Interactions of Glycopolymers with Assemblies of Peptide Amphiphiles

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The Interactions of Glycopolymers with Assemblies of Peptide Amphiphiles via Dynamic Covalent Bonding Jue Wang, Zhenfei Gao, Wenjing Qi, Yu Zhao, Pan Zhang, Mingchang Lin, Zhiming Li, Guosong Chen, and Ming Jiang ACS Biomater. Sci. Eng., Just Accepted Manuscript • DOI: 10.1021/acsbiomaterials.7b00642 • Publication Date (Web): 03 Oct 2017 Downloaded from http://pubs.acs.org on October 3, 2017

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ACS Biomaterials Science & Engineering

The Interactions of Glycopolymers with Assemblies of Peptide Amphiphiles via Dynamic Covalent Bonding Jue Wang, a Zhenfei Gao, a Wenjing Qi, a Yu Zhao, a Pan Zhang, a Mingchang Lin, a Zhiming Li, b

Guosong Chen *a and Ming Jiang a

a. The State Key Laboratory of Molecular Engineering of Polymers and Department of Macromolecular Science, Fudan University, 220 Handan Road, Shanghai 200433, China. E-mail: [email protected]. b. Department of Chemistry, Fudan University, 220 Handan Road, Shanghai 200433, China.

ABSRACT: In this work, peptide amphiphile (PA) with benzoboroxole (BOB) group at the hydrophilic end was prepared and assembled into fibers (PAA) with BOB group on the fiber surface. Then glycopolymer with mannopyranoside as pendent group interacted with the PAA via dynamic covalent bond between sugar and BOB. By combining the results from 2D 1H NMR spectroscopy, the exact binding mode of mannopyranoside pendent group and BOB, i.e. mannopyranoside participated by its diol on 2,3-position instead of that on 4,6-position, which was clearly observed on the fiber surface. The success in determining this binding mode in macroscopic material was due to the high density of BOB on PAA and the multivalent effect between the multiple BOB moieties on fiber surface and repeating mannopyranoside groups of the glycopolymer.

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KEYWORDS: glycopolymer, dynamic covalent bonds, peptide amphiphile, assembly

INTRODUCTION Glycopolymers,1 as a nice mimic of various glycoconjugates, i.e. polysaccharides, proteoglycans, glycolipids and glycoproteins,2 are very promising building blocks for biocompatible materials. To construct responsive biomaterials by using glycopolymers, sugar-involved dynamic covalent bonds (DCB) have been employed, among which the interaction between sugar and benzoboroxole (BOB) is the most common one. As a derivative of phenylboronic acid, BOB is featured by forming DCB with non-reducing saccharides at neutral pH, which has great potential in bioapplications. By examining a series of reference compounds and semi-empirical simulation, Hall et al proposed possible binding modes between BOB and monosaccharides in 2006, i.e. cis-1,2-diol of monosaccharide tends to form five-membered ring with BOB, while 1,3-diol forms six-membered ring, and the former was more stable than the latter. Afterwards, BOB or phenylboronic acid has been integrated onto polymers and this kind of DCB has been effectively employed to construct various responsive materials.3-5 For example, in our previous study, gelation ability between glycopolymers containing different monosaccharides (mannose, galactose and glucose) as pendent groups with BOB was compared.6 The mannose-containing polymer gave the highest modulus and viscosity of the hydrogel followed by that of the galactose-containing and then the glucose-containing polymers. This observation was explained by the possible binding modes, i.e. five-membered ring or six-membered ring between different sugars and BOB. However, we noticed that although the DCB between BOB or even its more


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popular derivative phenylboronic acid and sugars have been widely used in construction of sugar-responsive materials in literature, it is not clear whether the DCB follows the proposed binding mode at small molecular level or not, no direct experimental evidence in polymeric

Figure 1. Scheme of the assembly of peptide amphiphile (PAA), PMan and the DCB between PAA and PMan. materials was found in literature. To investigate the binding modes of BOB with saccharides in bulky materials, 2D 1H NMR technique, e.g. Nuclear Overhauser Effect Spectroscopy (NOESY) seems to be a powerful tool since it could detect atoms that are in close proximity to each other (< 5 Å). However, the crossing peaks are usually too weak to be detected in polymeric materials, as the signal could be easily disturbed by others. As a possible solution to this problem, the BOB/saccharide pair needs to be aligned and exposed to solvent with low molecular mobility. Thus in this work, peptide amphiphile (PA) carrying BOB was selected to form a scaffold. PA typically comprises a


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hydrophilic peptide sequence with attached lipid chains, favors to self-assemble into nano-belts or nano-fibers, which is a class of well-known pH-dependent, biocompatible and biodegradable nanostructures.7-9 Inspired by this design, in this work, PA is modified with BOB at the end, thus BOB could be exposed on the surface of the fibers after self-assembly. Then after addition of glycopolymer, the BOB-containing PAA could interact with glycopolymer via dynamic covalent bond. The BOB-modified PAA has a better solubility compared to the BOB-containing polymer in our previous work, thus it is benefit to research the binding mode of DCB directly by 2D 1H NMR techniques. Herein, the PAA will bind glycopolymers via DCB between mannopyranoside (Man) and BOB. Direct evidence on the binding mode between Man and BOB is provided by 2D 1H NMR. A combination of 2D 1H NMR techniques and molecular simulation showed that BOB and Man adapted the five-membered ring binding mode rather than the six-membered ring on the surface of PAA. This DCB bonding on nanofiber surface was also supported by UV-vis and fluorescence spectra. METHODS Syntheses of PMan and PA. In this work, glycopolymer (PMan) and PA were designed and synthesized (Figure 1, Scheme S1 and Scheme S2). PMan was prepared via post-polymerization modification. Briefly, poly(glycidyl methacrylate) (PGMA) (Mw, GPC = 2.2 × 104, PD.I. = 1.3, Figure S1 and Table S1) was synthesized via Free Radical Polymerization, then 1-thiol-α-Dmannopyranoside10 attacked the epoxide ring affording PMan (Mw = 3.5 × 104, 85%). PA was synthesized via several amino couplings and reduction, which was comprised by three parts: an eighteen-carbon alkyl chain, which aggregated as a core of assembly in aqueous solution; a


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peptide middle segment EFEFE (E: glutamic acid residue, F: phenylalanine residue), forming βsheet structure11-12 to make PAA stable; BOB as a terminal group, binding with the mannose derivative of PMan. Preparation of PAA. After synthesis PA was treated with trifluoroacetic acid (TFA) for 30 min at 25 °C and TFA was removed by rotary evaporator. Then PA was quickly dissolved in PBS buffer (pH 8) with an ultrasonic treatment at 50 °C for 30 min. This sample cooled down at room temperature for the incubation of PAA. RESULTS AND DISCUSSION In PBS buffer (pH 8), PA (15 mg/mL) was incubated for self-assembly for 8 h. As shown in Figure 2, long, fibrous structures with a diameter around 20 nm were observed under cryogenic Transmission Electron Microscope (cryo-TEM) (Figure 2a, b). Similar morphology was also observed under Transmission Electron Microscope (TEM) (Figure 2c). Under Atomic Force Microscope (AFM), the height of the fibrous structure was measured as 5 nm, indicating a

Figure 2. Images of PAA with or without PMan in PBS (0.2 M, pH 8). (a, b) cryo-TEM images of PAA (13 mM). TEM images of PAA (13 mM) in the (c) absence or (d) presence of PMan (148 mM).


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bilayer structure of PAA (Figure S4).8 Following the well-accepted models for these assemblies,7-8 we suppose that the alkyl chains are packed inside while BOB groups are on the surface of PAA. Both the hydrophobic interaction of the eighteen-carbon alkyl chain, and the formation of β-sheet peptide secondary structure are the driving forces for the assembly. In Fourier transform infrared (FT-IR) spectrum (Figure S5), the peak at 1632 cm-1(C=O, amide I) indicates the formation of β-sheet,7, 13-14 while a shoulder peak at about 1641 cm-1 may result from the transition from β-sheet to helix on the edge of PAA. A red shift of -COOH peak from 1720 cm-1 to 1697 cm-1 showed the effect of hydrogen bonding.13 Meanwhile, fluorescence emission spectra (Figure S6) of Thioflavine T (ThT) in PBS solution showed an emission at about 490 nm, indicating the insertion of ThT to the β-sheet of the PAA.15-16 In addition, the βsheet structure was also confirmed by a negative peak at 200 nm in Circular dichroism (CD) spectrum (Figure S7).7 To bind PAA with PMan, the two components were mixed together (the molar ratio of BOB/Man moieties, 1:11), which was employed in our previous study.6 We found that under TEM, the surface of PAA became rough compared to the PAA itself without PMan (Figure 2d). Then to characterize the existence of DCB, 11B NMR should be the first choice, as in literature, it has been used on polymers.17 But in the present case, the low abundance of boron in PA makes this technique not practical. NOESY18-20 is known to be powerful to characterize the neighboring atoms in close proximity. Thus we tried to understand the possible binding mode between Man and BOB in the mixed PAA system by using NOESY. To achieve this goal, it was necessary to complete the determination of protons on the pyranose ring of Man from PMan by means of total correlation spectroscopy (TOCSY), as the normally used correlation spectroscopy (COSY) was not effective. Careful analysis on TOCSY data


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presents information on two neighbouring protons along a covalent structure (Figure 3a), and all the peak assignments on the sugar ring are shown in Table 1 (TOCSY 1). To prove this result, a longer mixing time (τm) was employed in the TOCSY experiment and similar results were obtained (Figure S8, TOCSY 2 in Table 1). Our result from TOCSY is similar to the result in literature (Table 1, Line 3).19 Table 1. Chemical shifts of protons on the mannose ring of PMan. H1

H2

H3

H4

H5

TOCSY 1

5.33

4.04

3.74

3.65

3.94

TOCSY 2

5.34

4.07

3.77

3.68

3.95

D2*

5.04

4.06

3.84

3.64

3.73

* Determination of protons of a mannopyranoside with similar chemical surroundings from literature.19

Based on the determination of TOCSY 1, NOESY measurements of PAA were performed in the presence and absence of PMan. As shown in Figure 3, the mixture of PAA and PMan showed

Figure 3. (a) TOCSY spectrum (τm = 30 ms) of PMan in D2O. NOESY spectrum of (b) PAA/PMan (13 mM/148 mM) and (c) PAA (13 mM). Crossing peaks in (b) state that cis-2,3ACS Paragon Plus Environment diol is the probable binding mode.

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two crossing peaks, which indicated the correlation between Hα of BOB at 7.22 ppm with H2 (4.04 ppm) and H3 (3.74 ppm) on the mannopyranoside ring. The result demonstrated that the distance between Hα of BOB and H2 or H3 from Man was less than 5 Å, which clearly supported the five-member ring mechanism formed by the cis-1,2-diol of mannose. Meanwhile, crossing peaks between H4/H5 of Man and Hα of BOB were not observed, indicating the 4,6diol was probably not possible. As a control, PAA itself did not give any crossing peaks in the absence of PMan. To further confirm the results from NOESY, molecular simulation21 was employed to investigate the binding mode. PMan and PAA were simplified into two small molecules, i.e. Reactant 1 (R1) and Reactant 2 (R2) respectively (Figure 4a). Ground-state geometry optimization (B3LYP23, 22 Gaussian 092423) was performed for the proposed cis-2,3-diol and 4,6-diol complexes between R1 and R2. Considering the boron atom in the complex is stereogenic, both

Figure 4. (a) Chemical structures of R1 and R2. (b-e) Calculated results of complexes formed by R1 (PMan) and R2 (PA). ACS Paragon Plus Environment

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epimers are calculated for each complex (denoted as α-aryl and β-aryl). The potential energy of 4,6-diol complexes is significantly higher than cis-2,3-diol complexes, so cis-2,3-diol (Figure 4b, 4c) is much more favorable than 4,6-diol (Figure 4d, 4e) in the complex formation. In α-aryl form of cis-2,3-diol with lowest energy, the distances from Hα to H2 and H3 are found to be 3.225 and 4.405 Å respectively, which is in accordance with the result of NOESY. The other data i.e. simulated distances are shown in supporting information (Table S2). To understand the results from DCB of PAA/PMan with NOESY, the corresponding small molecular reactants i.e. benzeneboronic acid hemiester hydrochloride (ABOB) and Man are employed for further NOESY study. The result of ABOB/Man, shows that no crossing peaks appearing between the protons of ABOB and Man at the same concentration as that for the case of PAA/PMan (Figure S12). These results imply that the assembly structure of PAA and Man

Figure 5. (a) Fluorescence emission spectra of PAA/ARS (1.0 mM/0.1 mM; blue line, 578 nm), ABOB/ARS (1.0 mM/0.1 mM; red line, 599 nm) and ARS (0.1 mM; black line) in PBS pH 8. λ = 495 nm. (b) UV spectra of PAA/ARS (1.0 mM/0.1 mM; blue line, 479 nm), ABOB/ARS (1.0 mM/0.1 mM; red line, 490 nm), ARS (0.1 mM; black line, 510 nm), PAA (1.0 mM; green line) and ABOB (1.0 mM; pink line) in PBS pH 8.


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existing in polymers might be favorable for the formation the sugar-BOB interactions. To know why only PAA/PMan exhibits crossing peaks at the right region, Alizarin Red S. (ARS) is used to explore the speciality of PAA.24 From fluorescence emission spectra, we found that ARS reacted with the BOB from the assembled PAA giving a strong emission peak at 578 nm, while ARS binds ABOB leading to a very weak peak at 599 nm (Figure 5a). At the same time, from UV spectra ARS shows a peak at 510 nm. The peak shifts to 479 and 490 nm when PAA or ABOB are added, respectively (Figure 5b). These results state that PAA shows a stronger reactive efficiency with ARS than ABOB. Because in PAA, BOB is attached on the micron-grade surfaces of the assemblies, and therefore, possess a high density there. So the reactant such as ARS can bind BOB easily and reduce the influence of the thermal motion of solvent. In other words, there is much high probability for BOB formation on PAA than that from small molecular ABOB in solution. Furthermore, glycopolymers also provides a steadily local high-density of sugar species surrounding the polymer chains. Clearly both the factors mentioned above favor the DCB formation and thus make the detection of the bonding possible by NOESY in PAA/PMan. CONCLUSIONS In this paper, we attempt to determinate the binding mode of DCB between BOB and mannoside directly. 2D 1H NMR results showed that the binding mode is cis-2,3-diol rather than 4,6-diol. This observation was further proved by molecular simulation. We believe that this result relies on the steadily local high densities of BOB and sugar, which might provide an alternative way to characterize dynamic covalent bonds directly. AUTHOR INFORMATION


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Corresponding Author * E-mail: [email protected]. ORCID Guosong Chen: 0000-0001-7089-911X Notes The authors declare no competing financial interest. ACKNOWLEDGMENT The Ministry of Science and Technology of China and the National Natural Science Foundation of China (Nos. 91527305 and 51322306) are acknowledged for their financial support. ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website. Scheme S1, synthesis route of PA (TIF); Scheme S2, synthesis route of PMan (TIF); Figure S1, GPC result of PGMA (PDF); Table S1, GPC result of PGMA; Figure S2, TEM images of PAA (13 mM in PBS, pH 8) (TIF);


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Figure S3, TEM images of PAA/PMan (13 mM/148 mM in PBS, pH 8) (TIF); Figure S4, AFM images of PAA (1 mM in PBS, pH 8) (TIF); Figure S5, FT-IR spectra of PAA (5 wt% in PBS, pH 8) (TIF); Figure S6, Fluorescence Emission spectra of PAA (5 mM) with and without ThT (60 µM). λ = 440 nm (TIF); Figure S7, CD spectra of PAA in PBS (pH 8, 0.2 mg/mL) (TIF); Figure S8, TOCSY spectrum of PMan in D2O (148 mM in PBS, pH 8) (TIF); Figure S9, NOESY spectrum of PAA/PMan (13 mM/148 mM in PBS, pH 8) (TIFF); Figure S10, NOESY spectrum of PAA (13 mM in PBS, pH 8) (TIFF); Figure S11, NOESY spectrum of ABOB/Man (13 mM/148 mM in PBS, pH 8) (TIFF); Figure S12, NOESY Spectrum of (a) PAA/PMan (13 mM/148 mM) and (b) ABOB/Man (13 mM/148 mM). Only PAA/PMan shows crossing peaks at the right region. (TIFF); Table S2, Distance between H on benzene ring and mannose ring. REFERENCES (1) Su, L.; Zhang, W.; Wu, X.; Zhang, Y.; Chen, X.; Liu, G.; Chen, G.; Jiang, M. GlycocalyxMimicking Nanoparticles for Stimulation and Polarization of Macrophages via Specific Interactions. Small 2015, 11 (33), 4191-4200.


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(2) Belardi, B.; O'Donoghue, G. P.; Smith, A. W.; Groves, J. T.; Bertozzi, C. R. Investigating cell surface galectin-mediated cross-linking on glycoengineered cells. J. Am. Chem. Soc. 2012, 134 (23), 9549-9552. (3) Kotsuchibashi, Y.; Agustin, R. V. C.; Lu, J.-Y.; Hall, D. G.; Narain, R. Temperature, pH, and Glucose Responsive Gels via Simple Mixing of Boroxole- and Glyco-Based Polymers. ACS Macro Letters 2013, 2 (3), 260-264. (4) Lu, H.; Wang, Y.; Li, L.; Kotsuchibashi, Y.; Narain, R.; Zeng, H. Temperature- and pHResponsive Benzoboroxole-Based Polymers for Flocculation and Enhanced Dewatering of Fine Particle Suspensions. ACS Appl Mater Interfaces 2015, 7 (49), 27176-27187. (5) Wang, D.; Liu, T.; Yin, J.; Liu, S. Y. Stimuli-Responsive Fluorescent Poly(Nisopropylacrylamide) Microgels Labeled with Phenylboronic Acid Moieties as Multifunctional Ratiometric Probes for Glucose and Temperatures. Macromolecules 2011, 44 (7), 2282-2290. (6) Lin, M.; Sun, P.; Chen, G.; Jiang, M. The glyco-stereoisomerism effect on hydrogelation of polymers interacting via dynamic covalent bonds. Chem. Commun. 2014, 50 (68), 9779-9782. (7) Zhang, J.; Hao, R.; Huang, L.; Yao, J.; Chen, X.; Shao, Z. Self-assembly of a peptide amphiphile based on hydrolysed Bombyx mori silk fibroin. Chem. Commun. 2011, 47 (37), 10296-10298. (8) Cui, H.; Muraoka, T.; Cheetham, A. G.; Stupp, S. I. Self-assembly of giant peptide nanobelts. Nano Lett 2009, 9 (3), 945-951.


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(9) Mumcuoglu, D.; Sardan Ekiz, M.; Gunay, G.; Tekinay, T.; Tekinay, A. B.; Guler, M. O. Cellular Internalization of Therapeutic Oligonucleotides by Peptide Amphiphile Nanofibers and Nanospheres. ACS Appl. Mater. Interfaces 2016, 8 (18), 11280-11287. (10) Martin-Santamaria, S.; Andre, S.; Buzamet, E.; Caraballo, R.; Fernandez-Cureses, G.; Morando, M.; Ribeiro, J. P.; Ramirez-Gualito, K.; de Pascual-Teresa, B.; Canada, F. J.; Menendez, M.; Ramstrom, O.; Jimenez-Barbero, J.; Solis, D.; Gabius, H. Symmetric dithiodigalactoside: strategic combination of binding studies and detection of selectivity between a plant toxin and human lectins. Org. Biomol. Chem. 2011, 9 (15), 5445-5455. (11) Rapaport, H.; Kjaer, K.; Jensen, T. R.; Leiserowitz, L.; Tirrell, D. A. Two-Dimensional Order in β-Sheet Peptide Monolayers. J. Am. Chem. Soc. 2000, 122 (50), 12523-12529. (12) Zhang, X.; Dong, C.; Huang, W.; Wang, H.; Wang, L.; Ding, D.; Zhou, H.; Long, J.; Wang, T.; Yang, Z. Rational design of a photo-responsive UVR8-derived protein and a selfassembling peptide-protein conjugate for responsive hydrogel formation. Nanoscale 2015, 7 (40), 16666-16670. (13) Zhou, Y.; Tang, H.; Wu, P. Volume phase transition mechanism of poly[oligo(ethylene glycol)methacrylate] based thermo-responsive microgels with poly(ionic liquid) cross-linkers. Phys. Chem. Chem. Phys. 2015, 17 (38), 25525-25535. (14) Hernik, A.; Pulawski, W.; Fedorczyk, B.; Tymecka, D.; Mis-icka, A.; Filipek, S.; Dzwolak, W. Amyloidogenic Properties of Short alpha-L-Glutamic Acid Oligomers. Langmuir 2015, 31 (38), 10500-10507.


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(15) Wang, S.; Cai, Q.; Du, M.; Xue, J.; Xu, H. Synthesis of 1D Silica Nanostructures with Controllable Sizes Based on Short Anionic Peptide Self-Assembly. J. Phys. Chem. B 2015, 119 (36), 12059-12065. (16) Ramachandran, G.; Milan-Garces, E. A.; Udgaonkar, J. B.; Puranik, M. Resonance Raman spectroscopic measurements delineate the structural changes that occur during tau fibril formation. Biochemistry 2014, 53 (41), 6550-6565. (17) Ni, W.; Fang, H.; Springsteen, G.; Wang, B. The design of boronic acid spectroscopic reporter compounds by taking ad-vantage of the pK(a)-lowering effect of diol binding: nitrophenol-based color reporters for diols. J. Org. Chem. 2004, 69 (6), 1999-2007. (18) Wang, H.; Cheng, X.; Shi, Y.; Le, G. Preparation and structural characterization of polymannose synthesized by phosphoric acid catalyzation under microwave irradiation. Carbohydr. Polym. 2015, 121, 355-361. (19) Kubota, Y.; Hori, H.; Sawa, R.; Seki, H.; Uzawa, J. Structural analyses of mannose pentasaccharide of high mannose type oligosaccharides by 1D and 2D NMR spectroscopy. Magn. Reson. Chem. 2012, 50 (10), 659-664. (20) Seviour, T.; Lambert, L. K.; Pijuan, M.; Yuan, Z. Structural determination of a key exopolysaccharide in mixed culture aerobic sludge granules using NMR spectroscopy. Environ. Sci. Technol. 2010, 44 (23), 8964-8970. (21) Berube, M.; Dowlut, M.; Hall, D. G. Benzoboroxoles as efficient glycopyranosidebinding agents in physiological conditions: structure and selectivity of complex formation. J. Org. Chem. 2008, 73 (17), 6471-6479.


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Page 16 of 22

(22) (a) Becke, A. D. Density‐functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 1993, 98 (7), 5648-5652. (b) Stephens, P. J.; Devlin, F. J.; Chabalowski, C. F.; Frisch, M. J. Ab Initio Calculation of Vibrational Absorption and Circular Dichroism Spectra Using Density Functional Force Fields. J. Phys. Chem. 1994, 98 (45), 11623-11627. (c) Lee, C.; Yang, W.; Parr, R. G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 1988, 37 (2), 785-789. (23) Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Na-katsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T., Montgomery, J. A.; Jr., Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; To-masi, J.; Cossi, M.; Rega, N.; Millam, J. M.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, Ö.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian, Inc. Gaussian 09, Revision A.02. Wallingford CT, 2009. (24) Springsteen, G.; Wang, B. Alizarin Red S. as a general optical reporter for studying the binding of boronic acids with carbohydrates. Chem. Commun. 2001, (17), 1608-1609.


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TOC Graphic 394x224mm (120 x 120 DPI)



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Figure 1 315x297mm (96 x 96 DPI)


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Figure 2

251x247mm (96 x 96 DPI)



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Interactions of Glycopolymers with Assemblies of Peptide Amphiphiles

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