Fabrication of anti-icing surfaces by short Î±-helical peptides

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Fabrication of anti-icing surfaces by short #-helical peptides Yifan Zhang, Kai Liu, Kaiyong Li, Voytek Gutowski, Yuan Yin, and Jianjun Wang ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.7b13130 • Publication Date (Web): 25 Dec 2017 Downloaded from http://pubs.acs.org on December 26, 2017

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ACS Applied Materials & Interfaces

Fabrication of anti-icing surfaces by short α-helical peptides †

‡

§

†

†

Yifan Zhang, Kai Liu, Kaiyong Li, Voytek Gutowski, Yuan Yin and Jianjun Wang*

‡

†

Changchun Institute of Applied Chemistry, Chinese Academy of Sciences. Changchun.

P. R. China. ‡

Institute of Chemistry, Chinese Academy of Sciences. Beijing 100190, P. R. China.

§

Luoyang Institute of Science and Technology. Henan, P. R. China.

ABSTRACT We designed 12-amino acid peptides as AFP mimetics and tuned the antifreeze activity of the peptides by their structures. Moreover, these short peptides were firstly immobilized to surfaces as the anti-icing coating. We discover that the peptides with higher antifreeze activity exhibited better anti-icing performance. It is the first time that short peptides were successfully applied to fabricate anti-icing surfaces, which is certainly of advantages in comparison to AFP anti-icing coatings previous reported.

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KEYWORDS: antifreeze-peptide, helical structure, anti-icing, surface

INTRODUCTION Antifreeze proteins (AFPs) are a class of proteins that can control the formation of ice crystals as an evolutionary adaptation of organisms to cold climates enabling their survival, which were first separated from the serum of polar fishes1-2. During the past decades, AFPs were found in organism such as fishes, insects, plants, bacterium and fungus.2-10 According to different antifreeze activity and structures of AFPs, different mechanisms were proposed to explain the interaction between AFPs and ice.11-17 As the most widely accepted mechanism, the adsorption-inhibition mechanism considered that the AFPs bind to ice

crystal

surface,11 and the adsorption of

the

protein induces

microcurvatures on the surface of ice crystals, thus depresses the freezing temperature due to the Kelvin effect. Recent investigations reveal the antifreeze activity of AFPs in the molecular level, that is, AFPs bind to ice by their ice-binding site around which water molecules are ordered to form ice-like structure.18-20 In contrast, on non-ice-binding sites almost no ice-like structure can be formed.21 Due to their unique capability in controlling ice formation, AFPs are very attractive for potential practical applications including food storage,22-23 cryopreservation cells and tissues,24-26 and anti-icing of aircraft and other land and water vehicles and vessels, as well as infrastructure.27-28


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However, the limiting factor regarding practical applications of AFPs is that they cannot be extracted in viable quantities from living organisms.29 Moreover, although some AFPs could be expressed recombinantly in bacteria,30 they are expensive and unstable. Therefore, efficient synthetic analogues mimicking the effects of AFPs are highly desirable. As the investigation of the antifreeze mechanism of AFP goes further, the design of AFP mimetics was optimized. A number of synthetic AFP mimetics have been proposed as alternatives to naturally occurring AFPs,31-36 and some of them could be applied in cryopreservation.33-36 However, application for anti-icing coatings with AFPs mimetics have not been paid adequate attention.37 In this paper we designed three 12-amino acid analogues with α-helix and tuned their antifreeze activity by their structures. Subsequently, the peptides were applied for the fabrication of anti-icing surfaces. To our knowledge, it is the first time that short antifreeze peptide with 12 amino-acids has been used to construct anti-icing coatings, which has been achieved only by several AFPs.28, 38-39

Design and synthesis of AFP mimetics with 12-amino acids Herein, the sequence of DTASDAAAAAAL was carefully assessed for designing antifreeze peptide based anti-icing coatings, which was inspired by the natural type I AFP that is rich in alanine residues and has the simplest structure in the family of AFPs with only α-helix as its secondary structure. The ice-binding site of type I AFP are composed by the residues of Thr, Ala and Ala in the position of i, i+4 and i+8 respectively, which are arrayed along one face



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of the helix. Kun and co-workers had divided the natural type I AFP into three constituent

segments,

DTASDAAAAAAL.40

and

Based

confirmed on

the

antifreeze

sequence

of

activity

of

DTASDAAAAAAL

(hereinafter denoted as peptide 1-1), we designed two kinds of α-helical peptides (denoted as peptides 1-2 and 1-3) and tuned their secondary structures by amino acid sequences. As shown in Table 1, a lysine (K) and a glutamic acid (E) were used to replace an alanine in the sequence of peptide 1-1 to produce peptide 1-2 for enhancing the helicity, in which K and E are displayed by red color. In the sequence of peptide 1-2, the residues of Thr, Ala, Ala kept their positions in the i, i+4, i+8 as peptide 1-1, which compose the ice-binding site. According to the work of Chakrabartty et al.,41 an amide bridge can form between the amine in the side chain of lysine and the carboxyl in that of glutamic acid, thus increasing the helicity of peptide and, in turn, rendering the helical structure more stable. Moreover, the amide bridge in the helical structure was opposite to the ice-binding site, which would only affect the secondary structure of the peptide as well as the chemical structure of the opposite face of the ice-binding site, but would not affect the chemical structure of the ice-binding site. In the sequence of peptide 1-3, phenylalanine (F) was exploited to substitute an alanine in the sequence of peptide 1-1, whilst the residues of Thr, Ala, Ala kept their spatial position as the ice-binding site. The phenylalanine had phenyl as its side chain; the accompanying steric hindrance affected the folding of the sequence of amino acids, leading to the change of the helical structure as corroborated below.


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Additionally, the phenylalanine in peptide 1-3 was at the same position as the lysine in peptide 1-2, which would not change the chemical structure of the ice-binding site.

Table 1. The sequences and molecular weights of the designed peptides.

The designed peptides were synthesized by solid-phase peptide synthesis (SPPS) protocols. Peptide 1-1 was synthesized on Wang resin. Fmoc-A-amino acids

were

activated

by

HBTU

hydroxybenzotriazole

and

diisopropylethylamine, and reacted with L-Wang resin for 45 minutes. Fomc-protecting

groups

were

removed

by

using

20%

piperidine

in

dimethylformamide, and then the mixture was rinsed by dimethylformamide, methyl alcohol and dichloromethane. By repeating the above procedure, the amide acids A, A, A, A, A, D, S, A, T, D were coupled to the amino acid sequence. After synthesis, the peptides were cleaved from the resin and deprotected by treatment for 2 h with trifluoroaceticacid/triisopropylsilane/H2O (95:2.5:2.5). The crude peptides were obtained by freeze-drying the solution. Peptide 1-2 and peptide 1-3 were also synthesized following the above protocol. The molecular weight of the synthesized peptides was confirmed by mass spectrometry (see Figure S1-3). Moreover, the thermal hystersis (TH) of peptide



1-1 was characterized by the nanolitre osmometer and shown in Figure S4, which increased with the concentration, and at the concentration of 10 mg/mL, the TH value of peptide 1-1 is 0.46 ℃.

RESULTS AND DISCUSSION The structures of designed peptides were characterized by the circular dichroism (CD) spectroscopy in the far UV spectral range (190-260 nm wavelength). The peptides were dissolved in the PBS solution (0.1 mg/mL), and were subsequently tested under the room temperature condition (25 ℃). PBS solution is a commonly used buffer solution to stabilize the structure of peptides, which does not exhibit absorption in the wavelength range of 190-300 nm. The CD spectrum of peptide 1-1 (Figure 1a) exhibits double negative peaks at 206 and 222 nm, which is typical for α-helix. Moreover, consistent with the character of type I AFP, the α-helical contents of peptide 1-1 increase when the temperature decrease, as shown in Figure S5. Compared to peptide 1-1, the slight red shift of the peak at 206 nm and the stronger absorption at 222 nm of the spectrum assigned to peptide 1-2 demonstrate its higher helicity. Whereas, the blue shift of the peak at 206 nm and the weaker absorption at 222 nm of the spectrum assigned to peptide 1-3 indicate its lower helicity. Although we did not estimate the α-helical contents of peptides investigated in our works, based on the CD spectra illustrated in Figure 1a we are able to conclude that the CD spectra clearly demonstrate that all three peptides have α-helix in their structures, and the degree of helicity is consistent with our design, i.e., peptide


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1-2 > peptide 1-1 > peptide 1-3. The helical structures of these three peptides are illustrated in Figure 1b-d.

Figure 1. (a) The CD-spectra of peptide 1-1, 1-2, and 1-3. (b-d) The helical structure of peptide 1-1, 1-2, and 1-3, the substituted amino acids in the peptides are circled by black dotted lines. In the helical structure, the red, blue, and cyan spheres represent oxygen, nitrogen, and carbon atoms, respectively.

The ice shaping property exhibited the recognition and adsorption ability of AFPs to the prism/basal plane of ice. The observation of the ice shaping property of the peptides was performed using a nanolitre osmometer. The peptides were dissolved in ultrapure water at a concentration of 1.0 mg/mL. Then, the peptide solution was injected into a droplet of immersion oil in the sample well of



nanolitre osmometer using a stretched capillary. The ice crystal growth was examined by the protocol according to which rapid freezing ensued by slow melting of the peptide solution was used repeatedly to form a single ice crystal of a desired size. As shown in Figure 2a, compared to the circular ice crystals in pure water and the solution of peptide 1-3, the morphology of ice crystals grown in the solutions of peptides 1-1 and 1-2 are modified with the observation of hexagons. This unique shape of ice crystal signals the ability of peptides to interact with the prism faces of ice and ultimately shaped the ice crystal as well as hindered its growth. Similar to AFPs, the peptides shall adsorb to ice by their ice-binding sites indicated by the shape of ice crystal grown in the peptide 1-2 solution; and the lost of ice shaping property of peptide 1-3 possibly due to that the reduction of helicity change spatial position of i Thr, i+4 Ala, i+8 Ala. The change of the ice-binding site in peptide 1-3 lead to its deficiency in binding to the ice surface. Ice recrystallisation inhibition is the property of AFPs to inhibit the growth rate of an ice crystal, which occurs between adjacent ice crystals. During the recrystallization, larger crystals grow at the expense of smaller ones in order to minimise the total surface energy. The ice recrystallization inhibition (IRI) activity of peptide 1-1, 1-2 and 1-3 were observed by an optical microscopy via the rapid quenching and the following annealing at an elevated sub-zero temperature (details see supporting information). The assays were repeated at least 3 times. As shown in Figure 2b, the peptide 1-2 shows potent ice recrystallization inhibition activity compared to PBS. However, the peptide


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1-1 and 1-3 don’t exhibit ice recrystallization inhibition activity. This could be explained by the structure of the peptides. In our previous work, we proposed that AFPs suppress ice growth by both the ice-binding site and the non-ice-binding site.39 AFPs adsorb to ice by their ice-binding site and the-non ice-binding site is exposed to liquid water. The salt bridge of peptide 1-2 is in the non-ice-binding site which exhibited electronegativity due to p-π conjugation of carbonyl and nitrogen atom. The negatively charged surface could inhibit ice nucleation.42-43 Compared to peptide 1-1, the electronegativity of the non-ice-binding site on peptide 1-2 help it to suppress the growth of ice. The results of DIS and IRI indicate a relatively higher antifreeze activity of peptide 1-2 than peptide 1-1 and 1-3, which are caused by the difference of the α-helicity as well as the electronegtivity of non-ice-binding site. The decrease of the helicity changes the ice-binding site, as such the reduction (or lost) of the ice-binding ability. And the increase of electronegtivity on the non-ice-binding site could increase the ice growth inhibition performance.

Figure 2. (a) Optical microscopic images of the ice crystal morphologies grown in pure water and the solutions of peptides 1-1, 1-2, and 1-3. (b) The optical images of the ice crystal grown in PBS buffer and the peptide solutions. The scale bar is 100 µm.



For the anti-icing coatings, our designed antifreeze peptides were bound to a substrate (silicon wafer) via mussel-inspired surface chemistry,44-46 as shown in Figure 3a. The cleaned silicon wafers were first immersed into a freshly prepared solution of dopamine/HCl in 10 mM bicine buffer at a concentration of 2 mg/mL (pH = 8.4) for 24 h at the room temperature, and then the substrates were rinsed three times. Subsequently, the polydopamine coated substrates were immersed into a solution of 1 mg/mL peptide/PBS (pH = 7.4) for 24 h, which could ensure the chemical adsorption of peptide to the polydopamine coated surface was saturated. The peptide coated surface was rinsed three times and dried by the nitrogen-blow. Atomic force microscopy (AFM) and XPS of the peptide coated surface were used to confirm that the peptides were successfully bound to the polydopamine coated surface, as shown in Figure 3b and 3c. The roughness of the polydopamine coated surface is 0.523 nm. And the roughness of peptide 1-1, 1-2 and 1-3 coated substrates are 0.674 nm, 0.875 nm and 0.603 nm, respectively. The roughness of the peptide coated surfaces slightly increases, and the nitrogen/carbon ratio of peptide coated surfaces increase from 0.082 to 0.097 compared to polydopamine coated surface, which suggest that the peptides were successfully bound to the polydopamine coated surface. The average thickness the peptide coatings are increased from 2.25 nm to 3.80 nm in contrast with polydopamine coating as measured by ellipsometry. The contact angle of polydopamine coated surface is 36.8°, and that of the peptide 1-1, 1-2, 1-3 coated surfaces is: 43.2°, 42.3°, 47.7° respectively (as shown in Figure 3d). The contact angle results show similar hydrophilicity on peptide 1-1, 1-2 and 1-3 coated surfaces (the differences are between 0.9~5.4°).


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Figure 3. (a) Schematic representation of the fabrication process of the surfaces coated by antifreeze peptides. (b) Atomic force microscopy images (500×500 nm) of polydopamine coated surface, peptide 1-1, 1-2 and 1-3 coated surface. (c) The XPS spectra of peptide 1-1, 1-2, 1-3 coated surfaces and polydopamine coated surface. (d) The contact angles of polydopamine coated surface (DOP), peptide 1-1, 1-2 and 1-3 coated surfaces.

The anti-icing performance of the peptide coated surfaces were investigated in open air. The peptide coated surfaces were tested on a cooling stage (Linkam, THMS600) cooled at 2 ℃/min under the atmosphere of open environment at the room temperature with relative humidity of 50%. The moisture initially condensed onto each peptide coated surfaces in the form of droplets, which progressively coalesced and finally froze. The test for each surface was repeated at least 20 times. As shown in Figure 4, upon gradually cooling, the average freezing temperature of the condensed water on the surface coated by peptide 1-3 is -10.8 ℃, closely followed the surface coated by peptide 1-1 on which the water freeze at -11.9 ℃. Strikingly, the average freezing temperature of water on the surface coated by peptide 1-2 reaches -16.3 ℃. Compared to peptide 1-3, the peptide 1-1 and 1-2 coated surfaces depress the freezing temperature by 1.1 and 5.7 ℃ respectively. It demonstrates the feasibility of designing efficient



anti-icing coatings by using our proposed protocol.

Figure 4. Anti-icing performance of the surfaces coated by peptides 1-1, 1-2 and 1-3.

CONCLUSIONS The 12-amino acid α-helical antifreeze peptides were designed based on the structure character of Type I AFP, and the helicity of the peptide were tuned. The investigation of DIS and IRI properties of the peptides indicate higher antifreeze activity of the peptides with higher helicity. And the antifreeze peptides were immobilized on solid surfaces as anti-icing coatings, which was confirmed by AFM and XPS. We discover that the surfaces coated by peptides with higher antifreeze activity exhibited better anti-icing performance under open environment. Our work not only provides a type of peptide with good antifreeze activity, but also successfully applied short peptides to the fabrication of efficient anti-icing surfaces.


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ASSOCIATED CONTENT

Supporting Information. Mass spectrum of the peptides, temperature dependence on the helicity of the peptides, the ice recrystallization inhibition property of the peptides, the thermal hysteresis property of the peptide, the freezing temperature of the peptide solution. AUTHOR INFORMATION Corresponding Author *E-mail: [email protected]

Notes The authors declare no competing financial interest.

ACKNOWLEDGEMENT The authors are grateful to the Shanghai ketai Bio-Technique Co. Ltd. for the help of the peptide synthesis. The authors are grateful for the financial support from the Chinese National Nature Science Foundation (Grant Nos. 51436004, 21421061), Strategic Priority Research Program of Chinese Academy of Sciences (Grant XDA09020000), the 973 Program (2013CB933800) and the Recruitment Program of Foreign Experts (WQ20142200219).

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Fabrication of anti-icing surfaces by short Î±-helical peptides

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