Morphology Control between Twisted Ribbon, Helical Ribbon, and

Jan 11, 2014 - ABSTRACT: pH-Responsive molecular assemblies with a variation in morphology ranging from a twisted ribbon, a helical ribbon, to a nanot...
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Morphology Control between Twisted Ribbon, Helical Ribbon, and Nanotube Self-Assemblies with His-Containing Helical Peptides in Response to pH Change Akihiro Uesaka,† Motoki Ueda,† Akira Makino,† Tomoya Imai,‡ Junji Sugiyama,‡ and Shunsaku Kimura*,† †

Department of Material Chemistry, Graduate School of Engineering, Kyoto University, Kyoto-Daigaku-Katsura, Nishikyo-ku, Kyoto 615-8510, Japan ‡ Research Institute for Sustainable Humanosphere (RISH), Kyoto University, Gokasho, Uji, Kyoto 611-0011, Japan S Supporting Information *

ABSTRACT: pH-Responsive molecular assemblies with a variation in morphology ranging from a twisted ribbon, a helical ribbon, to a nanotube were prepared from a novel A3Btype amphiphilic peptide having three hydrophilic poly(sarcosine) (A block) chains, a hydrophobic helical dodecapeptide (B block), and two histidine (His) residues between the A3 and B blocks. The A3B-type peptide adopted morphologies of the twisted ribbon at pH 3.0, the helical ribbon at pH 5.0, and the nanotube at pH 7.4, depending upon the protonation states of the two His residues. On the other hand, another A3B-type peptide having one His residue between the A3 and B blocks showed a morphology change only between the helical ribbon and the relatively planar sheets with pH variation in this range. The morphology change is thus induced by one- or two-charge generation at the linking site of the hydrophilic and hydrophobic blocks of the component amphiphiles but in different ways.

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INTRODUCTION Some chiral amphiphiles can self-assemble into chiral fibers1−4 and chiral ribbons5−7 in addition to tubular structures8−10 in aqueous solution. In the former two molecular assemblies, chiral amphiphiles are able to transfer their molecular chirality to those macroscopic morphologies. There have already been several reports on the relationship between the chiral amphiphiles and the chiral morphologies of twisted ribbons and helical ribbons.4,5,11,12 This kind of issue is important, especially in the field of biologically active peptides and proteins, which sometimes form chiral self-assemblies closely related to biological key issues, such as protein fibrillation found in amyloid-related diseases.13,14 Chiral morphologies of twisted sheets, twisted ribbons, and helical ribbons have been discussed in terms of molecular association strength in recent years.4,7,11,15 When the chiral amphiphiles are molecularly packed tightly, they tend to selfassemble into helical ribbons and tubular structures rather than twisted ribbons with saddle-like curvatures. The latter morphology is currently considered to reflect a relatively weak intermolecular interaction.6,15,16 To transfer the molecular chirality to the morphology of selfassemblies, molecular organization in the self-assemblies should have regular and tight molecular packing. In this regard, the βsheet structure is highly potential to provide a rigid molecular frame for molecular organization as reported previously.5,7,9 © 2014 American Chemical Society

However, less information can be obtained currently with chiral morphologies prepared by α-helical peptides. This is simply because β-sheet is based on intermolecular hydrogen-bond formation, which can easily regulate molecular arrangements of the neighboring peptide chains. On the other hand, α-helix is stabilized by intramolecular hydrogen bonds, and there needs to be some interacting forces between helices to realize the regular and tight helix packing. One such typical example for the tight helix association in nature is the Leu-zipper motif.17,18 We have been studying self-assemblies of amphiphilic helical peptides, (Sar)m-b-(Leu-Aib)n, to find out that the hydrophobic helical blocks can be tightly packed to form a curved sheet morphology because of consecutive titling between helices in the molecular assembling process.10,19 Further, with using [(Sar)m]2-His-(Leu-Aib)6, which self-assembled into rolledsheet morphology, we could demonstrate that the layer spacing of the rolled sheets was changed by a pH change because of a single protonation at His of the amphiphilic polypeptide.20 For this morphology transformation, the amphiphilic polypeptide was needed to have two hydrophilic poly(Sar) chains per one hydrophobic helix to tolerate partially the strong helix−helix association. However, [(Sar)m]2-His-(Leu-Aib)6 kept the rolledReceived: December 13, 2013 Revised: January 9, 2014 Published: January 11, 2014 1022

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sheet morphology at neutral and acidic conditions, suggesting that the helix−helix association in the molecular assemblies of this A2B-type peptide was still too strong to induce a drastic pH-responsive morphology change. In the present study, we increased the number of hydrophilic (Sar)m chains attached to one hydrophobic helix up to 3, [(Sar)m]3-(His)n-(Leu-Aib)6 (Figure 1), with expectation to

Article

EXPERIMENTAL SECTION

Materials. The amphiphilic polypeptides, S263His2L12 and S233HisL12, were synthesized according to Schemes S1 and S2 of the Supporting Information, respectively. The synthetic details are described in the Supporting Information. All reagents and solvents were purchased commercially and used as received unless otherwise noted. The sarcosine N-carboxy anhydride (Sar NCA) monomer was purified just before polymerization according to the conventional procedures. Preparation of Molecular Assembly. Molecular assemblies were prepared by the film hydration technique with using buffers of 10 mM Tris-buffered saline (TBS, pH 7.4) and a 10 mM citrate-buffered saline (CBS, pH 5.0 and 3.0). Sonication for 5 min with a bath-type sonicator (Bransonic 2510J-MTH) was employed for obtaining peptide aqueous solutions (0.5 mg/mL), which were heated by an aluminum heat source if necessary, followed by cooling to room temperature for measurements. Transmission Electron Microscopy (TEM). TEM images were taken using a JEOL JEM-2000EXII at an accelerating voltage of 100 kV. Peptide aqueous solutions were applied on a carbon-coated Cu grid, and the samples were negatively stained with 2% uranyl acetate, followed by suction of the excess fluid with a filter paper. Platinum−Palladium Shadowing for Transmission Electron Microscopy (TEM). Peptide aqueous solutions were applied on a carbon-coated Cu grid, and the grid was put on the water droplet (200 μL) for 2 min 3 times, followed by suction of the excess fluid with a filter paper. Unidirectional platinum−palladium shadowing was performed at an angle of 30°. The samples were directly transferred into TEM to be subjected to evaluation of the handedness of the helical ribbons correctly. pH Titration. The amphiphilic peptides (1.0 mg), S233HisL12 or S263His2L12, were dispersed in 0.5 mM HCl solution containing 150 mM NaCl (1 mL), and the dispersions were heated at 70 °C for 6 h under a N2 atmosphere. The titration curves were obtained by monitoring the pH increase as a function of the amount of 1.0 mM NaOH (pH 11) solution added. The pH measurements were performed by using a Metrohm 808 Titrando equipped with a unitrode of Pt 1000 under a N2 atmosphere. pKa values were obtained using the equipped software, which evaluates the midpoint between inflection points in the titration curves as pKa.

Figure 1. Chemical structures of S233HisL12 and S263His2L12.

observe a distinctive morphology change by a pH change because of the weakened helix−helix interaction. Indeed, we observed here morphology changes between twisted ribbon, helical ribbon, and nanotube according to His numbers and pH changes. These chiral ribbons are here to discuss the relation of the helix−helix association strength and their morphologies. Elucidation of the self-assembling mechanisms and morphology control should be the key to application of peptide materials for biology-inspired nanodevices,21−23 templates for mineralization,24−26 and functional biomaterials.27

Figure 2. TEM images of molecular assemblies prepared from (a−f) S263His2L12 and (g and h) S233HisL12. The molecular assemblies were prepared in 10 mM TBS (pH 7.4, a and b) and in 10 mM CBS (pH 5.0, c and d; pH 3.0, e−h) (0.5 mg mL−1) by the film hydration technique with a heat treatment at 70 °C for (a, c, e, and g) 1 h, (d, f, and h) 6 h, and (b) 18 h. The assemblies were negatively stained with uranyl acetate. Bars indicate 200 nm. 1023

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Supporting Information). Upon subsequent heating at 70 °C for 1 h, S263His2L12 also formed curved sheets of ca. 100 nm size, which were the same as that in pH 7.4 (Figure 2c). After heating for another 5 h, curved sheets were unusually developed into helical ribbons with ca. 92 nm length, ca. 58 nm diameter, and ca. 39 nm width (Figure 2d and panels a−c of Figure 4). By heating for 18 h in total, helical ribbons were elongated to ca. 170 nm length while keeping ca. 52 nm diameter and ca. 39 nm width (panels d−f of Figure 4). Notably, nanotubes observed at pH 7.4 could not be found at pH 5.0 even after 12 h of heating. Even though we cannot rule out the possibility that the different buffers could affect the morphology, the morphology difference between pH 7.4 and 5.0 should be ascribed to some protonation of two His residues at pH 5.0, which generates positive charges at the boundary region of the hydrophilic and hydrophobic blocks of S263His2L12. As a result, the edges of curved sheets should be hindered to stick together into nanotubes because of the electrostatic repulsions, but they should be allowable to grow into helical ribbons. Unidirectional platinum−palladium shadowing of the helical ribbons showed a uniform left-handedness (panels a and b of Figure 6). The helical pitch/diameter ratios of helical ribbons composed of S263His2L12 and S233HisL12 were ca. 1.0 and ca. 1.2, respectively. The hydrophobic (L-Leu-Aib)6 helix is righthanded and has the bulky isobutyl side chains of the six Leu residues, which can be divided into two groups. Three isobutyl groups of each group form a line on the helix surface in a lefthanded sense. The three isobutyl groups highlighted in green of the front side helix (Figure 6c) provide three pockets to accommodate the three isobutyl groups highlighted in orange of the back-side helix. For this type of helix association, the helix axis should tilt in a counterclockwise way, which leads to the left-handed twist of the planar molecular assemblies. When S263His2L12 was dispersed at pH 3.0 in CBS, twisted ribbons of ca. 279 nm length and ca. 18 nm width were observed by TEM (panels a and b of Figure 5; see Figure S2c of the Supporting Information). Upon subsequent heating at 70 °C for 1 h, S263His2L12 formed twisted ribbons of ca. 282 nm length and ca. 23 nm width (Figure 2e and panels c and d of Figure 5). After heating for another 5 h, twisted ribbons were elongated to ca. 372 nm length while keeping ca. 26 nm width (Figure 2f and panels e and f of Figure 5). S263His2L12 therefore yielded twisted ribbons with saddle-like curvatures as a thermodynamically stable morphology at pH 3.0. The effect of medium pH on the morphology of S263His2L12 molecular assemblies was analyzed in depth with changing pH by intervals of pH 0.2 ranging from pH 6.0 to 3.0. S263His2L12 was dispersed in these pH buffers by sonication, followed by heating at 70 °C for 12 h (Figure 7). Surprisingly, morphology transformation from nanotubes to helical ribbons occurred sharply between pH 5.2 and 5.0. Similarly, transformation from helical ribbons to helical tubes was observed with lowering from pH 4.6 to 4.2. These sharp transitions in morphologies are reflecting that S263His2L12 self-assembles homogeneously because of the regular packing of helices, where the degree of protonation of two His residues should control the helix packing, leading to those morphology changes according to the medium pH. S233HisL12, which is another A3B-type amphiphilic helical peptide but with one His residue, formed planar sheets of ca. 125 nm size as a major morphology at pH 7.4 and 5.0 after heating at 70 °C for 6 h (see panels a and b of Figure S3 of the

Fourier Transform Infrared Spectroscopy/Attenuated Total Reflection (FTIR/ATR). The amphiphilic peptide (0.5 mg) was dispersed in the buffer (50 μL). The dispersion was lyophilized, and then D2O was added for the H/D exchange. The dispersion was spread onto the germanium ATR crystal in dry air to obtain a peptide film. Infrared transmission spectroscopy of the molecular assembly film was performed on a Fourier transform infrared spectrometer (Nicolet 6700 FT-IR, Thermo Fisher Scientific, Waltham, MA) at room temperature in dry air.

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RESULTS AND DISCUSSION Morphology Analysis by TEM. When S263His2L12 was dispersed at pH 7.4 in TBS, small sheets of ca. 20 nm size were observed by TEM (see Figure S2a of the Supporting Information). Upon subsequent heating at 70 °C for 1 h, curved sheets of ca. 90 nm size became dominant (Figure 2a), which grew into tubular structures of ca. 110 nm in length and ca. 45 nm in diameter with heating for another 11 h (panels a and b of Figure 3). The tubular structures were finally

Figure 3. Histogram of the (a and c) length and (b and d) diameter of tubular structures prepared from S263His2L12. The tubular structures were prepared in pH 7.4 TBS with heating at 70 °C for (a and b) 12 h and (c and d) 18 h.

elongated to ca. 160 nm by heating for 17 h in total with keeping the diameter at ca. 45 nm (Figure 2b and panels c and d of Figure 3). Without heating, the molecular assemblies maintained the morphology at least for several days at room temperature. S263His2L12 nanotubes therefore extended the tube length with a longer heating time, which was different from the nanotube formation of the AB-type amphiphilic peptide, (Sar)25-b-(Leu-Aib)6 (S25L12), which transformed the morphology directly from curved sheets to nanotubes.10 However, S263His2L12 could form curved sheets even though the size was smaller than S25L12, suggesting that the chiral helices, despite the bulky hydrophilic group, were packed tightly in a consecutive tilted manner similar to S25L12.10,19,20,28 S263His2L12 thus keeps the high association ability of the helix block, which may be attributable to the elongation of the hydrophobic helix block from (Leu-Aib)6 to His2-(Leu-Aib)6 at pH 7.4, resulting in strengthening the helix− helix association to overcome the steric hindrance of the bulky A3 moiety in the molecular packing. When S263His2L12 was dispersed at pH 5.0 in CBS, small sheets of ca. 35 nm size were observed (see Figure S2b of the 1024

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Figure 4. Histogram of the (a and d) length, (b and e) diameter, and (c and f) width of helical ribbons prepared from S263His2L12. The helical ribbons were prepared in pH 5.0 CBS with heating at 70 °C for (a−c) 6 h and (d−f) 12 h.

at pH 3.0 in CBS, the initially formed small sheets of ca. 23 nm size (see Figure S2d of the Supporting Information) were transformed to helical ribbons of ca. 145 nm length, ca. 87 nm diameter, and ca. 83 nm width upon subsequent heating at 70 °C for 1 h (Figure 2g and panels a−c of Figure 8). Even though the helical ribbons were a major fraction, small sheets still account for a ca. 10% fraction. After heating for another 5 h, helical ribbons were elongated to ca. 150 nm length while keeping ca. 87 nm diameter and ca. 85 nm width. No nanotubes were observed (Figure 2h and panels d−f of Figure 8). The main difference of S233HisL12 from S263His2L12 is short of one His residue. The molecular length of the three hydrophilic blocks was not so influential on morphology as the hydrophobic helix block,28 because poly(sarcosine) chains take random-coil conformation. The lack of nanotube observation with S263His2L12, therefore, can be ascribed to the formation of relatively planar sheets, which should reflect weaker helix association in self-assemblies of S233HisL12 than S263His2L12. Indeed, circular dichroism (CD) measurements revealed that the apparent helix content of S233HisL12 at pH 7.4 was 29%, which was lower than 38% of S263His2L12 (see Figure S4 of the Supporting Information; these helix contents are considered to be estimated lower than the real helix contents because the cotton effects somehow became weak in the molecular assemblies). The longer the helical block, the stronger the helix association. On the other hand, S233HisL12 at pH 3.0 formed helical ribbons, which is in contrast to twist ribbons of S263His2L12. The morphology transformation of S263His2L12 from helical ribbons at pH 5.0 to twisted ribbons at pH 3.0 is ascribed to weaken helix association at pH 3.0 because of charge generation of two protonated His residues at pH 3.0. However, in the case of S233HisL12, the charge generation at pH 3.0 was limited to one His residue, which may remain in the helix association stable enough for S233HisL12 to take the morphology of helical

Figure 5. Histogram of the (a, c, and e) length and (b, d, and f) width of twisted ribbons prepared from S263His2L12. The twisted ribbons were prepared in pH 3.0 CBS (a and b) before heat treatment and after heating at 70 °C for (c and d) 1 h and (e and f) 6 h.

Supporting Information). No nanotubes were found, suggesting that the nanotube morphology was not attainable because the sheets were relatively flat and not curving. On the other hand, 1025

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ribbons at pH 3.0. In either pH, the difference of one His residue resulted in a drastic change in their morphologies. pKa Value of His in Molecular Assembly. pKa values of the His residue in the molecular assemblies were determined by pH titration analyses with using molecular assemblies prepared at pH 3.0. pKa values of S233HisL12 and S263His2L12 were determined to be 6.0 and 5.8, respectively (see Figure S5a of the Supporting Information). These pKa values are lower than that of Ac-His-NHMe of 6.5.20 The lower shift of His pKa in the molecular assemblies can be interpreted as a result of suppression of charge production in molecular assemblies. The lower pKa of S263His2L12 than S233HisL12 can be explained similarly. The simultaneous protonation of two His residues should be hindered more than that of a single His residue. Protonation of S263His2L12, therefore, required a more acidic condition. Using these pKa values, we estimated the degree of His protonation (αH+) at each pH according to the Henderson− Hasselbach equation (see Figure S5b of the Supporting Information)20,29 as follows: αH+ of S233HisL12, 4% at pH 7.4, 91% at pH 5.0, and 100% at pH 3.0; αH+ of S263His2L12, 2% at pH 7.4, 86% at pH 5.0, and 100% at pH 3.0. His residues in the molecular assemblies were thus partially protonated at pH 5.0, leading toward taking an intermediate morphology between morphologies composed of fully protonated amphiphiles and non-protonated amphiphiles. One or two His residues, therefore, play the key role to control the helix packing in the molecular assemblies, resulting in morphologies specific to the His status. Correlation between Molecular Packing and Morphology. The correlation between molecular packing in molecular assemblies and medium pH was investigated by FTIR/ATR analysis. The molecular assemblies prepared from S263His2L12 at pH 3.0 showed the wavenumbers of symmetric and antisymmetric C−H stretching bands higher than those prepared at pH 7.4 and 5.0 (Figure 9). The shift to higher wavenumber is generally supposed to be due to impairing the crystalline structure, which is consistent with our interpretation that the molecular packing of S263His2L12 in the selfassemblies prepared at pH 3.0 should become weak because of electrostatic repulsions of His residues.6,15 Similarly, those wavenumbers of S263His2L12 were higher than those of S233HisL12 in the molecular assemblies prepared at pH 3.0, where two protonated His residues should perturb the helix association more significantly than one protonated His residue in the molecular assemblies. The different strength of helix packing reasonably explains twist ribbons of S263His2L12 and helical ribbons of S233HisL12 at pH 3.0.

Figure 6. Platinum−palladium shadowed helical ribbons prepared from (a) S263His2L12 at pH 5.0 and (b) S233HisL12 at pH 3.0 in CBS. The metal was deposited in the direction of a white arrow. Bars indicate 200 nm. (c) Schematic illustration of molecular packing of right-handed helices, leading to the left-handed helical ribbons.

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CONCLUSION Novel pH-responsive A 3 B-type amphiphilic peptides, S233HisL12 and S263His2L12, having a hydrophobic helix block were designed and synthesized. S263His2L12 assembled into various morphologies, tubular structures, helical ribbons, and twisted ribbons, as thermodynamically stable morphologies in the buffers depending upon the medium pH. This is because electrostatic repulsion according to the medium pH affects the tightness of molecular packing that is reflected in the morphologies of molecular assemblies. In neutral and weakly acidic conditions, the peptides were packed relatively tightly because of weak electrostatic repulsion, and therefore, tubular structures and helical ribbons with cylindrical curvatures were favored. On the other hand, in acidic conditions, S263His2L12

Figure 7. Histogram of morphologies prepared from S263His2L12 at various pH values.

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Figure 8. Histogram of the (a and d) length, (b and e) diameter, and (c and f) width of helical ribbons prepared from S233HisL12. The helical ribbons were prepared in pH 3.0 CBS with heating at 70 °C for (a−c) 1 h and (d−f) 6 h.

molecular assemblies. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Telephone: +81-75-383-2400. Fax: +81-75-383-2401. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This study is a part of a joint research, which is focusing on the development of the basis of technology for establishing a center of excellence (COE) for nanomedicine, carried out through Kyoto City Collaboration of Regional Entities for Advancing Technology Excellence (CREATE), Japan Science and Technology Agency, a part of the project entitled “Development of PET Probe for Imaging Solid Tumors Using Nanocarriers” under the contract of Innovation Plaza Kyoto, Japan Science and Technology Agency, and a part of the Innovative Techno-Hub for Integrated Medical Bio-Imaging of the Project for Developing Innovation Systems, from the Ministry of Education, Culture, Sports, Science and Technology (MEXT).

Figure 9. Values of (◆) symmetric and (●) antisymmetric C−H stretching bands of molecular assembly films from S233HisL12 in pH 3.0 and S263His2L12 in pH 7.4, 5.0, and 3.0.

formed twisted ribbons having saddle-like curvatures because of the weakened helix association by electrostatic repulsion. Furthermore, the difference in electrostatic repulsion by only one His residue made a large influence on the molecular packing and morphology. The sharp pH response of these molecular assemblies should originate from the secondary structure of the helix and will be subjected to fabrication of new functional molecular architectures, which studies are currently in progress.

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ASSOCIATED CONTENT

S Supporting Information *

Synthetic schemes and details of S233HisL12 and S263His2L12, matrix-assisted laser desorption ionization−time of flight (MALDI−TOF) mass data of the compounds, additional TEM images, CD spectra, and pH titration curve of the 1027

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