Quantitative Efficacy Classification of Ice Recrystallization Inhibition

Jul 30, 2014 - ABSTRACT: Experimental investigations of ice recrystallization inhibition (IRI) efficacy have been performed for a large number of diff...
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Quantitative Efficacy Classification of Ice Recrystallization Inhibition Agents Carsten Budke,†,§ Axel Dreyer,†,¶ Jasmin Jaeger,† Kerstin Gimpel,† Thomas Berkemeier,† Anna S. Bonin,‡ Lilly Nagel,‡ Carolin Plattner,‡ Arthur L. DeVries,∥ Norbert Sewald,‡,§ and Thomas Koop*,†,§ †

Atmospheric and Physical Chemistry, Faculty of Chemistry, ‡Organic and Bioorganic Chemistry, Faculty of Chemistry, and §Center for Molecular Materials, Bielefeld University, Universitätsstraße 25, D-33615 Bielefeld, Germany ∥ Department of Animal Biology, University of Illinois at Urbana−Champaign, 524 Burrill Hall, 407 South Goodwin, Urbana, Illinois 61801, United States S Supporting Information *

ABSTRACT: Experimental investigations of ice recrystallization inhibition (IRI) efficacy have been performed for a large number of different substances, including natural antifreeze proteins (AFP) and antifreeze glycoproteins (AFGP), several synthetic AFGP analogues, as well as synthetic polymers. Here we define IRI efficacy as that concentration at which the ice recrystallization rate is dominated by the IRI compound. The investigated 39 compounds show IRI efficacies from about 2 mmol L−1 for the least effective compound still showing activity to about 1 nmol L−1, which corresponds to the highest efficacy found for natural AFGP samples. Hence, the assay employed allows for a quantitative comparison of IRI efficacy over a range of at least 6 orders of magnitude, thereby enabling studies of distinguishing effects induced by even subtle structural variations in AFGP analogues that were synthesized. Our results show that AFGP are by far the most effective IRI agents in our assay, and we surmise that this particular efficacy may be due to their disaccharide moieties. This supposition is supported by the fact that IRI efficacy is strongly reduced for monosaccharide AFGP analogues, as well as for AFGP analogues with acetyl-protected monosaccharide moieties.

1. INTRODUCTION Ice formation and growth threatens many organisms that live at subzero temperatures.1,2 As a consequence, nature has developed two different protection strategies: freeze avoidance and freeze tolerance. In many insects freeze avoidance involves the accumulation of solutes and the removal of ice nucleating agents in order to minimize the likelihood of ice formation.2 Typical solutes are electrolytes, ethylene glycol or other polyols, which act by way of depressing the equilibrium freezing temperature and, as a consequence, also the ice nucleation temperature.3,4 For small solute concentrations, the equilibrium freezing temperature depends predominantly upon the amount of dissolved solute; i.e., freezing point depression is a colligative property, and at higher concentrations universal water activity corrections are available.5 With some insects and all fishes, freeze avoidance involves the inhibition of ice crystal growth in their body fluids by antifreeze proteins (AFP) and antifreeze glycoproteins (AFGP).1,2,6,7 Unlike their name suggests, AF(G)P do not act in a colligative manner as they do not cause significant depression of the equilibrium freezing temperature at physiological concentrations (∼10−30 mg per mL). Instead, these proteins adsorb to ice crystal surfaces, thereby preventing crystal growth normal to the affected ice faces. When AF(G)P concentrations are sufficiently high, ice crystal growth is inhibited entirely within a certain temperature range. Without AF(G)P, every ice crystal shrinks and finally melts completely above the equilibrium freezing temperature. Normally, a © 2014 American Chemical Society

temperature reduction below the equilibrium freezing temperature results in ice crystal growth. However, in the presence of AF(G)P, the growth is halted until the so-called hysteresis freezing temperature is reached. The concentration-dependent difference between the equilibrium freezing temperature and the hysteresis freezing temperature is called thermal hysteresis (TH).1,2,8,9 We also note that a slight superheating of ice crystals beyond the equilibrium freezing temperature is observed.10,11 The adsorption-inhibition mechanism of AF(G)P involves ice-binding of the proteins, which is why another commonly used name for this group is ice-binding proteins.12−14 Because AF(G)P adsorb preferentially to specific faces of an ice crystal, they cause ice crystal habit modification, sometimes also termed ice structuring.15−17 Ice crystals growing from slightly supercooled water and dilute aqueous solutions typically display a circular shape as this crystal habit minimizes the interface energy between the ice crystal and its surrounding solution. In the presence of AF(G)P, the ice crystals develop characteristic noncircular shapes. For example, a hexagonal crystal habit develops in the presence of AFGP (see Figure 1). The hexagonal crystal habit is a result of the inhibition of crystal growth normal to the primary prismatic faces of ice due to interaction with AFGP.18,19 Received: March 6, 2014 Revised: July 23, 2014 Published: July 30, 2014 4285

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Figure 2. Ice recrystallization in polycrystalline ice films as a function of annealing time t at −8 °C for three different conditions: without antifreeze agents (A) and at two different concentrations of AFGP8 (10) (B and C); adapted with changes from Nagel et al.83 (Copyright 2011 Springer) and with kind permisssion of Springer Science +Business Media.

AF(G)P, the recrystallization rate depends primarily upon the solution’s viscosity or, more precisely, upon the diffusion constant of water in the solution between adjacent ice crystals. The microphotographs in Figures 2B,C indicate that the reduction in ice crystal number and the increase of mean ice crystal size are slowed down at moderate AFGP8 concentration when compared to Figure 2A, and they are completely inhibited at high concentration.34 AFP and AFGP occur in various species in nature. Antifreeze proteins have been discovered first in fish in the late 1960s.6,8 Subsequently, four subclasses of fish AFP were termed AFP I− IV.35−39 All these proteins show noncolligative antifreeze properties independently of the expressing organism or of the method for determining antifreeze activity. AFP from plants typically show quite small thermal hysteresis ( 27 > 29 shows the same order as gradual changes in the corresponding circular dichroism (CD) spectra of these peptides.50 This similarity may be indicative of a moderate role of the secondary structure of the peptide upon IRI activity induced by variations in backbone amino acids. In addition to those substances shown in Figure 4, we have studied a wide range of additional substances including natural antifreeze proteins as well as synthetic AFGP analogues or simple polymers. The corresponding results of experimentally determined ci values are shown in Figure 5 for comparison. In panel A we have ranked the active compounds according to

Figure 5. (A) Ice recrystallization inhibition (IRI) concentration ci for various active IRI agents. The numbers on the left refer to the reference numbers of each compound as given in Tables 1 and 2. Abbreviated names or amino acid sequences are also provided, and colors indicate substances that belong to the same subgroup of compounds. (B) Substances that did not show IRI activity up to the specified concentration cLL, which is a lower limit for ci (that is cLL < ci). Colored bars refer to concentration in units of μmol L−1, while gray vertical lines refer to concentration in units of μg mL−1.

their IRI efficacy, i.e., in the order of increasing molar concentration values of ci. In panel B we show compounds that were inactive up to the indicated concentration cLL. These substances are either entirely inactive or may show a very low activity with a ci value above the indicated lower limit value cLL, and thus ci > cLL. From Figure 5A it can be concluded that for active compounds the molar IRI efficacy clearly scales with molecular mass (and thus size) of the molecules within a particular class of compounds (each indicated by one color): an increasing IRI efficacy corresponds to a decreasing ci. This is true for synthetic polymers such as poly(vinyl alcohol) with molar ci values decreasing in the order PVA6 (3) > PVA27 (2) > PVA145 (1), and similarly for natural samples of AFGP with AFGP8 (10) > AFGP1−5 (9), as well as for synthesized short monosaccharide AFGP (16 > 15 > 14 ≈ 13) or short disaccharide AFGP (12 > 11). This observed size dependence resulting from our IRI analysis is in accordance with similar dependencies for thermal hysteresis and IRI experiments reported previously.63,91,93,95 Note that in previous experiments this size trend was observed for AFGP from the two-repeat onward,93 while in more recent studies by the same group this trend was observed only from the four-repeat on, arguing that the former studies might have 4290

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and often near-linear dependence of IRI efficacy upon P−1. In the example of monosaccharide AFGP analogues (red triangles), the three-repeat (with P = 11) is almost 2 orders of magnitude less effective than the four-repeat (P = 14), and another order of magnitude less effective than the five-repeat (P = 17); however the six-repeat (P = 20) shows nearly the same efficacy as the five-repeat. The effect of chain length is more clearly observed in the case of natural AFGP, for which the longer AFGP1−5 (9; 22.1 kDa) are much stronger inhibitors than the smallest naturally available fraction AFGP8 (10; 2.65 kDa). The latter is chemically nearly identical to the synthesized peptide 11, and the two have practically identical IRI efficacies (0.085 μmol L−1 versus 0.086 μmol L−1, respectively). We note, however, that we do not have efficacy data of AFGP at intermediate number of amino acid residues between AFGP1−5 and AFGP8, because such samples were not available to us. Therefore, we indicate the anticipated ci values in this intermediate range by the gray area in Figure 6. The upper border of the gray area was constructed by linearly interpolating between the data for AFGP1−5 and AFGP8 likely representing an upper limit of ci. The lower border was constructed by linearly extrapolating the slope of ci versus P−1 for the disaccharide AFGP (black, diAFGP) to the five-repeat (P = 17) and then connecting this value to the measured AFGP1−5 value, yielding a likely lower limit for ci and a curve that is similar to that measured for the monosaccharide AFGP (red, monoAFG). Finally, the chain length effect is also observed for the synthetic polymer PVA. In the case of PVA, however, P is not the number of amino acid residues but rather the weightaverage degree of polymerization. We postulate that this molecular mass effect on efficacy is not only due to the actual size of the molecule, which may result in a larger ice surface area covered per molecule, but may also be caused by the fact that larger molecules do exhibit more potential moieties for the adsorption to the ice, which may lead to a faster and/or stronger adsorption to ice. For both the monosaccharide AFGP (red triangles) as well as the disaccharide AFGP (black and gray triangles), this effect apparently saturates at larger molecular masses, which may be explained by the fact that for the smaller molecules each additional tripeptide repeating unit represents a significant increase in the number of potential adsorbing moieties, while for the larger molecules there are already sufficient interactions that additional tripeptide repeats do not add significantly to the overall adsorption strength. Hence, for the larger molecules size may become a less relevant effect. As noted above we observed that the longest PVA145 is the most effective when compared at molar concentrations. In contrast, when the ci values are compared on a mass concentration basis, the midsized PVA27 is the most effective, as a result of a nonlinear increase in IRI efficacy with increasing chain length, see Figure 5A as well as Figure S13, Supporting Information. This observation might be because the PVA polymer molecules do not adsorb linearly to the ice, but form random coil structures in solution, such that not all binding moieties can be presented toward the ice surface.56 Hence, for the very long PVA molecules the adsorption strength increases only slightly with increasing chain length. As a result, this minor increase in adsorption strength for the larger polymers observed for molar concentrations cannot compensate for the higher number of smaller polymers when compared at the same mass concentration.

suffered from impurities by larger peptides.96 In particular, our results for PVA are in agreement with a recent analysis of IRI activity of PVA of different molar mass by Congdon et al.,91 which revealed that at least 19 repeating units are required for IRI activity. In order to obtain a more systematic overview on IRI efficacy of the various substances and to allow for a better comparison, we summarize in Figure 6 the bulk part of the results obtained

Figure 6. Ice recrystallization inhibition (IRI) concentration ci as a function of the inverse number of amino acid residues P−1 for several AFP, AFGP, and their analogues as well as for synthetic polymers. Note that for the polymers PVA, PEG3, and PAspNa, which do not contain amino acids, the weight-average degree of polymerization has been used for P. The gray area for the natural AFGP indicates the range of anticipated ci at intermediate number of amino acid residues between AFGP1−5 and AFGP8, for which no data are available (see text). The values for PEG3 and PAspNa correspond to cLL, which is the maximum concentration tested without signs of activity, thus representing a lower limit for ci with cLL < ci. This IRI concentration overview graph is shown on a mass concentration scale in Figure S13, Supporting Information.

in the present study using the IRRINA assay. The IRI efficacies vary over a huge concentration range, from about ci = 103 μmol L−1 for the acetyl-protected monosaccharide peptide (19) to about 10−3 μmol L−1, which corresponds to the highest efficacy found for natural AFGP1−5 (9) samples. In particular, we show in Figure 6 a comparison of natural AFP and AFGP, as well as several active AFGP analogues and the active synthetic polymer PVA. Also shown are the results for nonactive polymers such as PEG3 and PAspNa, which show no activity up to the indicated concentrations of 2700 μmol L−1 and 2900 μmol L−1, respectively. We note that the noneffective AFGP analogues that either exhibit very large ci or did not show any activity up to the investigated cLL are not included in Figure 6 in order not to clutter the entire figure. It is quite striking that in our assay the natural AFGP are by far the most effective substances investigated, being more effective than natural AFP I and AFP III as well as the largest investigated synthetic polymer PVA145 by at least 2 orders of magnitude. This also holds true when the ci data are shown on a mass concentration scale, i.e., in units of μg mL−1 (see Figure 5A, and also Figure S13, Supporting Information). In Figure 6 the ci data are shown as a function of the inverse number of amino acid residues P−1 to allow for a comparison between different oligomers or polymers within a compound class. For the same class of compounds, we observe a strong 4291

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the superior efficacy of the AFGP peptides is probably not due to the amino acid backbone, but the saccharide moieties may play an important role. Our results are in line with recent studies highlighting the importance of AFGP saccharide moieties by slowing down water dynamics in a large hydration shell, thus affecting ice growth.74,100 Because the saccharide moieties provide a large number of OH-groups able of hydrogen-bond formation, they are very effective in retarding water dynamics in the hydration shell. This fact is in agreement with our results, since we observed reductions of several orders of magnitude in IRI efficacy when comparing disaccharide AFGP (11) with monosaccharide AFGP (15) and their peptide backbone (17). Likewise, acetyl protection of the saccharide OH-groups reduced IRI efficacy much stronger than protection at the Nterminus. In spectroscopic studies on AFGP, a similar complexation of the saccharide OH groups by borate suppressed the long-range hydration shell,74 and in preliminary experiments we also observed a reduction in IRI efficacy of a synthetic AFGP (11) in the presence of boric acid.101 Finally, Ebbinghaus et al.74 estimated that the hydration shell of AFGP increased from ∼20 Å to ∼30 Å when the temperature is reduced from 20 to 5 °C. We propose that the hydration shell may be even further enlarged at the temperature of −8 °C in our IRRINA assay, thus providing a rationale for the particularly high IRI efficacy of AFGP observed here.

We also investigated several IRI-inactive compounds for comparison such as the synthetic polymers PEG3 (5) and PAspNa (4). These results indicate that it is not the polymeric nature of water-soluble molecules themselves that make them effective IRI agents, as has been noted previously.57 PEG3 does not show any inhibition activity up to the highest concentration tested (2700 μmol L−1), even though it is known to very effectively suppress ice nucleation.3,97 Moreover, poly-L-aspartic acid (30 kDa) has been reported to show a very slight ice recrystallization inhibition activity at a concentration of 1 mg mL−1, equivalent to 33 μmol L−1.57 Here, we do not see any effect for its sodium salt PAspNa (see structure in Supporting Information) with a molecular mass of 5.2 kDa at concentrations of up to 2900 μmol L−1, suggesting that either the investigated PAspNa is too small to be an effective IRI agent, or that the sodium cations are responsible for the lack of effect. Finally, as noted in the discussion of Figure 4A above, we see a strong effect when protecting groups block important moieties of an effective AFGP. For example, protecting the OH groups of the saccharide moieties by acetals reduces the inhibition efficacy of the monosaccharide AFGP five-repeat (14; P = 17, red triangle) by almost 2 orders of magnitude (18; P = 17, purple triangle labeled ac-prot). This change in inhibition is similar in magnitude to that of going from a monosaccharide to a disaccharide AFGP of the same length (compare the red and black/gray lines in Figure 6), indicating a relevance of the saccharides moieties for the IRI efficacy of AFGP. We tentatively subdivided the IRI efficacy range observed in our assay into three main classes according to the corresponding ci values: very effective IRI agents for ci values of up to about 10−1 μmol L−1, effective IRI agents for ci values between about 10−1 and 103 μmol L−1, and noneffective IRI agents for ci values beyond about 103 μmol L−1. As mentioned above, the synthetic polymers PEG3 (5) and PAspNa (4) belong to the class of noneffective IRI agents, in addition to many analogues studied but not shown in Figure 6 (see Figure 5B for comparison). In the intermediate range we find effective IRI agents such as the natural AFP I variants (6 and 7) and AFP III (8), PVA (1−3), the monosaccharide AFGP analogues (13−16) as well as the smallest disaccharide AFGP analogue (12), which contains only 11 amino acid residues. According to our classification scheme, only AFGP belong to the most potent group of very effective IRI agents. We note that also other natural AF(G)P not investigated here may belong to the class of very effective IRI agents, for example, some of the hyperactive AFP found in insects.45,98,99 However, a previous study has shown that it is not straightforward to infer IRI efficacy from a relative comparison of the TH activity.92 While within the class of AFGP there is a strong dependence of ci upon the number of amino acid residues P as outlined above, the high efficacy of AFGP is preserved also for very small P, because even AFGP consisting of only 14 amino acid residues (both from natural sources (10) and synthesized here (11)) are considerably more effective than the largest investigated polymer PVA145 and also more effective than AFP of type I or III (with 37 and 66 amino acid residues). On the other hand, AFP III (8) and the two variants of AFP I (6 and 7) all have only moderately larger or similar molecular masses (6.5, 3.2, and 3.3 kDa, respectively) when compared to that of 2.7 kDa for AFGP8 (10) and the synthetic disaccharide AFGP analogue (11). This further supports our suggestion that

4. CONCLUSIONS We have used the IRRINA assay to perform quantitative measurements on the IRI efficacy of a wide range of substances, including natural AFP and AFGP, several synthetic AFGP analogues, and synthetic polymers. To the best of our knowledge, the comparison provided here (Figures 5 and 6) is the most comprehensive of its kind allowing for a quantitative comparison of IRI efficacy over such a wide range of more than 6 orders of magnitude. Previous ice recrystallization assays often employ the same concentration for each compound and thus exhibit a smaller dynamic range of only about 2 orders of magnitude, because they often reveal a sensitivity that is in the percent range. The large dynamic range of the IRRINA assay arises from the fact that IRI agent concentrations can be varied over a wide range without losing sensitivity to rather minute changes in IRI agent concentration. Therefore, it is possible to observe and to distinguish even small differences in efficacy of AFGP analogues exhibiting only subtle structural variations. Our results indicate that AFGP are the most effective IRI agents investigated here, both on a molar concentration as well as on a mass concentration scale. We surmise that this particular efficacy is due to the disaccharide moieties of the AFGP. This supposition is further supported by the strongly reduced IRI efficacy for monosaccharide AFGP analogues, and even lesser efficacy for the plain backbone peptides as well as acetyl protected monosaccharide moieties. These observations are in accordance with recent investigations of the dynamics of water molecules in the hydration shell of AFGP using Terahertz spectroscopy.74,100 Both the overall comparison of the various substances as well as the observed effects of saccharide moieties may help in the development of synthetic noncolligative antifreeze agents and their application in the food industries or for biological cryo-storage applications. 4292

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S Supporting Information *

Figures S1−S12 present the primary structures of all substances investigated in this study. Also given are sources and specifications of those substances that were obtained commercially. For substances synthesized by ourselves, either more experimental details for the chemical synthesis are given or references describing the chemical synthesis are provided. Figure S13 presents the IRI concentration overview graph of Figure 6 on a mass concentration scale. This material is available free of charge via the Internet at http://pubs.acs.org.



= β-D-galactopyranosyl-(1 → 3)-2-acetamido-2-deoxy-α-Dgalactopyranosyl g = 2-acetamido-2-deoxy-α-D-glucopyranosyl m = 2-acetamido-2-deoxy-α-D-galactopyranosyl d

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REFERENCES

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Present Address ¶

Hamburg University of Technology, Institute Advanced Ceramics, Denickestrasse 15, D-21073 Hamburg, Germany.

Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS We gratefully acknowledge support from the German Science Foundation (DFG) for a grant for project A8 within Sonderforschungsbereich SFB613.



ABBREVIATIONS AFP = antifreeze protein AFGP = antifreeze glycoprotein IRI = ice recrystallization inhibition IRRINA = ice recrystallization rate inhibition analysis LSW = Lifshitz−Slyosov−Wagner TH = thermal hysteresis A = L-alanine Ĝ t = N-(1H-1,2,3-triazol-4-yl)methylglycine a = D-alanine Ä = acetyl-L-alanine D = L-aspartic acid E = L-glutamic acid G = glycine Ĝ = N-methylglycine (= sarcosine) I = L-isoleucine K = L-lysine L = L-leucine M = L-methionine N = L-asparagine O = L-trans-4-hydroxyproline P = L-proline Pt = L-cis-4-(4-hydroxymethyl-1H-1,2,3-triazolyl)proline P̲ t = L-trans-4-(4-hydroxymethyl-1H-1,2,3-triazolyl)proline Q = L-glutamine R = L-arginine S = L-serine T = L-threonine t = D-threonine Ť = allo-L-threonine V = L-valine Y = L-tyrosine a = α-D-galactopyranosyl b = β-D-galactopyranosyl c = 2-acetamido-3,4,6-tri-O-acetyl-2-deoxy-α-D-galactopyranosyl 4293

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