Studies on Composition and Sequence Effects in Surface-Mediated

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Studies on Composition and Sequence Effects in Surface-Mediated Octapeptide Assemblies by Using Scanning Tunneling Microscopy Fuyang Qu,†,‡,⊥ Lanlan Yu,†,§,⊥ Hanyi Xie,†,∥ Yongfang Zheng,†,§ Jing Xu,† Yimin Zou,†,‡ Yanlian Yang,*,† and Chen Wang*,† †

CAS Key Laboratory for Biological Effects of Nanomaterials and Nanosafety, CAS Key Laboratory of Standardization and Measurement for Nanotechnology, CAS Center for Excellence in Nanoscience, CAS Center for Excellence in Brain Science, National Center for Nanoscience and Technology, Beijing, 100190, People’s Republic of China ‡ Sino-Danish College, University of Chinese Academy of Sciences, Beijing, 100049, People’s Republic of China § Department of Chemistry, Tsinghua University, Beijing, 100084, People’s Republic of China ∥ Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, 100871, People’s Republic of China S Supporting Information *

ABSTRACT: A set of the homogeneous and heterogeneous octapeptides have been studied for the composition and sequence effects on surfacemediated assemblies at liquid−solid interfaces by using scanning tunneling microscopy. The observed assembly structures on graphite surface reveal that all these peptides can form homogeneous lamella characteristics. By analyzing the distributions of lamella width and intralamella peptide strand length, it is suggested that the composition and sequence of the octapeptides consisting of tryptophan and glycine in the present experiments do not have a significant impact on the observed assembling characteristics. These results indicate that the observed assembling stability on the highly oriented pyrolytic graphite (HOPG) surface is dominated by the main chains of the octapeptides containing tryptophan and glycine, and independent of the bulky moieties of tryptophan in the sequence.



INTRODUCTION Molecular self-assembly, mediated by noncovalent interactions, is a versatile approach to fabricate nanometer-scale structures with a variety of building blocks such as synthetic compounds,1−4 DNA,5−7 and peptides.8−11 The assembly process could not only proceed in a three-dimensional environment but also occur on surfaces or interfaces. The latter has drawn considerable interest as exemplified by the studies of biocompatible implants,12,13 biosensors,14,15 and, more recently, the folding behaviors of degenerative disease related polypeptides such as amyloid β 4216 and amylin.10 The dependence of aggregation propensity on the composition and sequence of peptides in solutions is central to the mechanistic studies of amyloidal structures. Such dependence has been extensively pursued by point mutations17−19 and sequence shuffling20 and provides important insight into aggregation propensity at the level of amino acids. For example, a pronounced sequence-dependent fibrillation propensity has been recognized in peptide segments in bovine pancreatic ribonuclease A (RNase A).20 In the parallel microscopic studies on molecular assemblies, it has been reported that submolecular structures of surfacebound peptides can be identified at both liquid−solid interface and vacuum conditions by using scanning tunneling microscopy (STM).21 Meanwhile, the assembling peptides on the © XXXX American Chemical Society

surface have been demonstrated by Fourier transform infrared (FTIR) and circular dichroism (CD) spectroscopies to have β structures.22,23 A variety of core regions and key folding sites of amyloidal peptides have been recognized.10,24 Identification of amino acid residues and side chain orientations has also been achieved in STM investigations as well.25,26 Such progress in structural analytical capability contributes to revealing fine details of peptide assemblies at surfaces and interfaces. Considering that the interactions between a solid surface and peptides could inevitably affect the adsorption conformation of both the main chains and side chains of the adsorbed amino acids,27 it is genuinely interesting to investigate the composition and sequence effect on the stability of the surface-mediated peptide assemblies which could be considered complementary to the aggregation propensity in solution phase. In this work, we designed six octapeptides with varying composition and sequences (G1W, G2W, G4W, G7W, G8, and W8, shown in Figure 1). The octapetides contain only glycine and tryptophan. Since glycine has no side chain moieties, it is ideal to be the control structure in our study. On the other hand, tryptophan is selected due to its well-known strong Received: January 25, 2017 Revised: April 28, 2017 Published: April 28, 2017 A

DOI: 10.1021/acs.jpcc.7b00825 J. Phys. Chem. C XXXX, XXX, XXX−XXX

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The Journal of Physical Chemistry C

Figure 1. Molecular structures of 4Bpy, tryptophan (W), and six octapeptides (G1W, G2W, G4W, G7W, G8, and W8). The tryptophan residues in the first four peptides (G1W, G2W, G4W, and G7W) are depicted in pink.

and incubated for ∼5 min. A 20 μL volume of the resulting mixture was deposited on a freshly cleaved HOPG (grade ZYB, NTMDT, Russia) surface followed by air drying at room temperature. STM experiments were performed after the water was evaporated from the HOPG surface. STM Experiments. All STM experiments were performed with a Nanoscope IIIa scanning probe microscope system (Bruker, USA) in constant-current mode under ambient conditions. The ambient temperature is around 298 K. The tips were prepared by Pt/Ir wire (80/20). First, one end of the wire was immobilized using forceps and then was cut by pliers. In order to form a sharp tip, the angle between the wire and edge of pliers should be as small as possible and a pull action along the wire is needed in the cutting process. After the formation of a tip, it was checked by using an optical microscope to make sure that a relatively sharp tip was well prepared. Otherwise, the above operation should be repeated again. Finally, the tip was installed on the tip holder for the STM experiments. Detailed tunneling conditions are given in the corresponding figure captions. Experiments were repeated independently using different tips for reproducibility. Statistical Method. The lengths of the peptide strands in STM images were measured by using Gwyddion (Version 2.31, Czech Metrology Institute, Czech Republic). The length increment of 0.325 nm for each residue was assumed in the

aggregation propensity among 20 common amino acids28 and the inherent aromatic interactions between its indole moiety and the highly oriented pyrolytic graphite (HOPG) surface. The first four heterogeneous ones (G1W, G2W, G4W, and G7W) with sequence shuffling are composed by seven glycine residues and one tryptophan. By contrast, the other two peptides (G8 and W8) are homogeneous. To label C-termini of peptides, 4,4′-bipyridyl (4Bpy, Figure 1) molecules were introduced to coassemble with peptides to facilitate the analysis of surface-bound peptide chain structures.10 The coassembly structures of peptides/4Bpy on the HOPG surface were carefully inspected by high resolution STM in ambient conditions. Our study shows that all the peptides can assemble into β structures and the numbers of surface-bound residues are all in the range of five to seven, which is independent of their composition and sequence.



EXPERIMENTAL SECTION Sample Preparation. Peptides were obtained from Bankpeptide biological technology Co. Ltd. with purity of >98%. The 4Bpy was purchased from Sigma-Aldrich Co. Ltd. All the materials were used without further purification. Lyophilized powders of peptides were dissolved in Milli-Q water to a concentration of 0.01−0.001 mg/mL. Solid powders of 4Bpy were dissolved to a concentration of 1 mg/mL. The peptide solution (100 μL) was mixed with the 4Bpy solution (900 μL) B

DOI: 10.1021/acs.jpcc.7b00825 J. Phys. Chem. C XXXX, XXX, XXX−XXX

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considered as a venue to evaluate such an impact on the peptide adsorption stability. The lamella structures between two 4Bpy arrays correspond to the assembling peptides (as highlighted by a blue line in Figure 2a). The angle (α1) between the peptide main chain and the 4Bpy stripe orientation is measured to be 33 ± 2°. The observed stripe orientation is originated from the hydrogen bond between 4Bpy and the C-terminus of peptide similar to a previous report.29 This stripe orientation has been documented in a number of reports as characteristic and dependent on the interaction between the coassembly molecules and peptides, and significantly variant in the pristine assemblies.23,31,35 In a previous study, the circular dichroism results revealed that the secondary structure of peptides can be transformed from α-helix in solution to β-sheet on graphite surface.22 Besides, the interchain spacing of two neighboring peptides (0.45 ± 0.05 nm) on the HOPG surface revealed by STM is also consistent with the β-sheet structural features.16 In another study, the spacing of two adjacent peptide chains in the peptide/4Bpy coassemblies (0.54 ± 0.02 nm) was still within the separation range of hydrogen bonds and implies the formation of β-sheet structure. Based on this observation, the folding sites of islet amyloid polypeptide (IAPP) analogues were thereby identified.10 Meanwhile, the parallel β-sheet structure in the peptide Q11/4Bpy coassemblies on the HOPG surface was further confirmed by using FTIR spectra.23 Similar to the previous structural features of peptide assemblies, the interchain spacing of two neighboring peptides in Figure 2a was measured to be 0.50 ± 0.02 nm, which can be plausibly assigned to the formation of hydrogen bonds and further the β structure. Considering the identification of C-termini of peptides by 4Bpy, the peptide length of C-terminal strands can be determined in the range 3.575−4.225 nm as depicted in Figures 2b and 3, with the most probable length of the Cterminal strands ca. 3.9 nm by Gaussian fitting. Since the separation between two neighboring residues is 0.325 nm in

statistical histograms of the peptide length distribution. All the statistical histograms were fitted by Gaussian distribution.



RESULTS AND DISCUSSION The molecule 4Bpy was introduced to coassemble with the peptides, similar to the previous investigations.10,24 Figure 2a

Figure 2. (a) High resolution STM image of the coassembly structures of G1W/4Bpy (scale bar = 2.0 nm). The angle (α1) between the peptide main chain and the 4Bpy stripe orientation was measured to be 33 ± 2°. Tunneling condition: I = 250 pA; V = 699.8 mV. The red and blue lines highlight the 4Bpy arrays and peptide chains, respectively. The yellow arrows designate the dim parts between two neighboring peptide strands. (b, c) Statistical histograms of the peptide length of C-terminal strands of G1W measured from the STM image. The gray curves represent the Gaussian fit to the histograms. The measurements of peptide length were carried out on the two neighboring peptides aligning in a head-to-head manner on the HOPG surface (b) or one of them (c). (d) Schematic model of the coassembly structures of G1W/4Bpy on the HOPG surface. The red arrows stand for the peptides, and their directions mean the peptides from amino termini to carboxyl termini. The molecular models on both sides of the arrows are the 4Bpy molecules. Color code: cyan for C; blue for N. The hydrogen atoms are omitted in the models.

shows the STM image of the coassembly structures of peptide G1W and 4Bpy on the HOPG surface. Close inspection of the image reveals that the linear bright arrays (as highlighted by a red line in Figure 2a) could be ascribed to the 4Bpy molecules. The contrast of 4Bpy moieties in this STM is in full agreement with the previous report.29 The consistency in the observed dimension and geometry of the topography features in both studies is supportive of the assignment of 4Bpy moieties. The C-terminal of peptides could be identified and immobilized due to the formation of hydrogen bonds between carboxyl groups of peptides and nitrogen atoms of 4Bpy molecules.30,31 The hydrogen bond, essentially, is an electric dipole−dipole interaction with a strength of approximately 5−10 kBT for each bond at 298 K.32 The thermal fluctuation is unlikely to disrupt these hydrogen bonds (N···H−O) until 168 °C, which has been verified by variable-temperature Fourier transform infrared (FTIR) spectroscopy.33 It should be noted that heterogeneity in the octapeptide sequence may be associated with possible solvophobic effects originating from the polarity differences in solvents and side chain moieties, which could affect the adsorption dynamics of molecules.34 The observations of the peptide strands in the assembly structures can be

Figure 3. Statistical histograms of the peptide length of C-terminal strands of six octapeptides (G1W, G2W, G4W, G7W, G8, and W8) measured from the STM images. The gray curves represent the Gaussian fit to the histograms. The measurements of peptide length were carried out on the two adjacent peptides aligning in a head-tohead manner on the HOPG surface. C

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The Journal of Physical Chemistry C parallel β-sheet structures,36 the number of surface-bound residues for the C-terminal peptide strands could be assigned to be in the range of 11−13. In view of the peptide G1W only consisting of eight residues, it can be reasonably concluded that the two neighboring peptides could align in a head-to-head manner with their N-termini approaching, and thereby the number of residues involved in the assembly was assigned to be between five and seven in each peptide. As shown in Figure 2a, the yellow arrows designate the dim portions where the Ntermini of peptide strands get close to each other. The measurement of the peptide length of C-terminal strands was also carried out on each peptide strand. The histogram in Figure 2c gives the range of probable length of C-terminal strands, that is, 1.625−2.275 nm, which reveals the number of surface-bound residues is in the range of five to seven, consistent with the result from the measurement of C-terminal strands for pairs of two neighboring peptides. The two relatively short columns located at two sides of the highest one in Figure 2c indicate the fluctuations of N-terminal residues sticking on the HOPG surface. Based on the above discussion, the rational structural model was proposed in Figure 2d. The red arrows stand for the parallel β structures formed by the surface-bound peptide residues which can be observed by STM. Comparing with G1W/4Bpy, peptide G2W and 4Bpy could also coassemble to the resembling structures (Figure 4).

adsorption of the bulky side groups of W on the surface could result in the bend of peptides like beams and therefore makes the assembling system unstable. Likewise, the peptide G4W and G7W also exhibit β structures on the HOPG surface as shown in Figures 5 and

Figure 5. High resolution STM image of the coassembly structures of G4W/4Bpy (scale bar = 3.0 nm). The angle (α3) between the peptide main chain and the 4Bpy stripe orientation was measured to be 38 ± 3°. Tunneling conditions: I = 400.0 pA; V = 600.0 mV.

Figure 4. High resolution STM image of the coassembly structures of G2W/4Bpy (scale bar = 3.0 nm). The angle (α2) between the peptide main chain and the 4Bpy stripe orientation was measured to be 31 ± 2°. Tunneling conditions: I = 150 pA; V = 699.8 mV. Figure 6. High resolution STM image of the coassembly structures of G7W/4Bpy (scale bar = 3.0 nm). The angle (α4) between the peptide main chain and the 4Bpy stripe orientation was measured to be 38 ± 3°. Tunneling conditions: I = 399.8 pA; V = 749.8 mV.

According to the statistical histogram of peptide length of Cterminal strands in Figure 3, the probable number of surfacebound residues for peptide G2W is also in the range of five to seven. Meanwhile, the proportions of peptide length in different ranges corresponding to Figure 3 are summarized in Table S1. As observed in the STM images (Figures 2a and 4), the two sequences (G1W and G2W) have similar β motifs. The side groups of tryptophan (W) have the possibility to point toward the graphite surface and interact via hydrophobic and π−π interactions. For most peptides in the assemblies, the number of surface-bound peptide residues is still in the range of five to seven. It could be presumed that the energy of thermal fluctuations is capable of overcoming the interactions between the indole ring of W and the graphite surface. Besides, the

6. The statistical histograms of peptide length of C-terminal strands of G4W and G7W (Figure 3) indicate that the probable values are all 3.575−4.225 nm and the corresponding numbers of surface-bound residues are five to seven. It should be noted that the side group of the residue tryptophan (W) in the assembly structures could adopt two configurations where the indole moiety points to the solvent or approaches the graphite surface. If the side group of W points to the solvent, it would be indiscernible in this STM observation. As depicted in Figure 1, the two carbon−carbon single bonds of W rotate freely due to the thermal motion and the absence of neighboring steric D

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The Journal of Physical Chemistry C hindrance, which could make the indole moiety unobservable by using STM. In another case, the side chain of W can interact with the graphite surface. In the coassembling structures of 4Bpy/G7W, if the indole moiety points toward the graphite surface, the ordered assembly structures of peptide G7W suggest that the bulky side group of W neighboring C-terminal has a minor effect on the formation of hydrogen bonds between carboxyl groups of peptides and nitrogen atoms of 4Bpy molecules. The above four peptides (G1W, G2W, G4W, and G7W) with the same composition (seven glycine residues and one tryptophan residue) but different sequences display similar β structures and have the same number of surface-bound peptide residues, which has been clearly demonstrated in Figure 3. This suggests that the residue tryptophan has limited mediation effect on the assembly structures though the indole moiety of W has the steric hindrance and variant conformations in the peptide assemblies. More importantly, these results indicate that the assembly structures have little dependence on their sequences. As control sequences for this study, the assembly structures of two homogeneous octapeptides (G8 and W8) were observed by using STM as shown in Figures 7 and 8. The assembly

Figure 8. High resolution STM image of the coassembly structures of W8/4Bpy (scale bar = 3.0 nm). The angle (α6) between the peptide main chain and the 4Bpy stripe orientation was measured to be 33 ± 2°. Tunneling conditions: I = 400.0 pA; V = 699.8 mV.

the rationality of the observed assembling characteristics of the four sequences (G1W, G2W, G3W, and G4W) where they all have the same number of surface-bound residues. Moreover, the phenomena that all the heterogeneous and homogeneous peptides involved here form the β structures and have the same number of surface-bound residues on the HOPG surface imply the inherent structural stability of the octapeptides that may be correlated to the persistence effect in oligomeric molecules.



CONCLUSIONS In summary, the assembly structures of six model peptides have been investigated at the submolecular level by using STM. The results demonstrate that all the peptides involved here could assemble to β structures and the numbers of surface-bound residues are all in the range of five to seven. This work indicates an inherent structural stability that can be plausibly attributed to the main chains of these octapeptides consisting of tryptophan and glycine alone with little dependence on the bulky groups of tryptophan when assembling on the HOPG surface.

Figure 7. High resolution STM image of the coassembly structures of G8/4Bpy (scale bar = 3.0 nm). The angle (α5) between the peptide main chain and the 4Bpy stripe orientation was measured to be 37 ± 3°. Tunneling conditions: I = 299.1 pA; V = 700.0 mV.



ASSOCIATED CONTENT

S Supporting Information *

structures of peptide G8 are stabilized by the weak van der Waals forces between peptide backbones and the graphite surface. However, the side groups of peptide G8 are only hydrogen atoms which could interact with the HOPG surface via the C−H···π interactions, which can be classified as weak hydrogen bonds.37 Consequently, it is plausible to explore the impact of side chain moieties on surface assembling structures by replacement of glycine with other amino acid residues, such as tryptophan (W). Specifically, in the formation of parallel β motifs of W8, half of the indole moieties could be adsorbed onto the graphite surface via π−π stacking and hydrophobic interaction. The STM observations concluded that the overall assembly structures of both G8 and W8 peptides can be stabilized on the HOPG surface. Nevertheless, the probable numbers of surfacebound residues of peptide G8 and W8 (Figure 3) are still in the range of five to seven observed by using STM, which suggests

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcc.7b00825. Statistical length distribution of six octapeptides corresponding to Figure 3 (PDF)



AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. Fax: +86 10 62656765. Tel.: +86 10 82545559. *E-mail: [email protected]. Fax: +86 10 62656765. Tel.: +86 10 82545561. Author Contributions ⊥

F.Q. and L.Y. contributed equally to this work.

Notes

The authors declare no competing financial interest. E

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ACKNOWLEDGMENTS This work was supported by the National Basic Research Program of China (2013CB934200) and the National Natural Science Foundation of China (91127043, 21332006). Financial support from the CAS Key Laboratory for Biological Effects of Nanomaterials and Nanosafety is also gratefully acknowledged.



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DOI: 10.1021/acs.jpcc.7b00825 J. Phys. Chem. C XXXX, XXX, XXX−XXX