Photomechanical Azobenzene Crystals

crystals

Review Photomechanical Azobenzene Crystals

Takuya Taniguchi 1 , Toru Asahi 2,3 and Hideko Koshima 3,* 1 Center for Data Science, Waseda University, 27 Waseda-cho, Shinjuku-ku, Tokyo 1620042, Japan 2 Department of Advanced Science and Engineering, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 1698555, Japan 3 Research Organization for Nano & Life Innovation, Waseda University, 513 Wasedatsurumaki-cho, Shinjuku-ku, Tokyo 1620041, Japan * Correspondence: [email protected]; Tel.: +81-3-5286-8307

Received: 12 August 2019; Accepted: 20 August 2019; Published: 22 August 2019

Abstract: Photomechanically responsive materials are promising candidates for future smart actuator applications. The photo-responsive behaviors originate from the photoisomerization of photochromic molecules. A typical photochromic compound, azobenzene, has been studied extensively in the solution state and has played a crucial role in the photomechanical behaviors of materials such as polymers and gels, via chemical bridging with their matrix. In contrast to polymers and gels, the photomechanical attributes of molecular crystals have not progressed to the same degree, due to their rigidity and fragility. However, the past decade has witnessed an increasing number of reports of the photomechanical motion of molecular crystals, including azobenzene crystals. This paper reviews the current state-of-the-art of mechanically responsive azobenzene crystals, including the history, crystal design strategy, and future promising applications.

Keywords: azobenzene; photomechanical motion; trans-cis photoisomerization; molecular crystal; actuation

1. Introduction to Photomechanical Materials

1.1. Actuator Materials Actuation, which refers to mechanical motion or operation resulting from an energy conversion process, is prevalent throughout nature and characterizes some human activities. Animals and plants consume energy to create the mechanical motion required for survival and reproduction. Humans have developed mechanical systems for many purposes, and related to a wide range of actuation functions, to meet various needs. As to the specific materials used for actuation, inorganic materials that respond mechanically to external stimuli have historically played crucial roles in advancing actuation technology. For instance, a small piece of quartz, i.e., a crystal of silicon dioxide, ticks every second in an electric watch by oscillating at a constant frequency under an applied voltage. Shape memory alloys have been developed for many applications due to their shape recovery effect in response to a temperature change. Other examples of material actuation include those based on the piezoelectric effect, magnetostrictive effect, shape recovery, and thermal expansion [1]. The development of organic materials, mainly polymeric materials, for actuation has advanced steadily. Responses to various kinds of stimuli, including light, heat, voltage, magnetic fields, pressure, humidity, and biological enzymes have been achieved [2,3]. In addition, organic materials are generally softer, lighter, and cheaper than inorganic materials. Therefore, mechanically responsive organic materials are expected to come to the forefront in next-generation smart actuators. Potential future applications include soft robots, mechanical devices, active catheters, wearable applications, and so on [4,5].

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1.2. Azobenzene Compounds for Actuator Materials The photomechanical response upon light irradiationirradiation has advantages for remote control and diverse actuation actuation via via focused focused light light or orselective selective wavelengths wavelengths [6]. [Photomechanical6]. Photomechanical polymers polymers have havebeen beenwell developed well developed by crosslinking by crosslinking the polymeric the polymeric main chain main with chain photochromic with photochromic compounds, compounds, which whichconvert convert their molecular their molecular geometry geometry and andelectronic electronic state state upon upon photoirradiation photoirradiation [7]. [7]. The The typical photochromic compound compound is isazobenzene, azobenzene, which which undergoes undergoes transtrans-to-cis-to- photoisomerizationcis photoisomerization and cis and-to- cistrans-to- transback-isomerizationback-isomerization reversibly reversibly (Scheme (Scheme 1). 1The). The physicochemical physicochemical properties properties of azobenzeneazobenzene compounds havehave been been researched researched extensively extensively in the in solution the solution state [8 ].state In polymeric [8]. In polymeric networks, networks, molecular geometrymolecular changesgeometry due changes to trans due-to- tocis transphotoisomerization-to-cis photoisomerization result in photo-actuation. result in photo-actuation. When a polymer When crosslinkeda polymer withcrosslinked azobenzene with is azobenzene irradiated by is light irradiated at wavelengths by light suitable at wavelengths for photoisomerization, suitable for cisphotoisomerization,-isomer photoproducts cis-isomer are generated, photoproducts mostly on are the generated, irradiated mo surface.stly on The the number irradiated of photoproducts surface. The decreasesnumber of according photoproducts to the penetration decreases according depth of the to light. the penetration The gradient depth distribution of the oflight.cis-isomer The gradient results indistribution a bilayer-like of structurecis-isomer in results the material, in a bilayer-like inducing macroscopic structure in deformations the material, such inducing as bending, macroscopic twisting, anddeformations helicoidal such motions as bending, [9–11]. This twisting, actuation and helico mechanismidal motions can also [9–11]. be applied This actuation to azobenzene-containing mechanism can gels.also be Gels applied are generally to azobenzene-containing much softer than gels. polymers Gels are due generally to the existence much softer of solvents, than polymers and result due in to a photomechanicalthe existence of solvents, response and with resu smallerlt in a photomechanical output force [12,13 response]. with smaller output force [12,13].

Scheme 1.1. Trans-to--to-cis photoisomerizationphotoisomerization ofof azobenzeneazobenzene uponupon photoirradiationphotoirradiation (h(hνν).). CisCis-to--to-trans back-isomerization undergoesundergoes by by thermal thermal energy energy (kT) (kT) or lightor light irradiation irradiation at di ffaterent different wavelengths wavelengths (hν’). (hν’). 1.3. Photomechanical Crystals 1.3. PhotomechanicalIn contrast to soft Crystals materials such as polymers and gels, molecular crystals are considered a more rigidIn and contrast fragile to material. soft materials For example, such as polymers when strain and is gels, applied molecular to a single crystals crystal are viaconsidered photoproducts a more orrigid mechanical and fragile stress, material. the periodicallyFor example, ordered when strain alignment is applied of molecules to a single results crystal in via the photoproducts collapse of a singleor mechanical crystalline stress, state the into periodically a polycrystalline ordered or alignment amorphous of state molecules [14]. However, results in inthe contrast collapse to of this a stereotypicalsingle crystalline characterization, state into a polycrystalline a landmark report or amorphous published in state 2007 [14]. demonstrated However, thatin contrast photochromic to this crystalsstereotypical of diarylethene characterization, compounds a landmark bent at anreport observable published scale in upon2007 lightdemonstrated irradiation that [15 photochromic]. This finding hascrystals had aof significant diarylethene impact compounds on the research bent at community. an observable A decade scale later,upon interestlight irradiation in photomechanical [15]. This crystalsfinding ofhas various had photochromica significant compoundsimpact on the continues research togrow, community. as evidenced A decade by the numerouslater, interest reports in inphotomechanical the literature [16 crystals–21]. of various photochromic compounds continues to grow, as evidenced by the numerousRegarding reports typical in photochromic the literature compound [16–21]. azobenzenes, dozens of crystals have been reported to enableRegarding various typical photomechanical photochromic behaviors compound based azobenz on theirenes,trans dozens-cis photoisomerization of crystals have been (Figure reported1). Thus,to enable azobenzenes various photomechanical have played a rolebehaviors in demonstrating based on their the trans photo-responsive-cis photoisomerization functionality (Figure ofthe 1). crystallineThus, azobenzenes state, prompting have played this reviewa role in of demonstra its potentialting contribution the photo-responsive to future developments functionality inof thisthe researchcrystalline area. state, prompting this review of its potential contribution to future developments in this researchBefore area. moving to the next section, we briefly discuss the mechanical properties of mechanically responsiveBefore molecular moving to crystals the next by section, comparing we briefly them to discuss other actuator the mechanical materials properties (Figure2)[ of22 mechanically]. Molecular crystalsresponsive possess molecular a Young’s crystals modulus by ofcomparing 1–10 GPa andthem deform to other with aactuator strain of materials 0.1–1%. Metals, (Figure inorganics, 2) [22]. andMolecular shape memorycrystals alloyspossess are a locatedYoung’s at modulus the higher of end 1–10 of theGPa Young’s and deform modulus with range a strain compared of 0.1–1%. with molecularMetals, inorganics, crystals. and In contrast,shape memory polymers alloys and are gels located reside at in the the higher lower end modulus of the Young’s regime, however,modulus theirrange properties compared can with be molecular tuned over crystals. a broad In range. contrast, The mappingpolymers of and actuator gels reside materials in the shown lower in modulus Figure2 indicatesregime, however, that mechanically their properties responsive can be molecular tuned over crystals a broad are range. located The in mapping the unexplored of actuator area materials between hardshown and in soft Figure materials. 2 indicates This has that motivated mechanically the search responsive for new mechanicalmolecular crystals molecular are crystals located for in novel the andunexplored exciting area applications. between hard and soft materials. This has motivated the search for new mechanical molecular crystals for novel and exciting applications.

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Figure 1. Photomechanical azobenzene crystals previously reported in [26] for 1, [27] for 2, [29] for 3– FigureFigure 1. 1.Photomechanical Photomechanical azobenzene azobenzene crystals crystals previously previously reported reported in in [26] [26] for for1 1,, [27] [27] for for2 2,, [29] [29] for for3 3––7, 7, [32] for 8, [33] for 9, [49] for 10, [38] for 11, [42,43] for 12–16, [44] for 17–21, [53] for 22, [45] for 23– [32]7, [32] for 8for, [33] 8, [33] for for9, [49] 9, [49] for for10, 10 [38], [38] for for11, 11 [42,43], [42,43] for for12 –1216–,16 [44], [44] for for17 –1721–,21 [53], [53] for for22 22, [45], [45] for for23 23–25–, 25, [46] for 26, and [47] for 27. [46]25, for[46]26 for, and 26, [47]and for[47]27 for. 27.

Figure 2. Relationship between the Young’s modulus and strain of actuator materials. Reprinted with FigureFigure 2. 2. Relationship Relationship betweenbetween the Young’s modulus andand ststrainrain ofof actuator actuator materials. materials. Reprinted Reprinted with with permission from [22]. Copyright 2019 Wiley-VCH. permissionpermission fromfrom [22].[22]. CopyrightCopyright 2019 Wiley-VCH.

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2. Development of Photomechanical Azobenzene Crystals

2.1. Early Stage of Photomechanical Azobenzene Crystals Although thethe crystal crystal structures structures of trans of -trans and -cis and-azobenzene cis-azobenzene with no substituentwith no substituent were determined were almostdetermined 50 years almost ago 50 [23 years,24], transago [23,24],-cis photoisomerization trans-cis photoisomerization in the crystalline in the state crystalline had been state thought had been not tothought occur atnot all to [ 25occur], or toat occurall [25], only or underto occur controlled only under circumstances, controlled circumstances, as the molecular as transformation the molecular requirestransformation motion requires of molecules motion in aof densely molecules packed in a space.densely However, packed space. reports However, on the photomechanical reports on the bendingphotomechanical of diarylethene bending crystals of hasdiarylethene motivated crys renewedtals explorationhas motivated of photomechanically renewed exploration bendable of azobenzenephotomechanically crystals. bendable azobenzene crystals. A crystalcrystal of transof -4-(dimethylamino)azobenzenetrans-4-(dimethylamino)azobenzene (trans- 1)( wastrans reported-1) was as thereported first photomechanical as the first azobenzenephotomechanical crystal azobenzene [26]. A thin crystal plate-like [26]. A crystalthin plate-like of trans -crystal1, which of trans was- prepared1, which was by sublimation,prepared by bentsublimation, along the bentb-axis along upon ultravioletthe b-axis (UV)upon light ultraviolet irradiation (UV) onto light the (001)irradiation surface onto (Figure the3). (001) The bending surface reached(Figure 3). a steadyThe bending statein reached 5 s under a steady light state irradiation, in 5 s under and thenlight returnedirradiation, to and the initialthen returned unbent shapeto the withininitial unbent 30 s upon shape the within removal 30 ofs upon UV irradiation. the removal Notably, of UV irradiation. reversible bendingNotably, wasreversible demonstrated bending overwas 100demonstrated cycles [26]. over 100 cycles [26]. The bending response originates from the strain induced by trans-to-cis photoisomerization via a mechanism similar to that foundfound inin polymers.polymers. The photoisomerization is most significant significant at the irradiated surface and decreases depending on thethe lightlight penetrationpenetration depth.depth. The gradientgradient formationformation of cis-isomers generates strain in the thin crystal, resulting in a bending motion away from the light source. One of the critical factorsfactors relatedrelated toto thethe bendingbending response response is is the the electron electron donor donor substituent substituent of of1. The1. The amino amino group group works works as an as electron an electron donor donor and increases and increases the photoreactivity the photoreactivity of the n– πof* transition,the n–π* throughtransition, which throughtrans which-to-cis transphotoisomerization-to-cis photoisomerization occurs [8]. Theoccurs increased [8]. The reactivity increased allows reactivity conversion allows ofconversiontrans-1 into of transcis-1 -in1 into the crystal,cis-1 in whichthe crystal, is su ffiwhichcient is for sufficient bending for by bending the generated by the strain. generated strain.

Figure 3. Photomechanical bending of a thin crystal of transtrans--11 ((aa)) before before and and ( (b)) after after ultraviolet ultraviolet (UV) (UV) irradiation. The The irradiation irradiation was was conducted conducted from from the the right right rear rear side side of the of thecrys crystal,tal, as indicated as indicated by the by arrow.the arrow. The The scale scale bar bar is is200 200 µm.µm. Reprinted Reprinted with with permission permission from from [26]. [26]. Copyright Copyright 2009 2009 AmericanAmerican Chemical Society.

Shortly after the initial report, trans-4-aminoazobenzene (trans-2) bending under UV irradiation was demonstrated [[27].27]. As to the molecular structure, trans-2 has also been used as an electron donor substituent. A thin thin crystal crystal of of transtrans--22,, whose whose longitudinal longitudinal direction direction corresponds corresponds to the the crystallographic crystallographic b-axis, bent away from the light source upon UV irradiation from thethe left side (Figure4 4).). AfterAfter turningturning ooffﬀ the light,light, the bendingbending returnedreturned toto thethe initialinitial statestate withinwithin 240240 s.s. However, when irradiated by visible light (530 nm) the initial state waswas achievedachieved withinwithin 6060 s.s. These ﬁndingsfindings suggest that tuning the photoreactivity of azobenzene compounds providesprovides the means to constructconstruct photomechanicalphotomechanical azobenzene crystals.

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Figure 4. Photomechanical bending of a thin crystal of transtrans--22 ((a)) before before and and ( (b)) after after UV UV irradiation. irradiation. The scale bar is 100 µµm.m. Reprinted with permissionpermission from [[27].27]. CopyrightCopyright 2012 Elsevier.

2.2. Fast Response Photomechanical crystals show dynamic photo-responsivephoto-responsive deformations, however, the bent crystal takes tens of seconds or minutes to return to its initial shape, limiting practical application. The reversiblereversible bendingbending cancan be be divided divided into into two two processes: processes: a a photomechanical photomechanical bending bending process process due due to transto trans-to-cis-to-photoisomerizationcis photoisomerization and an and unbending an unbending process dueprocess to cis -to-duetrans tothermal cis-to-trans or photochemical thermal or back-isomerization.photochemical back-isomerization. Thus, the bending Thus, process the bending depends process on the depends light conditions on the light (e.g., conditions intensity (e.g., and wavelength)intensity and andwavelength) the photoreactivity and the photoreactivity (for trans-cis photoisomerization).(for trans-cis photoisomerization). The consecutive The consecutive unbending processunbending is aff processected by is theaffected half-life by ofthecis half-life-trans back of cis isomerization.-trans back isomerization. Of course, both Of course, processes both also processes depend onalso the depend size and on shapethe size of and crystals shape and of othercrystals external and other conditions, external such conditions, as temperature. such as temperature. The fast relaxation of cis-to-trans back isomerization can be tuned by adding an electron- withdrawing groupgroup to to an an azobenzene azobenzene [28]. [28]. The electron-withdrawingThe electron-withdrawing group worksgroup toworks pull theto electrons,pull the resultingelectrons, in resulting the short in lifetimes the short of lifetimescis-isomers of relativecis-isomers to other relative azobenzenes. to other azobenzenes. The electron-withdrawing The electron- groupwithdrawing also shifts group its absorption also shifts peak its absorption into wavelengths peak into ranging wavelengths from blue ranging to green, from enabling blue a to response green, toenabling visible a light. response Bushuyev to visible et al.ligh reportedt. Bushuyev fast et reversible al. reported bending fast reversible of azobenzene bending crystals of azobenzene (1, 3–7 in transcrystals-form) (1, by3–7 irradiation in trans-form) with by high-power irradiation visible with lighthigh-power [29]. Among visible them, light thin [29]. crystals Among of 3them,–7, which thin havecrystals an electron-withdrawingof 3–7, which have an –NO electron-withdrawing2 or –COOH group, exhibited –NO2 or a faster–COOH unbending group, exhibited speed at half-lives a faster 2 ofunbending less than speed 0.1 s afterat half-lives the removal of less of than high-power 0.1 s after light the removal irradiation of high-power of 1 W/cm .light The irradiation crystals of of3– 71 2 inW/cmtrans2. -formThe crystals required of minimal 3–7 in trans light-form intensities required of 50–200minimal mW light/cm intensitiesfor photo-bending, of 50–200 mW/cm whereas2 thefor 2 transphoto-bending,-1 crystal initiated whereas bending the trans at 1- mW1 crystal/cm dueinitiated to its higherbending photoreactivity. at 1 mW/cm2 due to its higher photoreactivity. 2.3. Model of Dynamical Photo-Bending 2.3. ModelThere of have Dynamical been anPhoto-Bending increasing number of reports of photomechanical azobenzene crystals, however, a quantitative mathematical description of the mechanical response has not yet been There have been an increasing number of reports of photomechanical azobenzene crystals, provided. The classical bending model is based on the bimetal model described by Timoshenko [30]. however, a quantitative mathematical description of the mechanical response has not yet been When a plate with a specific coefficient of thermal expansion is attached to another plate that has provided. The classical bending model is based on the bimetal model described by Timoshenko [30]. a different coefficient of thermal expansion, the bilayer material bends upon heating towards the When a plate with a specific coefficient of thermal expansion is attached to another plate that has a material with the lower coefficient due to the generated strain. In the case of photomechanical different coefficient of thermal expansion, the bilayer material bends upon heating towards the actuation, the bending strain originates from photoproducts, which form nonuniformly in the crystal. material with the lower coefficient due to the generated strain. In the case of photomechanical The structural mismatch between the photoproduct and the reactants creates a residual strain that actuation, the bending strain originates from photoproducts, which form nonuniformly in the crystal. causes macroscopic deformation of the crystal. Although Timoshenko’s bimetal model can explain the The structural mismatch between the photoproduct and the reactants creates a residual strain that bending speed of photomechanical crystals [31], it is essential to establish a mathematical model that causes macroscopic deformation of the crystal. Although Timoshenko’s bimetal model can explain provides a kinematic explanation of the macroscopic reshaping. the bending speed of photomechanical crystals [31], it is essential to establish a mathematical model Naumov et al. constructed two kinematic models, one simple model and one extended model, that provides a kinematic explanation of the macroscopic reshaping. to describe the bending angle as a function of time based on reaction kinetics theory [32]. The simple Naumov et al. constructed two kinematic models, one simple model and one extended model, model considers the rate constants of the primary reactions between the reactant and photoproduct to describe the bending angle as a function of time based on reaction kinetics theory [32]. The simple and describes bending and relaxation as monolithic exponential models. The extended model is a model considers the rate constants of the primary reactions between the reactant and photoproduct biexponential model that considers chemical processes in detail, including the excited state, intersystem and describes bending and relaxation as monolithic exponential models. The extended model is a crossing, and internal conversion. The two models were verified by reference to the experimental biexponential model that considers chemical processes in detail, including the excited state, intersystem crossing, and internal conversion. The two models were verified by reference to the

Crystals 2019, 9, x FOR PEER REVIEW 6 of 14 Crystals 2019, 9, 437 6 of 14 experimental results of slender azobenzene crystals of trans-8 (Figure 5). The time profile of the resultsbending of angle slender during azobenzene photomechani crystalscal of bendingtrans-8 was(Figure fully5). fitted The timeto the profile simple of model, the bending and was angle also duringwell explained photomechanical by the extended bending model. was fully The fittedbending to the angle simple during model, the relaxation and was also process well explainedwas not well by theexplained extended by model.the simple The model, bending but angle well during fitted thethe relaxationextended processbiexponential was not model. well explained Such kinematic by the simplemodel was model, further but wellextended fitted as the described extended in biexponential their review model.[19]. They Such also kinematic reported model photomechanical was further extendedbehavior of as 9 described [33]. in their review [19]. They also reported photomechanical behavior of 9 [33].

Figure 5.5. ModelModel construction construction of theof the kinematic kinemati behaviorc behavior of photo-bending. of photo-bending. (a) Bilayer (a) Bilayer model of model bending. of (bending.b) Definition (b) Definition of angular of deflection angular anddeflec relatedtion and parameters. related parameters. (c) Model verification (c) Model byverification reference by to thereference experimental to the experimental results of slender results photomechanical of slender photomechanical crystals of trans -crystals8. The models of trans include-8. The a models simple modelinclude for a simple bending model (A), a for simple bending model (A), for a unbendingsimple model (B), for and unbending an extended (B), model and an for extended unbending model (C). Reprintedfor unbending with (C permission). Reprinted from with [32 permission]. Copyright from 2014 [32]. American Copyright Chemical 2014 American Society. Chemical Society. 3. Design of New Azobenzene Crystals for Actuation 3. Design of New Azobenzene Crystals for Actuation Molecular crystals provide a platform for various functionalities, as organic molecules can form Molecular crystals provide a platform for various functionalities, as organic molecules can form diverse structures with limited constituents. The strategy used to functionalize a crystal relies on the diverse structures with limited constituents. The strategy used to functionalize a crystal relies on the crystal design, specifically, the molecular structure and intermolecular interactions. The molecular crystal design, specifically, the molecular structure and intermolecular interactions. The molecular architecture provides the basis for new crystal structures expressing specific functions, although it is architecture provides the basis for new crystal structures expressing specific functions, although it is challenging to predict crystal structures from molecular structures. This section reviews several works challenging to predict crystal structures from molecular structures. This section reviews several describing photomechanical azobenzene crystal construction, according to the crystal design. works describing photomechanical azobenzene crystal construction, according to the crystal design. 3.1. Chirality Induction 3.1. Chirality Induction Dozens of photomechanical crystals, not of only azobenzenes but also of other photochromic Dozens of photomechanical crystals, not of only azobenzenes but also of other photochromic compounds, have been reported to bend under photoirradiation. The bending motion is a mode of compounds, have been reported to bend under photoirradiation. The bending motion is a mode of actuation resulting from elongation or contraction of the irradiated surface. In contrast to bending, actuation resulting from elongation or contraction of the irradiated surface. In contrast to bending, there have been few reports on twisting of the crystal, which is another mode of actuation [34–37]. there have been few reports on twisting of the crystal, which is another mode of actuation [34–37]. The twisted shape has chirality, because the right-handed twist does not overlay its mirror image, The twisted shape has chirality, because the right-handed twist does not overlay its mirror image, i.e., the left-handed twist. Thus, photoisomerization in chiral photochromic crystals may lead to i.e., the left-handed twist. Thus, photoisomerization in chiral photochromic crystals may lead to macroscopic deformation with chirality, such as a twisting motion. macroscopic deformation with chirality, such as a twisting motion. Based on this concept, the photomechanical motion of thin crystals of compound trans-(S)-11 was Based on this concept, the photomechanical motion of thin crystals of compound trans-(S)-11 revealed [38]. In this study, a thin plate crystal was obtained by sublimation. The crystal had a (001) was revealed [38]. In this study, a thin plate crystal was obtained by sublimation. The crystal had a face with the b-axis as the longitudinal axis, along which intermolecular NH---O hydrogen bonding (001) face with the b-axis as the longitudinal axis, along which intermolecular NH---O hydrogen

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bonding chains formed in the crystal. When the front (001) face was irradiated with UV light, the crystal bent away from the source with slight left-handed twisting (Figure 6). The crystals, which showed bending with the slight twist, returned to their initial shape within 2–3 min after turning off the UV light. When the back (00-1) surface was irradiated, bending motion with a twist was observed, similar to that of the (001) face (Figure 6).

CrystalsThis2019 bending, 9, 437 accompanying a twist is caused by elongation of the irradiated surface along7 of the 14 orthogonal direction. At the molecular level, trans-to-cis photoisomerization of compound trans-(S)- 11 leads to contraction of the a-axis and elongation of the b-axis, based on the optimized molecular chainsgeometries formed of cis in-( theS)- crystal.11. This Whenchange the in frontmolecular (001) facestructure was irradiated occurs mostly with on UV the light, irradiated the crystal surface, bent awayand the from probability the source of with trans slight-to-cis left-handed photoisomerization twisting (Figure decreases6). The along crystals, the thickness which showed direction bending due to withthe attenuation the slight twist, of UV returned light. This to theiris why initial cis-( shapeS)-11 molecules within 2–3 are min formed after turning in the crystal oﬀ the along UV light. a gradient When thefrom back the (00-1)irradiated surface surface. was irradiated, The strain bending induces motion elongation with along a twist the was b-axis observed, and contraction similar to that along of thethe (001)a-axis, face resulting (Figure in6). bending away from the light source with a twist.

Figure 6.6. PhotomechanicalPhotomechanical reversible reversible bending bending with with twisting twisting of a of chiral a chiral azobenzene azobenzene crystal crystal of trans of-( transS)-11-. Upon(S)-11. UV Upon irradiation UV irradiation on the front on the (001) front face, (001) the thinface, crystal the thin bends crystal with bends a left-handed with a left-handed twist. Bending twist. in theBending same directionin the same as thedirection twist was as the seen twist upon was light seen irradiation upon light on theirradiation back (00-1) on face.the back Reprinted (00-1) withface. permissionReprinted with from permission [38]. Copyright from 2016[38]. Wiley-VCH.Copyright 2016 Wiley-VCH.

3.2. CrystallizationThis bending with accompanying Multi-Molecular a twist Components is caused by elongation of the irradiated surface along the orthogonal direction. At the molecular level, trans-to-cis photoisomerization of compound trans-(S)-11 Another strategy is to design photomechanical azobenzene crystals with multi-components. One leads to contraction of the a-axis and elongation of the b-axis, based on the optimized molecular notable crystal engineering technique is co-crystallization. A co-crystal is defined as a crystal geometries of cis-(S)-11. This change in molecular structure occurs mostly on the irradiated surface, consisting of at least two molecules. Co-crystals can be obtained by tuning intermolecular and the probability of trans-to-cis photoisomerization decreases along the thickness direction due to interactions, for instance hydrogen bond and halogen bond interactions. To induce intermolecular the attenuation of UV light. This is why cis-(S)-11 molecules are formed in the crystal along a gradient interactions between two components, it is of key importance to design one component as a donor from the irradiated surface. The strain induces elongation along the b-axis and contraction along the and the other as an acceptor of the expected intermolecular interaction. To date, there have been a-axis, resulting in bending away from the light source with a twist. numerous reports on co-crystallization techniques, and the functions of co-crystals, where the 3.2.number Crystallization of combinations with Multi-Molecular of two components Components is nearly infinite and affords diverse crystal structures [39–41]. AnotherThe crystals strategy of fluorinated is to design azobenzenes photomechanical 12–16 in cis azobenzene-form exhibit crystals photomechanical with multi-components. bending due Oneto cis notable-to-trans crystal photoisomerization engineering technique upon visible isco-crystallization. light irradiation [42,43]. A co-crystal Photomechanical is defined azobenzene as a crystal consistingco-crystals of 17 at–21 least were two developed molecules. by Co-crystals constructing can halogen be obtained bonds by tuningbetween intermolecular halogenated interactions,azobenzene foras a instance donor and hydrogen a pyridine bond compound and halogen as an bond accepter interactions. [44]. The halogen To induce I- or intermolecular Br- at the para interactions-position of betweenthe electron-deficient two components, perfluorphenyl it is of key importance group is highly to design polarizable one component and works as aas donor a donor, and forming the other the as anlinear acceptor interaction of the expectedbetween intermolecularan accepter of interaction.the halogen Tobond, date, pyridine. there have The been halogen numerous bonding reports motif on co-crystallizationresults in a zig-zag techniques, crystal structure, and the with functions alternating of co-crystals, alignment where of the the donor number and acceptor of combinations molecules, of twofor example components at a pitch is nearly of 20 infinite Å in the and case aff ofords the diverse co-crystal crystal of 17 structures (Figure 7). [39 Here,–41]. the co-crystal consists of cisThe-azobenzene, crystals of despite fluorinated the lower azobenzenes stability12 of– 16thein ciscis-isomer-form exhibit compared photomechanical with the trans bending-isomer; due the tociscis-trans-to- transthermalphotoisomerization back-isomerization upon of fluorinated visible light azobenzene irradiation [is42 very,43]. sl Photomechanicalow, allowing retention azobenzene of the co-crystalscis-isomer during17–21 were recrystallization. developed by constructing halogen bonds between halogenated azobenzene as a donorAll co-crystals and a pyridine of 17– compound21 exhibit asphotomechanical an accepter [44 ].bending The halogen under I- or532-nm Br- at laser the para irradiation,-position ofhowever, the electron-deficient the deflection angle perfluorphenyl depends on group the compon is highlyents polarizable and partners and of works the co-crystals. as a donor, The forming most thebendable linear interactionco-crystal under between weaker an accepter light intensity of the halogen (5 mW/cm bond,2) was pyridine. that of The 17 halogen(Figure bonding7). Upon motif light resultsirradiation, in azig-zag the crystal crystal bent structure, away from with the alternating light source alignment up to a deflection of the donor angle and of 90 acceptor°. The bent molecules, crystal for example at a pitch of 20 Å in the case of the co-crystal of 17 (Figure7). Here, the co-crystal consists of cis-azobenzene, despite the lower stability of the cis-isomer compared with the trans-isomer; the cis-trans thermal back-isomerization of fluorinated azobenzene is very slow, allowing retention of the cis-isomer during recrystallization. Crystals 2019, 9, x FOR PEER REVIEW 8 of 14 did not return to its initial shape after the removal of irradiation, indicating irreversible photomechanical bending due to cis-to-trans photoisomerization upon visible light irradiation. When a cis-isomer transforms to a trans-isomer, the trans-isomer forms a halogen bond with another pyridine, leading to a new co-crystal structure made from the trans-isomer. The structural mismatch between the new daughter crystal and the mother co-crystal of the cis-isomer produces the strain to bend away. The presence of a small amount of co-crystals in the trans-isomer was confirmed experimentally via in-situ X-ray crystallographic analysis, which also revealed that the conversion process unfolded as a crystal-to-crystal process (Figure 7). Besides co-crystals, molecular machines such as rotaxanes are also composed of multi- components with an axial molecule and a ring molecule. Photo-reactive pseudorotaxane crystals of 23–25 were constructed with an axial element with azobenzene and a ring element with different substituents [45]. The pseudorotaxanes with different substituents afforded crystal structures with differing intra- and intermolecular π–π distances and angles. All crystals of 23–25 bent upon UV (360 Crystalsnm) and/or2019, 9, 437visible light (445 nm) irradiation due to trans-cis photoisomerization, although8 ofthe 14 bending angle varied with the crystal structure.

Figure 7.7. Irreversible photomechanical bending of aa plate-likeplate-like co-crystalco-crystal ofof 1717.. ReprintedReprinted withwith permissionpermission fromfrom [[44].44]. Copyright 20142014 RoyalRoyal SocietySociety ofof Chemistry.Chemistry.

4. OtherAll co-crystalsMechanical of 17Responses–21 exhibit of photomechanical Azobenzene Crystals bending under 532-nm laser irradiation, however, the deflection angle depends on the components and partners of the co-crystals. The most bendable Besides bending and twisting behaviors, some azobenzene crystals reportedly exhibit co-crystal under weaker light intensity (5 mW/cm2) was that of 17 (Figure7). Upon light irradiation, movement, that is, locomotion, on a substrate surface upon encountering an external stimulus. the crystal bent away from the light source up to a deflection angle of 90◦. The bent crystal did not Locomotion of a material from one position to another is potentially useful for the transfer of return to its initial shape after the removal of irradiation, indicating irreversible photomechanical compounds, and to penetrate small spaces. Effectively, locomotive molecular crystals may work as bending due to cis-to-trans photoisomerization upon visible light irradiation. When a cis-isomer small robots in some environments. Two locomotive features of azobenzene crystals are described in transforms to a trans-isomer, the trans-isomer forms a halogen bond with another pyridine, leading the following. to a new co-crystal structure made from the trans-isomer. The structural mismatch between the First, crawling locomotion occurs due to a change in the physicochemical properties of the new daughter crystal and the mother co-crystal of the cis-isomer produces the strain to bend away. crystal caused by trans-cis photoisomerization [46]. When rhombus-shaped crystals of 3,3′- The presence of a small amount of co-crystals in the trans-isomer was confirmed experimentally via dimethylazobenzene (26) were irradiated by UV light from one direction, and simultaneously by in-situ X-ray crystallographic analysis, which also revealed that the conversion process unfolded as a visible light from the opposite direction, the crystals moved, i.e., crawled, very slowly on the glass crystal-to-crystal process (Figure7). surface in the direction of visible light irradiation (Figure 8). Phenomenologically, crawling Besides co-crystals, molecular machines such as rotaxanes are also composed of multi-components with an axial molecule and a ring molecule. Photo-reactive pseudorotaxane crystals of 23–25 were constructed with an axial element with azobenzene and a ring element with different substituents [45]. The pseudorotaxanes with different substituents afforded crystal structures with differing intra- and intermolecular π–π distances and angles. All crystals of 23–25 bent upon UV (360 nm) and/or visible light (445 nm) irradiation due to trans-cis photoisomerization, although the bending angle varied with the crystal structure.

4. Other Mechanical Responses of Azobenzene Crystals Besides bending and twisting behaviors, some azobenzene crystals reportedly exhibit movement, that is, locomotion, on a substrate surface upon encountering an external stimulus. Locomotion of a material from one position to another is potentially useful for the transfer of compounds, and to penetrate small spaces. Eﬀectively, locomotive molecular crystals may work as small robots in some environments. Two locomotive features of azobenzene crystals are described in the following. Crystals 2019, 9, 437 9 of 14

First, crawling locomotion occurs due to a change in the physicochemical properties of the crystal caused by trans-cis photoisomerization [46]. When rhombus-shaped crystals of 3,30-dimethylazobenzene (26) were irradiated by UV light from one direction, and simultaneously by Crystals 2019, 9, x FOR PEER REVIEW 9 of 14 visible light from the opposite direction, the crystals moved, i.e., crawled, very slowly on the glass surfacelocomotion in the of direction the crystal of originates visible light from irradiation the melting (Figure and8). crystallization Phenomenologically, of opposite crawling surfaces locomotion via light ofirradiation. the crystal The originates crystalsfrom of 26 the, whose melting melting and crystallizationtemperature is of ca. opposite 51–54 °C, surfaces melt upon via light UV irradiation.irradiation Theat room crystals temperature, of 26, whose due melting to the temperature depression is ca.of 51–54the melting◦C, melt point upon induced UV irradiation by trans at-to- roomcis temperature,photoisomerization. due to theOn the depression back side, of visible the melting light irradiation point induced causes by cistrans-to--to-transcis photochemicalphotoisomerization. back- Onisomerization, the back side, resulting visible light in recrystallization irradiation causes ofcis trans-to-trans-26. Thisphotochemical suggests that back-isomerization, the retraction caused resulting by inUV-light-induced recrystallization melting, of trans- 26and. This crystal suggests growth that caused the retraction by visible-light-induced caused by UV-light-induced recrystallization, melting, are andlikely crystal responsible growth for caused crawl bylocomotion visible-light-induced on the glass su recrystallization,rface. Recently, arethe likelycrawling responsible motion of for crystals crawl locomotionof 27 was achieved on the glass by surface. using only Recently, visible the light crawling [47]. motion Such solid-to-liquid of crystals of 27 transitionswas achieved induced by using by onlyphotoisomerization visible light [47 also]. Such enable solid-to-liquid swimming on transitions water surfaces induced [48] by and photoisomerization multi-directional alsobending enable of swimmingthin crystals on of water compound surfaces 10 [[49].48] and multi-directional bending of thin crystals of compound 10 [49].

Figure 8.8. Light-inducedLight-induced crawlingcrawling ofof crystalscrystals ofof 3,33,30-dimethylaminoazobenzne′-dimethylaminoazobenzne ((2626).). ReprintedReprinted withwith permission fromfrom [[46].46]. CopyrightCopyright 20152015 SpringerSpringer Nature.Nature.

Second, thermal locomotion is induced by structural phase transitions in trans-(S)-11 crystals, whichwhich is also expressed expressed as as photomechanical photomechanical motion, motion, as as described described previously previously [50]. [50 In]. this In thisstudy, study, the thethermal thermal structural structural phase phase transiti transitionon was wasunexpectedly unexpectedly found found to be toa reversible be a reversible process process at 145 at °C 145 upon◦C uponheating heating and cooling. and cooling. This Thisphase phase transition transition proceed proceedss in ina asingle-crystal-to-single-crystal single-crystal-to-single-crystal manner, manner, withoutwithout collapsecollapse of of the the single single crystal. crystal. Due toDue the to phase the transition,phase transition, the length the of thelengthb-axis, of thethe longitudinal b-axis, the directionlongitudinal ofa direction plate-like of crystal, a plate-like decreases crystal, by decreases 0.3% at temperatures by 0.3% at temperatures higher than 145higher◦C, than and returns145 °C, toand the returns initial to length the initial at lower length temperatures. at lower temperat Here, anures. azobenzene Here, an azobenzene molecule in molecule a unit cell in changes a unit cell its conformationchanges its conformation slightly but maintainsslightly buttrans maintains-form during trans-form the phase during transition. the phase The transition. decrease of,The and decrease return toof, theand original, return to crystal the original, length crystal lead to length bending lead motion to bending at the motion phase transition, at the phase due transition, to the temperature due to the gradienttemperature along gradient the thickness along direction.the thickness Upon direction. heating, theUpon phase heating, transition the phase starts attransition the lower starts side ofat the low-temperaturelower side of the (LT)low-temperature phase crystal, (LT) and thephase crystal crystal, bends and due the to crystal shortening bends of due the to crystal shortening length. of With the crystal length. With additional heating, the whole crystal completes the phase transition to a high- temperature (HT) phase. The HT phase crystal returns to the LT phase upon cooling through additional bending motion, as the transition to the LT phase occurs at the upper side cooled by the surrounding air. In turn, this leads to elongation of the crystal at the upper side. Thus, the crystal exhibits bending during both the heating and cooling cycles.

CrystalsCrystals 20192019,, 99,, 437x FOR PEER REVIEW 1010 ofof 1414

When a plate-like crystal with thickness gradient along the length was repeatedly heated and additionalcooled near heating, the phase the whole transition crystal temperature completes the on phase a silanized transition glass, to ait high-temperature was noted that (HT)the crystal phase. The“walked” HT phase in the crystal manner returns of an to theinchworm LT phase due upon to repeated cooling through bending additional and straightening bending motion, (Figure as9). the In transitionanother case, to the a thin LT phase plate-like occurs crystal at the moved upper sidemuch cooled faster by by the rolling surrounding on a glass air. surface In turn, after this leadsa single to elongationheating or cooling of the crystal process. at theIn the upper cases side. of both Thus, walking the crystal and exhibitsrolling, bendingthe locomotion during is both induced the heating by the andasymmetric cooling cycles.shape of the crystal. Walking occurs according to the thickness gradient, where one side is thickerWhen than a plate-like the other, crystal leading with to unidirectional thickness gradient movement along thevia bending length was and repeatedly straightening. heated Rolling and cooledoccurs nearaccording the phase to the transition width gradient, temperature and leads on a silanized to loss ofglass, balance it was during noted bending that the and crystal then “walked” flipping. in theThese manner examples of an inchworm suggest that due the to repeatedmechanical bending responses and straighteningof molecular (Figurecrystals9 ).can In be another diversified case, aby thin a photoisomerization-induced plate-like crystal moved much phase faster bychange rolling from on athe glass crystal surface form after to a singlea melted heating form, or coolingand by process.thermal Instructural the cases phase of both transitions. walking andThe rolling,mechanical the locomotion function of is the induced structural by the phase asymmetric transition shape can ofbe thecombined crystal. with Walking the photomechanical occurs according response to the thickness of photochromic gradient, wherecrystals. one Combining side is thicker the structural than the other,phase leadingtransition to unidirectionalwith photoisomerization movement via has bending resulted and in straightening.multiple mechanical Rolling occursmotions according of crystals to the[51,52]. width gradient, and leads to loss of balance during bending and then ﬂipping.

FigureFigure 9.9. ThermalThermal locomotion locomotion of of crystals crystals of oftranstrans-(S-()-S11)-11 duedue to tothe the structural structural phase phase transition. transition. (a) (Inchworm-likea) Inchworm-like “walking” “walking” of a of crystal a crystal with with a thickn a thicknessess gradient gradient along along the the length length under under cycles cycles of ofheating heating and and cooling. cooling. (b) ( bRolling) Rolling of ofa athin thin crystal crystal with with a a widt widthh gradient gradient upon upon heating heating or cooling. ReprintedReprinted withwith permissionpermission fromfrom [[5050].]. CopyrightCopyright 20182018 SpringerSpringer Nature.Nature.

5. PossibilitiesThese examples for Future suggest Applications that the mechanical responses of molecular crystals can be diversified by a photoisomerization-induced phase change from the crystal form to a melted form, and by thermal So far, we have reviewed the mechanical responses of azobenzene crystals. The actuation structural phase transitions. The mechanical function of the structural phase transition can be combined mechanism is interesting from a purely scientific standpoint. However, it is important to remember with the photomechanical response of photochromic crystals. Combining the structural phase transition that mechanically responsive crystals also show great potential as smart actuators and will find with photoisomerization has resulted in multiple mechanical motions of crystals [51,52]. appropriate applications as the field advances. 5. PossibilitiesA straightforward for Future example Applications of implementation is provided by photomechanical bending of azobenzene crystals, applied to the gripper of a micropipette (Figure 10) [53]. Here, the micropipette So far, we have reviewed the mechanical responses of azobenzene crystals. The actuation was constructed using the arm of an azobenzene compound 22 nanowire on the left side, and an mechanism is interesting from a purely scientific standpoint. However, it is important to remember that additional fixed polystyrene nanowire arm on the right side. When the pipette arms were irradiated mechanically responsive crystals also show great potential as smart actuators and will find appropriate by UV light, the azobenzene nanowire bent towards the light source, owing to the transparency of applications as the field advances. polystyrene. The bending of the azobenzene nanowire led to the grabbing of a small particle. This is A straightforward example of implementation is provided by photomechanical bending of one of many possible applications of azobenzene crystals while other potential applications include azobenzene crystals, applied to the gripper of a micropipette (Figure 10)[53]. Here, the micropipette microelectromechanical systems (MEMS), soft robots, flexible devices, medical catheters, aerospace was constructed using the arm of an azobenzene compound 22 nanowire on the left side, and an devices, and so on. Recent advances in 3D and 4D printing technology could be further improved by additionalmechanically fixed responsive polystyrene molecular nanowire crystals, arm on owing the right to side.inherently When advantageous the pipette arms properties were irradiated such as bylight UV weight light, and the azobenzenesoftness [54,55]. nanowire bent towards the light source, owing to the transparency of

Crystals 2019, 9, 437 11 of 14 polystyrene. The bending of the azobenzene nanowire led to the grabbing of a small particle. This is one of many possible applications of azobenzene crystals while other potential applications include microelectromechanical systems (MEMS), soft robots, ﬂexible devices, medical catheters, aerospace devices, and so on. Recent advances in 3D and 4D printing technology could be further improved by mechanically responsive molecular crystals, owing to inherently advantageous properties such as light weightCrystals 2019 and, 9 softness, x FOR PEER [54 REVIEW,55]. 11 of 14

Figure 10.10.Demonstration Demonstration of aof micro-pipette a micro-pipette using azobenzeneusing azobenzene nanowire nanowire of compound of 22compound. Azobenzene 22. Azobenzenenanowire bends nanowire towards bends the lighttoward sources the andlight grips source a particle; and grips the a polystyrene particle; the (PS) polystyrene nanowire (PS) is a nanowiretransparent is supporter. a transparent Reprinted supporter. with permission Reprinted fromwith [ 53permission]. Copyright from 2015 [53]. Royal Copyright Society of 2015 Chemistry. Royal Society of Chemistry. However, there are still some problems limiting the application of azobenzene crystals. The first concernsHowever, the di therefficulty are of still increasing some problems the maximum limiting forcethe application at actuation, of azobenzene and the second crystals. concerns The first the concernsdifficulty the of fabricating difficulty theof increa desiredsing shape. the maximum Regarding force the first at actuatio one, mechanicallyn, and the responsivesecond concerns molecular the difficultycrystals typically of fabricating generate the adesired maximum shape. stress Regarding in the rangethe first of one, 1–50 mechanically MPa at actuation responsive [50,56, 57molecular]. These crystalsvalues are typically generally generate 10–100 timesa maximum larger than stress the in maximum the range stress of 1–50 of typical MPa at human actuation muscle [50,56,57]. (0.3 MPa) These [58]. valuesTo lead are larger generally stress to10–100 larger times output larger force, than multiple the maximum pieces of stress crystals of typical need to human be integrated. muscle (0.3 Also, MPa) it is [58].challenging To lead tolarger fabricate stress molecular to larger output crystals force, with mu theltiple desired pieces shape of crystals and size. need to be integrated. Also, it is challengingThe hybridization to fabricate of crystals molecular and polymerscrystals with is a the promising desired approachshape and to size. overcome the limitations discussedThe hybridization above [59]. When of crystals molecular and polymers crystals are is incorporateda promising approach into a connective to overcome polymer, the limitations the hybrid discussedmaterial will above be more[59]. When flexible molecular and easier crystals to control, are incorporated in terms of into size a and connective shape, due polymer, to the the properties hybrid materialof the polymer. will be Inmore addition, flexible such and hybrideasier to materials control,should in terms respond of size fasterand shape, and generate due to the a larger properties force ofthan the polymers, polymer. owingIn addition, to the such inherent hybrid advantages materials ofshould molecular respond crystals. faster Thus, and generate the hybrid a larger strategy force of thancombining polymers, a polymer owing withto the a inherent mechanical advantages crystal, expectedof molecular to be crystals. realized Thus, in the the near hybrid future, strategy should of combiningenhance the a maximumpolymer with force a capabilitymechanical and crystal, simplify expected the fabrication to be realized process in of the actuator near future, materials. should enhance the maximum force capability and simplify the fabrication process of actuator materials. 6. Conclusions 6. ConclusionsThis paper reviewed the current state-of-the-art of photomechanical azobenzene crystals. PhotomechanicalThis paper reviewed responses the result current from state-of-the simple trans-art-cis ofphotoisomerization, photomechanical azobenzene but lead to crystals. a wide Photomechanicalarray of photomechanical responses behaviorsresult from varying simple trans by actuation-cis photoisomerization, mode (bending but or lead twisting), to a wide bending array ofmagnitude, photomechanical response behaviors speed, and varying relaxation by actuation time. Tuningmode (bending azobenzene or twisting), substituents bending and magnitude, employing responsecrystal engineering speed, and techniques, relaxation suchtime. as Tuning co-crystallization, azobenzene havesubstituents crucial rolesand inemploying diversifying crystal the engineeringphoto-responsiveness techniques, and such functionality as co-crystallization, of azobenzene have crystals. crucial Although roles in therediversifying are still the challenges photo- responsivenessahead, photomechanical and functionality crystals showof azobenzene promise as crysta novells. actuators, Although with there possible are still applications challenges ahead, in soft photomechanicalrobots, and medical crystals and flexible show prom devices.ise as novel actuators, with possible applications in soft robots, and medical and flexible devices.

Author Contributions: Writing—original draft preparation, T.T.; writing—review and editing, T.T. and H.K.; supervision, T.A. and H.K.

Funding: This research was funded by the JSPS Grant-in-Aid for Scientific Research B (17H03107) and Challenging Exploratory Research (16K12918).

Acknowledgments: T.T. and T.A. thank the Leading Graduate Program in Science and Engineering at Waseda University.

Conflicts of Interest: The authors declare no conflict of interest.

Crystals 2019, 9, 437 12 of 14

Author Contributions: Writing—original draft preparation, T.T.; writing—review and editing, T.T. and H.K.; supervision, T.A. and H.K. Funding: This research was funded by the JSPS Grant-in-Aid for Scientific Research B (17H03107) and Challenging Exploratory Research (16K12918). Acknowledgments: T.T. and T.A. thank the Leading Graduate Program in Science and Engineering at Waseda University. Conflicts of Interest: The authors declare no conflict of interest.

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