Ice Nucleation Inhibition: Mechanism of Antifreeze by Antifreeze Protein
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1 JBC Papers in Press. Published on June 26, 2003 as Manuscript M Ice Nucleation Inhibition: Mechanism of Antifreeze by Antifreeze Protein Ning Du, X.Y. Liu* Department of Physics, National University of Singapore, 10 Kent Ridge Crescent, Singapore Choy Leong Hew Department of Biology, National University of Singapore, 14 Science Drive 4 Singapore SUMMARY The effect of Antifreeze Protein type III (AFP III, one type of fish antifreeze protein) on ice crystallization was examined quantitatively based on a micro-sized ice nucleation technique. It is found for the first time that Antifreeze Proteins can inhibit the ice nucleation process by adsorbing onto both the surface of ice nuclei and that of dust particles. This leads to an increase of the ice nucleation barrier and the desolvation kink kinetics barrier, respectively. Based on the latest nucleation model, the increases in the ice nucleation barrier and the kink kinetics barrier were measured. This enables us to quantitatively examine the antifreeze mechanism of AFPs for the first time. * To whom correspondence should be addressed. Tel: ; Fax: ; phyliuxy@nus.edu.sg. Copyright 2003 by The American Society for Biochemistry and Molecular Biology, Inc. 1
2 INTRODUCTION Antifreeze proteins are found in the blood and tissues of organisms that live in freezing environments (1). In these organisms, ranging from fish to bacteria, the effect of freezing is retarded or the damage incurred upon freezing and thawing is reduced (2-4). Applications of the antifreeze effect of these antifreeze proteins (AFPs), that is the capacity to inhibit ice crystallization, have been sought for maintaining the texture in frozen food, improving storage of blood, tissues and organs, cryosurgery, and protecting crops from freezing (4). Freezing is a process of ice crystallization from supercooled water. In this process, water should undergo the stage of ice nucleation, followed by the growth of ice (5). Actually, whether or not freezing takes place is determined to a large extent by ice nucleation. In other words, there would be no ice growth if ice nucleation did not occur. The freezing inhibition brought about by antifreeze proteins is actually to impede the nucleation and the growth of ice by reducing the associated kinetics. Previous studies of the AFPs were mainly focused on the modification of the crystal morphology of ice and the inhibition of ice crystal growth in terms of the adsorption of antifreeze protein molecules on specific surfaces of ice (6-8). It is believed (9-11) that antifreeze proteins lower the freezing point of water merely by adsorbing their residues onto the ice crystal surfaces, and thereby inhibiting their growth. Although some reports show the modification of the ice morphology caused by AFPs (7), no study has thus far been carried out to show how AFPs inhibit ice crystallization, in particular ice nucleation. We notice that the neglect of the initial and key stage of ice crystallization, i.e. 2
3 nucleation, is likely due to the fact that a well-defined kinetics measurement is a difficult and challenge task. In this paper, we will present the first study on the effect of AFPs on the nucleation of ice in supercooled water using a newly developed technique, so-called double oil layer micro-sized ice crystallization technique (12). This technique allows us to minimize the influence of the wall of the container on the nucleation of micro-sized ice, therefore obtain reliable and reproducible data on ice nucleation. Since the water is confined in a micro-sized droplet, it is a model system to mimic the freezing in organisms or in the air, where water is normally distributed in micro or sub-micro sized droplets. Apart from this, our new model on nucleation (13) will be applied to analyze quantitatively the effect of AFP III on ice crystallization. This will be achieved by a quantitative measurement of the change of the free energy barrier associated with different dynamic steps in ice nucleation. Based on these results, we wish to obtain a new and comprehensive understanding on the AFP antifreeze mechanism, in particular that of the effect of AFPs on ice nucleation. We hope that this study will provide us fresh physical insight into the phenomenon of AFP antifreeze, which will shed light on the identification of new and effective antifreeze proteins/agents. THEORY In most cases, the formation of a new crystalline phase from the ambient phase proceeds via nucleation followed by growth (5). This implies that in the case of ice crystallization, nucleation is the initial and one of the most important steps toward 3
4 creating ice. Without this step, ice will never occur in supercooled water. In the following discussion, we will examine ice nucleation based on the newly developed model (13). For ice crystallization, a positive thermodynamic driving force is required, which is defined as (14) f s µ µ µ ( H m / Tm ) T = = kt kt kt (1) where µ f and µ s are the chemical potential of solute molecules in the fluid phase and in the solid phase, respectively; H m denotes the enthalpy of melting per molecule and T m the melting temperature; Τ is supercooling ( T k is the Boltzmann constant. = T m T, T is the actual temperature); The nucleation process can be regarded as a kinetic process for ice nuclei to overcome a kinetics barrier, the so-called nucleation barrier under a given thermodynamic driving force µ/kt (14). Taking into account the effect of foreign particles on nucleation, the nucleation rate of ice, which is defined as the number of nuclei generated per unit of time-volume, is given according to the model as s 2 o [( R ) N ] f" ( m) f ( m) 2 [ /( ) ] [ ] 1/ 2 B exp f ( m) J = 4π aβ κ T (2) knk with κ 16πγ 3 Ω 2 3 kts 2 m, (3) = cf B = 14 1/ 2 2 γ a Ω cf π (4) kt where γ cf denotes the specific interfacial free energy between the crystals and the mother phase, Ω is the volume of the growth units, S m is the entropy of melting per molecule, a is the dimension of a growth unit, R s and N 0 are the radius and the density of foreign bodies 4
5 respectively, β kink denotes the kink kinetic coefficient, and n 1 the density of growth units in the system, m is a function of the interfacial free energy difference between the different phases m = (γ sf - γ sc )/γ cf (5) (γ is the interfacial free energy, subscripts f, c and s denote the fluid-phase, the cluster of the crystalline phase and the foreign body, respectively), and f(m)=1/4(2-3m+m 3 ) (6) f (m)=1/2(1- m) (7) Notice that f(m) is a factor describing the lowering of the nucleation barrier G* due to the occurrence of foreign bodies (or substrate). f(m) = G * / (8) * G homo In the equations, G * is the actual nucleation barrier and * G homo is the homogeneous nucleation barrier, m ( 1 m 1) can be approximately regarded as cosθ (θ is the contact angle between the nucleating phase and the substrate (15,16)). Both f(m) and f (m) change from 0 to 1, depending on the correlation and the structure match between the nucleating phase (ice) and the substrate (foreign bodies) (17,18). When the interaction between the nucleating phase and the substrate is optimal, one has m 1 and f(m) 0 (cf. Eq. (6)). On the other hand, if the interaction between the nucleating phase and the substrate is very poor, one has m -1 and f(m) 1 (cf. Eqs. (6) and (7)), meaning that the substrate exerts almost no influence on nucleation. Under such conditions, the nucleation of ice will become very difficult. As demonstrated by our experiments (see Section Result and Discussions and Table I), we cannot completely eliminate the influence of foreign bodies, such as dust particles, 5
6 which will in most cases promote ice nucleation. Therefore, in order to inhibit ice nucleation any antifreeze agent should be able to disrupt the interaction between ice nuclei and foreign bodies. Apart from surpassing the nucleation barrier, the nucleation of ice is also affected by the incorporation of H 2 O molecules onto the surface of ice nuclei at the kink sites (cf. Fig. 1 (a)). The rate of kink kinetics is described by β kink. β kink is associated with G kink, the energy barrier to be overcome in order to remove other molecules adsorbed at the kink sites (cf. Fig. 1(c)), and is given by β kink ~ exp(- G kink / kt ) (9) Obviously, the adsorption of additives on the surface of ice, in particular, at the kink sites (cf. Fig. 1(b)), will enhance G kink by ( G kink) = G kink - G kink (cf. Fig.1(c), G kink denotes the kink kinetics barrier attributed to the adsorption of impurities/additives on the surface). Consequently, the integration of H 2 O units into ice crystals will be significantly slowed down or even terminated due to a very low β kink (or high G kink) (cf. Eq. (9)). Notice that one of the most common ways to examine the nucleation kinetics is to measure the induction time t nucl of nucleation at different supercoolings instead of a direct measurement of the nucleation rate (cf. Eq. (2)) (13). However, due to the crystallization sequence, what one then measures is the induction time t i for crystallization, which is defined as the mean time lapse for the appearance of the first crystal in the liquid. Actually, t i includes the nucleation induction time t nucl, and the time t g necessarily required for ice crystals to grow from the critical size r c to an observable size. Since the free energy barrier of 3D nucleation is much higher than that of growth, the growth of crystals then becomes in most cases much easier than nucleation. This is exactly the case for ice crystallization: 6
7 once ice nuclei are formed, the rapid growth rate leads to instant freezing of the whole water droplet in less than 0.5 second. This implies that we have t g << t nucl, and then t i t nucl. According to the definition of the nucleation rate, one has J = 1/(t nucl V) = 1/(t i V) (10) where V is the volume of the water droplet in the experiment. Combining Eqs. (2), (9) and (10) yields ln( t nucl V) = κf(m)/( Τ) 2 + G kink / kt - ln{ f (m)[ f(m)] 1/2 B } (11) where s 0 B' = 4πa( R ) 2 N CB, which remains constant under a given condition (C is constant). It follows from Eq. (11) that for ice nucleation, the plot ln(τv) ~ 1/( Τ) 2 will give rise to a straight line for a given f(m) (and f (m)) (cf. Fig. 3a) (f(m) can be utilized to derive the key parameters associated with the kinetics of ice nucleation. See the discussions in the following sections). This equation will be applied in the following discussion to analyze the antifreeze effect of AFPs. EXPERIMENTAL PROCEDURES In our experiments, AFP III (A/F Protein Canada) was used to examine the antifreeze effect. The protein is a compact, angular structure in which the overall fold comprises numerous short β-strands and one turn of α-helix. To measure the induction time of ice nucleation, a newly developed experimental technique, the so-called double oil layer micro-sized crystallization technique (12) was employed. This technique can minimize the influence of the container and dust particles on ice nucleation, and also allow us to examine the effect of antifreeze proteins on ice nucleation kinetics quantitatively. 7
8 The experiments of micro-sized ice crystallization were performed in a micro-sized water droplet, which was suspended in two layers of immiscible oil in a circular quartz cell (12). Firstly, the lower layer of oil (Silicon Oil AR 1000 from Fluka), which has a larger density than water, was injected into the quartz cell up to one-half of its volume. Secondly, a drop of pure water or AFP III solution was carefully injected onto the surface of the oil using a micro syringe. Thirdly, an oil (200/500cS Fluid from Dow Corning) with a density smaller than water was injected to fill the cell, which covers the water droplet and the lower oil layer. A glass cover slip was then placed on the top of the cell to avoid evaporation. Due to the density differences, the water droplet is suspended between the two layers of immiscible oils. In order to minimize the effect of dust particles, before the water and oils were injected into the cell, they were filtered twice using 20nm filters to remove big particles. The water used in the experiments was in a highly pure deionized form (18.2 MΩ). The ice crystallization was controlled by a Linkam THMS 600 Heating and Freezing stage, which is capable of controlling the temperature within 0.1 o C from the range of 192 to o C where the cell was mounted. Nucleation was observed using a polarized transmitted microscope (Olympus, BX60-F) to which a 3 CCD color video camera (Panasonic, KY- F55BE) with an S-VHS video recorder (Panasonic AG-MD830) was attached (Fig. 2). Any ice crystal occurring in the drop could immediately be detected by a polarized microscope. RESULTS AND DISCUSSION 8
9 Our experiments show that under normal crystallization conditions, it is almost impossible to eliminate the influence of dust particles. This is evidenced by the fact that the freezing temperature (for a constant droplet volume) decreases progressively as the pore size of the filters is decreases progressively from 200nm, to 100nm to 20 nm (cf. Table I). Actually, in most cases, the term homogenous ice crystallization, to which most authors refer (19), is a heterogeneous ice nucleation process promoted by dust particles. This implies that the effect of the dust particles on ice crystallization is inevitable, and should be taken into account in our discussion. Just as an ice nucleation substrate does, so do foreign bodies always lower the nucleation barrier by a factor f (cf. Eq. (8)). In the case of nucleation promotion, the adsorption of additives on foreign particles will improve the interaction and/or the structural match between the substrate (foreign particles) and the nucleating phase. This will then result in m 1 and f 0. Since for a given nucleation system, κ is constant under a given condition (see Eqs. (3) and (11)), such a change can then be identified from the lowering of the slope and the increase of the intercept of ln(τv) ~ 1/( Τ) 2 plot(cf. Eq. (11)). The shift from curve 0 to curve 1 in Fig. 3(a) illustrates this change. Conversely, if the adsorption of additives leads to a stronger repulsion and an interfacial structure mismatch between the substrate and the nucleating phase, one has then m -1 and f 1. This corresponds to an increase in the nucleation barrier (cf. Eq. (8)). The effect can be identified from the increase in the slope f(m) of ln(τv) ~ 1/( Τ) 2 and the decrease of the intercept (from line 0 to line 2 in Fig. 3(a)). Apart from the aforementioned effect, AFP III may also adsorb onto the surface of ice nuclei, which, as shown in Fig. 1(b) and (c), will enhance G kink. According to Eq. (11), 9
10 the variation in the intercept of the ln(τv) ~ 1/( Τ) 2 plot at a constant f(m) corresponds to the change in G kink / kt, as illustrated by Fig. 3(b). In our experiments, AFP III was added to deionized water at 0.05%wt and 0.25%wt. When AFP molecules adsorb on these substrates (foreign particles) (cf. Fig. 5(a)), the interaction and the structure match between foreign particles and the nucleating phase will be significantly altered. As mentioned before, this adsorption on the substrate (dust particles) and the impact on nucleation can be quantified from the ln(τv) 1/( T) 2 plot. For the above experiments, the plots of deionized water (DI water) without AFP III and with AFP III are given in Fig. 4. The slopes and intercepts resulting from the linear regression for these systems are listed in Table II. It follows that ice nucleation is inhibited by AFP III (longer induction time) at the two concentrations. The two effects can be quantified by the changing in the slopes and the intercepts compared with the DI water within the range of supercoolings. For the details of calculating f(m), m, ( G kink/kt) add, κ, from the slope and the intercept of ln(τv) ~ 1/( Τ) 2, see Ref. 13. Let us look at Fig. 4 and Table II again. The adsorption of AFP III molecules on foreign particles turns out to strongly disturb the structural match between the nucleating ice and the dust particles. This can be identified from the variation of m (or f(m)), which decreases from 0.43 to 0.2 and 0.07 and the enhancement of the nucleation barrier by a factor 1.75 and 2.25, for a 0.05%wt and 0.25%wt solution, respectively. The results given in Fig.4 and Table II show that AFP III will also adsorb onto the growing ice nuclei. As illustrated in Fig. 5(b), the adsorption will suppress the incorporation of water molecules into the ice nuclei so as to inhibit ice crystallization. This 10
11 can be seen from the increases in the desolvation kink kinetics barrier G kink. (13.7kT for 0.05%wt solution, 13.9kT for 0.25%wt solution, cf. Table II). Note that as mentioned previously, in order to change the nucleation kinetics of ice the AFP molecules should be able to adsorb onto either the surface of dust particles or the surface of ice nuclei as illustrated by Fig. 5(a) and (b). This implies that in the reported experimental condition, AFP III should be surface active (13). Our latest results indicate that similarly to surfactant molecules, AFP molecules will accumulate and self-assemble on the surface of water. This is due to the fact that each AFP III molecule has both the hydrophobic and the hydrophilic portions. When these molecules are introduced in the water, the hydrophobic dominant portion of the molecules will avoid water, consequently the molecules will assemble on the surface of water so as to have a portion pointing away from water (cf. Fig. 6). According to the Gibbs Equation (20) 1 dγ Γ add = (12) RT d ln a add (R: gas constant, a add : activity of AFP in the aqueous solutions and Γ add : surface excess of AFP in the chosen dividing surface), the accumulation of AFP III on the surface leads to a lowering of the surface tension γ. This is confirmed by the measurements given in Fig. 6. Note that when the surface is fully occupied (saturated) by AFP III molecules, γ will then reach its minimum. In analogy with surfactants, the further addition of AFP will cause the aggregation of AFP. This has been confirmed by our Light Scattering experiment and SEC (Size Exclusion Chromatography) (the work is in process). Therefore, the lowermost point of the curve in Fig.6 is defined as the Critical Aggregation Concentration (CAC) of the AFP. Similarly to other amphiphilic molecules, based on the surface active nature of AFP, 11
12 we can also expect a self assembly of AFP on the surface of ice and on the surface of dust particles. The adsorbed AFP III molecules will repel the approaching water molecules, causing a direct impact on ice crystallization (21). It is worth noting that the presence of the AFP III molecules on the surface of the embryos causes also the interfacial free energy γ cf between the crystalline phase c and mother phase f to decrease. Based on Eq. (3), this change will lower κ and induce nucleation promotion. However, our analysis shows that this promotion effect is not dominant compared to the other two inhibition effects caused by AFP III. In summary, we have quantified here the inhibition effect of AFP III on ice nucleation at two different concentrations. This complex effect is caused by the interaction between AFP III and ice nuclei/crystals, as well as that between AFP III and foreign particles. The adsorption of AFP III on foreign particles will disturb the structural match between the nucleating ice and dust particles, while the adsorption on the surface of growing ice will inhibit the integration of water molecules into the ice lattice. These two effects can be identified from the increase of the ice nucleation barrier and the desolvation kinetics barrier. This new understanding of the antifreeze mechanism of AFP has never been examined before, and is expected provide us with guidelines in identifying new antifreeze proteins. ACKNOWLEDGEMENTS The authors are very much indebted to Dr. C. Strom for her valuable suggestions and critical reading of the manuscript. They also greatly appreciate Dr. Shashikant Joshi for his valuable discussions and kind assistance for the recycling of AFPIII. 12
13 REFERENCES 1. Davies, P. L., and Sykes, B. D. (1997) Curr. Opin. Struct. Biol. 7, Davies, P. L., and Hew, C. L. (1990) FASEB J. 4, Knight, C. A. (2000) Nature 406, Jia, Zongchao, and Davies, P. L. (2002) TRENDS in biochemical Sciences 27, Mutaftschiev, B. (1993) Handbook of Cryst. Growth, North-Holland, Amsterdam 6. Jia, Zongchao, DeLuca, C. I., Chao, H., and Devies, P. L. (1996) Nature 384, Antson, A. A., Smith, D. J., Roper, D. I., and Lewis, S. (2001) J. Mol. Biol. 305, Knight, C. A. (2001) Crystal Growth & Design 1, Chao, H., Sonnichsen, F. D., Deluca, C. I., Sykes, B. D. and Davies, P. L. (1994) Protein Sci. 3, Yeh, Y. and Feeney, R. E. (1996) Chem. Rev. 96, Yang, D. S. C., Hon, Wai Ching, Bubanko, S., Xue, Yiqi, Seetharaman, J., Hew, C. L., and Sicheri, F. (1998) Biophys. J. 74, Du, N., and Liu, X. Y. (2002) Appl. Phys. Lett. 81, Liu, X. Y. (2001) Generic mechanism of heterogeneous nucleation and molecular interfacial effect. In Advances in Crystal Growth Research. K. Sato, Y. Furukawa, K. Nakajima, editors. Elsevier, Amsterdam Zettlemoyer, A. C. (1969) Nucleation, Dekker/NewYork 15. Liu, X. Y. (2001) J. Phys. Chem. B105, Liu, X. Y. (2001) Appl. Phys. Lett. 79,
14 17. Liu, X. Y. (2000) Langmuir 16, Liu, X. Y. (1999) J. Phys. Chem. 111, Liu, X. Y. (2000) J. Phys. Chem. 112, Adamson, A. W. (1990) Physical Chemistry of Surfaces, 5th Ed., John-Wiley & Jones, New York 21. Liu, X. Y., Sawant, P. D., and Tan, W.B. (2002) J. Am. Chem. Soc. 124,
15 Figure Captions Fig. 1(a) In the process of ice nucleation, water molecules enter kink sites on the ice surface (b) the adsorption of additives at the kink sites suppresses the approach of water molecules to the ice surface (c) enhancement of the kink kinetics barrier ( G kink ) = G kink - G kink by the adsorption of additives at the kink site. Fig. 2 Experimental setup: 1.Polarized optical microscope (Olympus BX60-F); 2. 3CCD camera (Panasonic, KY-F55BE); 3.Heating and freezing stage (Linkam THMS 600); 4. Temperature control system; 5. Computer and image processing system. 6. Illustration of the sample cell and the placement of an AFP III solution drop. The density of Oil I is lower than that of the solution, and the density of oil II is higher than that of the solution. Fig. 3(a) Illustration of the effect of m on the nucleation kinetics. The increase of m will lower the interfacial effect parameter f and the slope of the ln(τv) ~ 1/( Τ) 2 and vice versa. (b) Illustration of the change in kink kinetics and the corresponding shift in the ln(τv) ~ 1/( Τ) 2 plot. The change in the kink kinetic coefficient β kink or the kink integration barrier will cause a parallel shift upward or downward, depending on the nucleation inhibition or promotion. Fig. 4 The effect of AFP III on the ice nucleation kinetics and the corresponding shift in the ln(τv) ~1/( T) 2 plot. Fig. 5(a) Illustration of adsorption of AFP III molecules on the interface of foreign particles and liquid. The arrows show the repulsion effect caused by these adsorptions of AFP III molecules on the interface. (b) Illustration of adsorption of AFP III molecules at a kink site and suppression of water molecules approaching ice surface. 15
16 Fig. 6 The Critical Aggregation Concentration (CAC) of AFP III molecules measured by the surface tension experiment. (T = 25 C). The accumulation of AFP III on the surface leads to the lowering of the surface tension γ. When the surface is fully occupied (saturated) by AFP III molecules, γ will then reach its minimum. The minimal point of the curve is defined as the Critical Aggregation Concentration (CAC) of AFP 16
17 TABLE I. The freezing temperature (for a droplet of constant volume) is dependent on the number and size of dust particles Filter Pore Size (nm) Freezing Temperature ( C) TABLE II. The effect of AFP III on the interfacial effect parameter and kink kinetic energy barrier for the nucleation of ice Curve κf * κ f(m) G * / G * DI water + m B # ( G kink/kt) add DI Water AFPIII (0.05% wt) AFPIII (0.25% wt) DI water: Deionized water * κf is the slope of the curve. # B is the intercept of the curve + G * / G * DI water = f(m) AFP III / f(m) DI water 17
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28 J. Biol. Chem. Ice nucleation inhibition: Mechanism of antifreeze by antifreeze protein Ning Du, Yang Xiang Liu and Choy Leong Hew published online June 26, 2003 Access the most updated version of this article at doi: /jbc.M Alerts: When this article is cited When a correction for this article is posted Click here to choose from all of JBC's alerts
Ice Nucleation Inhibition
THE JOURNAL OF BIOLOGICAL CHEMISTRY Vol. 278, No. 38, Issue of September 19, pp. 36000 36004, 2003 2003 by The American Society for Biochemistry and Molecular Biology, Inc. Printed in U.S.A. MECHANISM
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