Article pubs.acs.org/Langmuir
Liposomes as Chaperone Mimics with Controllable Affinity toward Heat-Denatured Formate Dehydrogenase from Candida boidinii Makoto Yoshimoto,* Ryohei Kozono, and Naoki Tsubomura Department of Applied Molecular Bioscience, Yamaguchi University, 2-16-1 Tokiwadai, Ube 755-8611, Japan S Supporting Information *
ABSTRACT: Chaperone machinery in living systems can catch denatured enzymes and induce their reactivation. Chaperone mimics are beneficial for applying enzymatic reactions in vitro. In this work, the affinity between liposomes and thermally denatured enzymes was controlled to stabilize the enzyme activity. The model enzyme is formate dehydrogenase from Candida boidinii (CbFDH) which is a homodimer and negatively charged in the phosphate buffer solution (pH 7.2) used. The activity of free CbFDH readily decreased at 58 °C following the first-order kinetics with the half-life t1/2 of 27 min. The turbidity measurements showed that the denatured enzyme molecules formed aggregates. The liposomes composed of zwitterionic phosphatidylcholines (PCs) stabilized the CbFDH activity at 58 °C, as revealed with six different PCs. The PC liposomes were indicated to bind to the aggregate-prone enzyme molecules, allowing reactivation at 25 °C. The cofactor β-reduced nicotinamide adenine dinucleotide (NADH) also stabilized the enzyme activity. The affinity between liposomes and denatured CbFDH could be modulated by incorporating cationic 1,2-dioleoyloxy-3-trimethylammonium propane chloride (DOTAP) in PC membranes. The t1/2 values significantly increased in the presence of liposomes ([lipid] = 1.5 mM) composed of PC and DOTAP at the mole fraction f D of 0.1. On the other hand, the DOTAP-rich liposomes ( f D ≥ 0.7) showed strong affinity toward denatured CbFDH, accelerating its deactivation. The liposomes with low charge density function as chaperone mimics that can efficiently catch the denatured enzymes without interfering with their intramolecular interaction for reactivation.
1. INTRODUCTION Physicochemical conditions of fluids determine the conformation and function of biopolymers1,2 including enzymes, which have to be considered in applying the enzyme-catalyzed reactions in vitro. Conformational change of enzymes triggers intermolecular hydrophobic interaction, which results in irreversible formation of their aggregates.3 Thus, the recovery of activity of denatured enzymes through intramolecular folding reaction is kinetically competitive with the formation of aggregates.3,4 In living systems, molecular chaperones can assist the correct folding of polypeptides into proteins and prevent the formation of aggregates among denatured proteins at high temperatures.5−7 Chaperones possess a fascinating function to selectively accelerate the intramolecular reaction of proteins, which is derived from highly specialized structure and properties of the chaperones as well as the aid of cochaperones.8 The chaperone machinery is potentially useful for maintaining the quality of enzymes in vitro. Molecular chaperones themselves, however, may be deactivated under harsh conditions and difficult to be produced and purified at large scale in a cost-effective manner. In this regard, chaperone mimics (artificial chaperones) with well-controlled affinity toward denatured enzymes are recognized as useful materials that would allow promoting industrial application of enzymecatalyzed reactions. © 2014 American Chemical Society
Various types of chaperone mimics and relevant materials have been reported using detergents, polymeric materials, and gels as platforms for the interactions with denatured proteins.9−15 The key functions required for chaperone mimics are catching denatured proteins, facilitating their conformational change into the biologically active forms, and dissociating from them. In the catching process, the hydrophobic sites of denatured proteins need to be shielded through strong affinity with chaperone mimics. In the conformational change and the dissociation processes, on the other hand, the interaction should become rather mild in order to promote intramolecular interactions. The interaction between enzymes and the host materials can be weakened by adding the cochaperone-like molecules such as cyclodextrin.10,11,14,15 It is quite meaningful and challenging to control the properties of chaperone mimics to be suitable for catching denatured enzymes and at the same time for assisting the formation of their active forms without additives.16 Molecular assemblies-based materials would be advantageous as chaperone mimics because their size, morphology, hydrophobicity, and surface charge density are flexibly altered on the basis of constituent molecules.17 Received: October 18, 2014 Revised: December 16, 2014 Published: December 16, 2014 762
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as follows.31 Phospholipase D catalyzes the hydrolysis of PCs producing free choline which is oxidized by choline oxidase. The hydrogen peroxide produced by the oxidation reaction can be quantified by the peroxidase-catalyzed reaction. The total concentration of PC/DOTAP mixed liposomes was calculated on the basis of the concentration of PC measured and the molar ratio of DOTAP. Measurements of Size Distribution and ζ-Potential of Liposomes. Mean diameter Dp, size distribution, and ζ-potential of liposomes were measured in a quartz cuvette at 25 °C with the instrument ELSZ-2plus from Otsuka Electronics (Osaka, Japan). The size of liposomes was measured by the dynamic light scattering (DLS) method using a semiconductor laser with the wavelength and the fixed angle of the light of 660 nm and 160°, respectively. The diameter of liposomes was determined on the basis of Einstein−Stokes relation with a refractive index of 1.33. The size distribution was calculated with Marquardt algorithm, followed by the determination of polydispersity index (PI). ζ-Potential of liposomes was measured by the laser Doppler method with the light source at the fixed angle of 15°. All measurements were performed in triplicate. The phosphate buffer solution, which was used for diluting the liposome suspension, was filtrated through membrane pores with nominal diameter of 0.22 μm using Milex PVDF from Millipore. Preparation of CbFDH-Containing Liposomes. DOPC liposomes encapsulated with CbFDH were prepared as follows. The dry DOPC film was prepared as described above. Then, the lipid film was hydrated with the phosphate buffer solution containing 4.0 mg/mL CbFDH. The lipid−CbFDH mixture was subjected to the freezing and thawing treatments (see above), followed by extruding 11 times through 100 nm membrane pores. A part of the liposome suspension was further passed through the pores with nominal diameter of 50 nm. The free (nonencapsulated) CbFDH molecules were separated from liposome-encapsulated enzymes with a sepharose 4B column (1.0 (i.d.) × 20 cm). Each fraction collected in the GPC separation was analyzed with respect to the concentration of lipid (see above) and enzyme activity (see below) to assess the separation of the free CbFDH molecules from the enzyme-containing liposomes. Measurements of Enzyme Activity of CbFDH. Enzyme activity of CbFDH was determined at 25 ± 0.3 °C with sodium formate as substrate.32 CbFDH catalyzes oxidation of formate in the presence of NAD+ producing carbon dioxide and the reduced form of cofactor NADH. The reaction mixture initially contained 300 mM sodium formate, 1.5 mM NAD+, 40 mM sodium cholate, and CbFDH, unless otherwise indicated. Cholate at the above concentration can induce complete solubilization of liposome membranes. Therefore, the enzyme molecules within lipid membranes and inside liposomes are released into the bulk liquid. Moreover, the turbidity derived from liposomes is eliminated by the addition of cholate. For the measurements of activity of free enzyme, sodium cholate (40 mM) was also added to the reaction mixture. The NADH accumulated in the reaction mixture was continuously followed for 60 s at the absorbance at 340 nm using a spectrophotometer (V-550, Jasco, Tokyo, Japan). A quartz cuvette with optical path length of 0.5 cm was used for the measurement. The molar extinction coefficient ε340 of NADH was taken as 6300 M−1 cm−1. One unit of CbFDH is defined as the amount of enzyme that catalyzes the oxidation of 1.0 μmol of formate at 25 °C for 1.0 min. Measurements of Thermal Stability of CbFDH. The CbFDHcontaining samples with and without liposomes were incubated at 58 ± 0.3 °C in a capped plastic tube for 30 min. Aliquots (75 μL) was withdrawn periodically, and the enzyme activity in the sample was measured at 25 ± 0.3 °C as described above. To examine the effect of liposome membranes on the CbFDH activity at 25 °C, the activity was followed for 1 day with respect to the mixture of CbFDH and liposomes treated at 58 °C for 30 min at the lipid concentration of 1.5 mM. In this specific case, the activity measurements were performed in the absence of cholate. The effect of turbidity on the measurement was negligible because of the low lipid concentration. For the DOPC liposomes encapsulated with CbFDH, the stability of enzyme activity was also examined at 58 °C at the lipid concentration of 10 mM. In this case, each sampling volume for measuring the remaining activity
Liposomes are assemblies of the phospholipid molecules, which can interact with proteins through hydrophobic and electrostatic interaction involving conformational changes of the proteins.18,19 Liposomes possess fluid bilayers which can stabilize the structure and activity of enzymes.20 Liposomes are reported to exhibit chaperone-like function toward refolding intermediate of enzymes and heat- or shear-denatured ones.21−23 Phospholipids with various acyl chain length, degree of unsaturation, and charged headgroup can be used to precisely control the rigidity, hydrophobicity, and charge density of liposome membranes. The interaction of lipid assemblies with hydrogen peroxide, for example, depends significantly on the physicochemical properties of constituent lipids.24 Such characteristics of liposomes have not been utilized so far for fabricating chaperone mimics with controllable affinity toward denatured proteins. In this work, we examined the chaperone-like function of liposomes toward heat-denatured formate dehydrogenase from Candida boidinii (CbFDH). The formate dehydrogenasecatalyzed reaction is applicable to controlling redox state of dehydrogenases and the sequential reduction of carbon dioxide into methanol with the combination with other dehydrogenasecatalyzed reactions.25−27 We examined the effects of the properties of hydrophobic region of liposomes and charge density of the lipid bilayers on the affinity toward the denatured molecules for their reactivation.
2. EXPERIMENTAL SECTION Materials. Formate dehydrogenase from Candida boidinii (CbFDH, EC 1.2.1.2) was obtained from Roche Diagnostics GmbH (Mannheim, Germany). The CbFDH molecule is a homodimer with molecular mass Mr of 74 000 and isoelectric point pI of 5.4.28,29 βReduced nicotinamide adenine dinucleotide (NADH) and β-oxidized nicotinamide adenine dinucleotide (NAD+) were obtained from Oriental Yeast (Tokyo, Japan). 1,2-Dilauroyl-sn-glycero-3-phosphocholine (DLPC), 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC), 1-myristoyl-2-palmitoyl-sn-glycero-3-phosphocholine (MPPC), 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC), 1palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine (POPC), 1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC) 1,2,-dierucoyl-sn-glycero-3phosphocholine (DEPC), and 1,2-dioleoyloxy-3-trimethylammonium propane chloride (DOTAP) were obtained from NOF (Tokyo, Japan). Sodium cholate and sodium formate were obtained from Wako Pure Chemical Industries (Osaka, Japan). Sepharose 4B was obtained from Sigma-Aldrich (St. Louis, MO). 1,6-Diphenyl-1,3,5-hexatriene (DPH) was obtained from Invitrogen (Carlsbad, CA). All chemicals were used as received. Water was prepared with the instrument Elix 3UV from Millipore (Billerica, MA). The minimum resistance to the water purified was 15 MΩ cm. Preparation of Liposomes. Each PC or a mixture of PC and DOTAP was dissolved in chloroform in a round-bottom flask, and the solvent was removed with a rotary evaporator. The unsaturated lipids were further dissolved in diethyl ether, and the solvent was removed. This procedure was performed twice. The lipid film formed in a flask was placed under reduced pressure (25 mV) at f D ≥ 0.3. Effects of the cationic liposomes were examined on the stability of CbFDH activity at 58 °C in the absence (Figure 6A) and presence (Figure 6B) of NADH (100 μM). The initial concentration of biologically active enzyme was 0.83 ± 0.06 U/mL. Figure 7A shows the t1/2 values as a function of f D. In
Figure 6. Linear plot (−ln(A/A0) vs time) for the determination of first-order deactivation constant kd at 58 °C in the phosphate buffer solution (pH 7.2) for the enzyme activity of CbFDH (A) and CbFDH/NADH (B) systems with POPC/DOTAP liposomes (f D = 0.1−0.9). The initial enzyme activity was 0.83 ± 0.06 U/mL. The concentration of NADH in the CbFDH/NADH system was 100 μM. 767
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interface induced by their adsorption and desorption processes. Adequate control of relative contribution of electrostatic and hydrophobic interactions is the key to develop the chaperone mimics in the present liposomal system. The charge distribution within the enzyme molecules can also affect their thermostability43 and potentially their interaction with liposomes. Our results show that, in the process of thermal denaturation of CbFDH, the positively charged liposomes with relatively low charge density can efficiently bind to the partially denatured enzyme molecules at 58 °C without interfering with the rapid reactivation process at 25 °C. The interaction between liposomes and CbFDH is schematically illustrated in Figure 8 on the basis of all of the above observations. The
Figure 8. Schematic illustration of the interaction between thermally denatured CbFDH and liposomes. In the absence of liposome (path i), the partially denatured CbFDH molecules irreversibly form inactive aggregates. In the presence of zwitterionic PC-rich liposomes with the f D values of 0−0.1 (path ii), the aggregate-prone enzyme molecules bind to the lipid membranes. Therefore, the formation of enzyme aggregates is suppressed. The liposome-bound enzyme molecules rapidly become their biologically active forms at 25 °C. In the presence of the DOTAP-rich liposomes with the f D value of 0.7 and 0.9 (path iii), the denaturation of enzyme is enhanced on the surface of liposomes and the inactive aggregates are irreversibly formed among the enzyme molecules and liposomes.
Figure 7. (A) Half-life t1/2 of the CbFDH and CbFDH/NADH systems at 58 °C in the phosphate buffer solution suspending POPC/ DOTAP liposomes ([lipid] = 1.5 and 5.0 mM) with various fractional content f D of DOTAP. (B) Time courses of fractional CbFDH activity remained at 58 °C in the presence of liposomes with the f D value of 0.1 at the lipid concentrations of 0.56−5.0 mM. (C) Time courses obtained in the presence of liposomes with the f D value of 0.9 at the lipid concentrations of 0.56−5.0 mM. The curves in panels B and C were calculated as exp(−kdt), where kd is the first-order deactivation constant determined at each condition.
Supporting Information). The activity is practically unchanged at 25 °C, whereas the activity progressively decreases at 58 °C in a liposome concentration-dependent manner. These results clearly show that the electrostatic interaction alone can little affect the structure and catalytic activity of CbFDH. At the high temperature, conformational change of CbFDH is induced, which would involve rearrangement of intramolecular charge distribution. At the same time, the structural perturbation of liposome membranes is induced at the high temperature, as shown in Figure S3 of the Supporting Information for DOPC liposomes and as previously reported for POPC and DPPC liposomes.21,40 Perturbed membranes allow exposing their local hydrophobic sites to the bulk liquid. Thus, significant conformational change in the CbFDH molecules occurs at 58 °C through both electrostatic and hydrophobic interactions on the liposome membranes with high charge density. Hirano et al.41 reported the importance of both hydrophobic and electrostatic interactions in the disruption of negatively charged liposomes by aggregated lysozyme. Felsovalyi et al.42 reported the conformational change of proteins at the solid−liquid
interaction would be controllable on the basis of the molecular type of lipids, the charge density of liposome membranes, and the phase behavior of lipid bilayers. The liposomes with controlled charge density would be useful as chaperone mimics that can stabilize the CbFDH activity in the practical bioprocesses such as the CbFDH-catalyzed reduction of carbon dioxide.25−27,44,45
4. CONCLUSION Liposome membranes were modulated to become chaperone mimics which have affinity toward the thermally denatured CbFDH molecules for their reactivation. The deactivation rate of CbFDH at 58 °C decreased in the presence of zwitterionic liposomes composed of PCs in the phosphate buffer solution (pH 7.2). The affinity between the denatured CbFDH molecules and liposomes was modulated by introducing positive charge in the lipid membranes. The charged liposomes composed of PC and 10 mol % cationic DOTAP exhibited the chaperone-like activity toward the thermally denatured CbFDH 768
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molecules, whereas the liposomes incorporated with 90 mol % DOTAP significantly accelerated thermal deactivation of the enzyme. All of the results obtained clearly demonstrate that the zwitterionic liposomes and the liposomes with controlled charge density can function as chaperone mimics that can catch the denatured CbFDH molecules at 58 °C, allowing their rapid reactivation at 25 °C.
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ASSOCIATED CONTENT
S Supporting Information *
The method for estimation of concentration of CbFDH in DOPC liposomes, the t1/2 values of CbFDH at 58 °C with POPC/DOTAP liposomes, the effects of PC liposomes on the thermal stability of CbFDH, the linear plots for determination of first-order deactivation constant of CbFDH in the presence of PC liposomes, the temperature-dependent membrane fluidity of DOPC liposomes, the effect of liposome membrane on the reactivation of thermally denatured CbFDH, the effect of size of liposomes on the thermal stability of CbFDH in liposome suspensions, the GPC profile for the separation of free enzymes from enzyme-containing liposomes, the linear plots for the determination of t1/2 values of the liposomeencapsulated CbFDH, the physical stability of CbFDHcontaining liposomes at high temperature, and the effect of temperature on the positively charged liposome-induced conformational change of CbFDH. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected] (M.Y.). Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This work was supported in part by the Grant-in-Aid for Scientific Research (C) (no. 25420833) from Japan Society for the Promotion of Science (JSPS).
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REFERENCES
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