ORCID Yoshitsugu Morita: 0000-0001-9288-4840 Teruyuki Komatsu: 0000-0002-7622-3433 Author Contributions T.K. designed and initiated this study. All the authors conducted experiments and analyzed the data. N.S. and T.K. drafted the manuscript. Notes The authors have no conflict of interest related to this study.

ACKNOWLEDGMENTS This work was supported by Grants-in-Aid for Scientific Research (B) (No. 15H03533 and No. 18H01833) from JSPS.


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