Article pubs.acs.org/Biomac
Effect of Glucosamine Sulfate on Surface Interactions and Lubrication by Hydrogenated Soy Phosphatidylcholine (HSPC) Liposomes Anastasia Gaisinskaya-Kipnis, Sabrina Jahn, Ronit Goldberg, and Jacob Klein* Department of Materials and Interfaces, Weizmann Institute of Science, 76100 Rehovot, Israel ABSTRACT: Glucosamine sulfate (GAS) is a charged monosaccharide molecule that is widely used as a treatment for osteoarthritis, a joint disease related to friction and lubrication of articular cartilage. Using a surface force balance, we examine the effect of GAS on normal and, particularly, on shear (frictional) interactions between surfaces in an aqueous environment coated with small unilamellar vesicles (SUVs), or liposomes, of hydrogenated soy phosphatidylcholine (HSPC). We examine the effect of GAS solution, pure water, and salt solution (0.15 M NaNO3) both inside and outside the vesicles. Cryoscanning electron microscopy shows a closely packed layer of liposomes whose morphology is affected only slightly by GAS. HSPC-SUVs with encapsulated GAS are stable upon shear at high compressions (>100 atm) and provide very good lubrication when immersed both in pure water and physiologicallevel salt solutions (in the latter case, the liposomes are exceptionally stable and lubricious up to >400 atm). The low friction is attributed to several parameters based on the hydration lubrication mechanism. controversy about the efficiency of GAS in osteoarthritis,23,24 long-term clinical studies over 3 years have shown moderate protective effects at the joint structure of OA patients.25 In earlier studies, we showed that gel-phase HSPC liposomes adsorbed to solid surfaces reduce sliding friction coefficients to remarkably low values of ∼2 × 10−5 in pure water and 6 × 10−4 in high salt solutions26,27 up to physiological pressures. We attributed the lubrication effect primarily to the hydration layers surrounding the zwitterionic phosphocholine headgroups of the phosphatidylcholine liposomes. The hydration water molecules are thought to be tenaciously attached, yet labile, thereby providing a ball-bearing-like effect.28 The contact pressures between the surfaces that were reached in those studies were >100 atm, comparable with the maximal pressures acting in major human synovial joints.27,29,30 Hence, apart from the usage of liposomes as drug delivery vectors 31,32 and biomembrane models,33 which have been investigated for a long time, liposomes may be used as lubrication agents for alleviating osteoarthritic conditions.34 Glucosamine (GA), which, as noted above, is used extensively as a treatment for OA,18−20 is a positively charged monosaccharide molecule. In view of some evidence that GAS provides benefit to OA sufferers,25 we examine here its possible role as a lubricant and the possibility that together with phosphatidylcholine (PC) lipids as well as PC-SUVs a synergistic effect may arise. In addition, GA can stabilize the
1. INTRODUCTION Lubrication of mammalian synovial joints involves a multifaceted interplay among various factors, including the composition and structure of the tissue as well as mechanics, that are capable of performing over a range of length and time scales. The outstanding friction, wear, and load-bearing properties of physiological articular cartilage have classically been attributed to a mixed lubrication regime that includes fluid-film lubrication of synovial fluid,1,2 interstitial fluid pressurization,3−6 and boundary lubrication between thin films adsorbed to the surface of the cartilage.7−12 Osteoarthritis has classically been associated with degenerative joint conditions such as insufficient boundary lubrication, although it may also be related to upregulation of cartilage-degradation enzymes.13 Roughening, disintegration, and progressive wear of the articular surface are typical morphological changes present in osteoarthritic conditions. The intrinsic avascular and aneural nature of the cartilage tissue provides little scope for its natural self-repair.14−16 Drug therapy for osteoarthritis (OA) is limited to symptomatic treatment.17 Glucosamine sulfate (GAS), an endogenous amino-monosaccharide synthesized from glucose, is currently used extensively as a treatment for OA.18−20 In vivo, glucosamine sulfate is a building block and a direct stimulator for the synthesis of the important cartilage components proteoglycans and glycosaminoglycans (GAGs).21 Thus, it balances cartilage cata- and anabolism and restores the proteoglycan-rich matrix.18,21 In the case of cartilage lesions, glucosamine sulfate is proposed to protect damaged cartilage from metabolic impairment.22 Despite a © XXXX American Chemical Society
Received: August 13, 2014 Revised: September 22, 2014
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vesicle as sugars do.35−41 It was found that saccharides can be used as stabilizers of frozen and freeze-dried liposomes by inhibiting both the phase separation and membrane fusion between liposomes while preventing the increase of the gel-toliquid crystalline phase-transition temperature.35,37 Another study proposed that saccharides work as a spacing matrix between liposomes and are involved in maintaining membrane permeability.39 In addition, many studies have suggested that saccharides replace the bound water around PC liposomes by direct interaction between sugars and the polar headgroup of PC lipids.35−37,42 In this study, we examine the effect of glucosamine sulfate on the normal and shear (i.e., frictional) interaction behavior of surface-attached liposomes. We systematically compare the behavior of either GAS-solution-filled or water-filled liposomes as lubricants across the different solvents as well as controls between bare mica surfaces across pure solvents. Further insight is provided by the corresponding surface morphology of the different configurations, studied using cryo-scanning electron microscopy. Our results reveal a wide range of behavior depending on the detailed configurations. Broadly, our results demonstrate that very low sliding friction arises with adsorbed liposomes containing GAS inside the vesicle measured in pure water and salt solutions, attributed to the hydration lubrication mechanism, whereas in GAS solution, greater frictional dissipation arises, attributed to bridging by the divalent sulfate ions due to charge−dipole interactions.
HSPC liposomes were prepared in pure water and in glucosamine sulfate (GAS) solution, referred to as H2O/H2O and GAS/GAS, respectively, meaning that there is the same solution inside and outside the vesicle. Liposomes with different solutions inside and outside the vesicle were prepared after dialyzing the vesicles for 7 days using a cellulose membrane (MWCO = 3500). For example, GAS/H2O and NaNO3/H2O mean that the liposomes consist of a water core in both cases but are suspended in different bulk solutions: GAS and sodium salt, respectively. In the present study, we examine the lubrication properties of two sets of three different liposomal configurations
H 2O/H 2O, GAS/H 2O, GAS/GAS
H 2O/GAS, NaNO3 /GAS, GAS/GAS
(I) (II)
where (I) describes the influence of GAS on the stability and the lubrication of the HSPC-SUVs and (II) examines the lubrication properties of HSPC-SUVs with GAS inside the vesicle in the presence of different aqueous solutions. As controls, measurements of normal and shear interactions between bare mica surfaces in GAS, pure water, and NaNO3 were carried out. 2.2.2. Dynamic Light Scattering (DLS). The size distribution of the liposomes was obtained by dynamic light scattering (DLS) 24 h after preparation prior to surface adsorption. In this study, all HSPC-SUVs configurations were measured with diameters in the range of 70 ± 10 nm. 2.2.3. Cryoscanning Electron Microscopy (Cryo-SEM). The samples were rapidly frozen in liquid ethane at −160 °C using a custom-made spring plunger, subsequently mounted on a holder, and moved to the freeze fracture apparatus (BAF 60, Leica Microsystems, Vienna) using a vacuum cryotransfer (VCT) device (model 100, Leica Microsystems, Vienna). Ice was sublimated at −80 °C for 1.5−2 h. The samples were rotary-shadowed with 3−5 nm Pt/C at an angle of 45°. Thereafter, the samples were transferred using a VCT to an Ultra 55 SEM (Zeiss, Germany) and observed at voltages of 0.9−2.5 kV by means of an in-lens secondary electron detector at a temperature of −120 °C. 2.2.4. Surface Force Balance (SFB). The surface force balance (SFB), schematic inset to Figure 3, measures normal and shear forces between atomically smooth mica substrates (either bare or coated) with unique sensitivity and resolution. The technique and detailed procedure for the SFB measurement of normal and shear forces have been previously described elsewhere.45,28,46,47 Briefly, normal forces Fn(D) and shear forces Fs(D) were measured by monitoring the bending of two orthogonal sets of springs: a vertical (normal force) spring (with spring constant Kn = 130 N/m) and a horizontal (shear force) spring (Ks = 300 N/m). Prior to every experiment, the glassware was cleaned in piranha solution (70% H2SO4, 30% H2O2) and sonicated in water (Barnstead NANOpure Diamond system, TOC < 1 ppb, 18.2 MΩ cm) and ethanol for 10 min. Stainless steel tools were passivated in 50% HNO3 followed by sonication in water and ethanol for 10 min each. All preparations were carried out in a laminar flow hood in a downstream configuration to avoid particulate contamination.48 The bending of the normal-force spring is determined using multiple beam interferometry by measuring the change in the wavelength of fringes of equal chromatic order (FECO) in response to applied motion in the normal direction.46,47 Normal forces were normalized by the mean radius of curvature of the crossed cylinders, R, i.e., as Fn/R. This value is directly proportional to the interaction energy E(D) per unit area between parallel plates a distance D apart obeying the same force vs distance law, as predicted from the Derjaguin approximation (D ≪ R), where Fn(D)/R = 2πE(D).49 The bending Δx of the shear-force spring is monitored by the change in capacitance of an air gap capacitor probe. The signal from the capacitor probe, which provides a direct measure of the shear force, is recorded simultaneously with the voltage applied to the sectored PZT, which gives a direct measure of the applied lateral motion Δx0.46 The shear force Fs = KsΔx was derived from a filtered response signal. The filtration was accomplished by an FFT algorithm in order to remove ambient noise. Typical shear force Fs traces, which
2. MATERIALS AND METHODS 2.1. Materials. NaNO3 salt (99.99% purity, Merck) was used as received at a concentration of 0.15 M for liposomal studies. Glucosamine sulfate (GAS), an aminomonosaccharide, supplied by Sigma-Aldrich as crystalline D-glucosamine 2-sulfate sodium salt (MW = 281 g/mol), was used at a concentration of 0.025−0.028 M. The chemical structure of D-glucosamine 2-sulfate sodium salt is shown is Figure 1. The pKa of glucose amine (GA) is 6.91.43 Hence, D-
Figure 1. Glucosamine sulfate sodium salt. glucosamine 2-sulfate sodium salt in solution consists of free water molecules, hydrated positively charged GA molecules, hydrated negatively charged sulfate, and Na+ hydrated counterions. The pH of its aqueous solution is ∼5.8. 2.2. Methods. 2.2.1. Liposome Preparation. We prepared small single unilamellar vesicles (SUVs) of hydrated soy phosphatidyl choline (HSPC) liposomes (16/18:0, MW = 762.10 g/mol, Tm = 53 °C). The liposomes were prepared using a lipid concentration of 0.015 M according to standard approaches.44 HSPC (99% purity, Lipoid, Germany) was dispersed in water or in GAS solution and sonicated for 30 min in order to obtain dispersed multilamellar vesicles (MLV). During the whole HSPC-SUV preparation procedure, the temperature was maintained at around 60 °C, which is above the main phase transition (Tm). Thereafter, the MLVs were progressively downsized using an extruder (Northern Lipid Inc., Burnaby, BC, Canada) through polycarbonate filters with defined pore sizes of 400 nm (5 cycles), 100 nm (5 cycles), and twice with 50 nm (10 cycles). B
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were obtained by subtracting the noise level shear force from the shear force at each separation, are shown in Figure 6. For low loads where the shear force is comparable with the noise, the frequency-dependent value of Fs (determined via an FFT algorithm) was extracted at the drive frequency of Δx0, as described previously.28 The mean pressure P between the mica surfaces is calculated as Fn/ A, where A is the contact area. A can be obtained by two different methods. The first approach is based directly on the elastic flattening of the curved surfaces mainly due to compression of the glue supporting the mica sheet. This flattening is clearly observed as a flattening of the fringes of equal chromatic order (FECO). The radius a of the contact area can be therefore measured, and the area can be calculated as A = πa2. The second approach utilized the Hertzian model of contact mechanics for nonadhering surfaces45 with A = π(FnR/K)2/3, where R is the mean radius of mica surface determined separately to each contact position and K is the mean effective modulus of the mica/glue combination. Thus, for a given contact point where a mean P(Fn = F0n) could be calculated from fringe flattening at a high load F0n, the pressure at lower loads Fn in which case no clear flattening was observed, was evaluated as P(Fn) = (F0n)·(Fn/F0n)1/3. All SFB experiments in the present study were carried out in a symmetrical configuration between two identically covered surfaces.
3. RESULTS We report the effect of glucosamine sulfate on the normal and shear interactions between opposing mica surfaces covered with HSPC-SUVs as well as on the morphology of the liposomes attached to the surfaces. We entrap GAS into HSPC-SUVs, adsorb the vesicles on atomically smooth mica surfaces, and study their behavior in the presence of pure water, salt, and GAS bulk solution compared to liposomes prepared in pure water as well as to the different solvents between bare mica surfaces. We use the surface force balance approach to measure interaction forces and cryo-SEM for prior surface morphological characterizations. 3.1. Cryo-SEM Characterization of Different Liposomal Systems. Figure 2A−C shows cryomicrographs of different liposomal configurations after adsorption onto mica surfaces. Three distinct HSPC-SUV systems with the following configurations were analyzed and compared: (A) standard H2O/H2O liposomes (similar to cryo-SEM micrographs reported in ref 50), (B) H2O/GAS liposomes, which adsorbed from pure water overnight, and (C) GAS/GAS liposomes that adsorbed overnight in the presence of GAS bulk solution and were then rinsed with pure water before freezing the sample for cryo-SEM. The final wash in case C was required to allow imaging without freezing GAS molecules in the bulk solution. All three systems exhibit close-packed layers of liposomes on the mica substrate surface, with a sparser overlayer of loosely attached, randomly distributed excess liposomes on top. This loosely attached overlayer is composed of either clustered or separate spherical liposomes and ruptured debris potentially arising from the cryo-SEM preparation protocol. In terms of size and packing density on the mica surface, the images reveal that the H2O/GAS and GAS/GAS systems exhibit similar results to those of H2O/H2O liposomes.50 The mean diameter of the liposomes on the surfaces (Figure 2A, B) appears to be around 80−90 nm, slightly larger than the DLS measurements of liposomes in suspension (70 ± 10 nm). The liposomes appear flattened in the cryo-SEM micrographs, but earlier studies of their hydrodynamic thickness50 suggest that they have a thickness around 20 nm. A simple geometrical consideration shows that a spherical liposome of 70 nm in diameter would form a 20 nm thick circular liposome with a diameter of around 82 nm, which is consistent with the cryo-
Figure 2. Cryo-SEM images of mica surfaces coated with SUV-HSPCs in the following configurations: H2O/H2O (A), H2O/GAS (B) adsorbed in water, and GAS/GAS (C) washed with water before freezing the samples.
SEM images. Generally, the adsorption of the liposomes from pure water onto the mica can be explained by the dipole− charge attraction between the zwitterionic phosphocholine headgroups exposed by the PC vesicles with the negatively charged mica surface. From the cryo-SEM image in Figure 2C, it can be seen that GAS liposomes suspended in GAS bulk solution also adsorb on mica, likely via desorption of relatively small GA+ molecules due to entropy gain. 3.2. Force Profiles in the Absence of Liposomes. Prior to the adsorption of liposomes on the mica substrates, we studied as a control the interactions across 0.1 and 0.01 M Na+ solutions, conductivity water, and 0.025 M GAS solution between bare mica surfaces. Figure 3A shows the normal forces Fn(D) as a function of surface separation D under different solvent conditions determined in the SFB. First and subsequent normal force profiles are shown for a given contact point. The C
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contact at D of several nanometers, which is driven by vdW attraction between the surfaces. With respect to the 0.1 and 0.01 M NaNO3 solutions, the following values were extracted from the DLVO fit, respectively: κ−1 = 1.6 ± 0.2 nm, ψ0 = 102 ± 13 mV, σ0 = e/ 2 ± 0.2 nm2 and κ−1 = 4.5 ± 0.6 nm, ψ0 = 105 ± 12 mV, σ0 = e/ 6 ± 0.7 nm2. Across both sodium salt solutions at large separations, long-ranged repulsion arises due to counterion pressure.45,51,53 At short separations (D ≤ 2 nm), the normal force profiles exhibit a characteristic hydration repulsion, which arises from the tightly bound hydration shells surrounding Na+ counterions between negatively charged mica surfaces, a phenomenon that has been well-described in the literature.53,28 The shear traces in the salt solution (not shown) reveal low friction arising from the hydration lubrication mechanism, as has been frequently observed before.28,54 Interactions across GAS solution (0.025 M), Figure 3A, show a short-range repulsion from 100 atm pressure.
(6) McCutchen, C. W. The frictional properties of animal joints. Wear 1962, 5, 1−17. (7) Charnley, J. The lubrication of animal joints in relation to surgical reconstruction by arthroplasty. Ann. Rheum. Dis. 1960, 19, 10−9. (8) McCutchen, C. W. Boundary lubrication by synovial fluid: demonstration and possible osmotic explanation. Fed. Proc. 1966, 25, 1061−8. (9) Schmidt, T. A.; Sah, R. L. Effect of synovial fluid on boundary lubrication of articular cartilage. Osteoarthritis Cartilage 2007, 15, 35− 47. (10) Seror, J.; Merkher, Y.; Kampf, N.; Collinson, L.; Day, A. J.; Maroudas, A.; Klein, J. Articular cartilage proteoglycans as boundary lubricants: structure and frictional interaction of surface-attached hyaluronan and hyaluronanaggrecan complexes. Biomacromolecules 2011, 12, 3432−43. (11) Walker, P. S.; Dowson, D.; Longfield, M. D.; Wright, V. “Boosted lubrication” in synovial joints by fluid entrapment and enrichment. Ann. Rheum. Dis. 1968, 27, 512−20. (12) Swann, D. A.; Slayter, H. S.; Silver, F. H. The molecularstructure of lubricating glycoprotein-I, the boundary lubricant for articular-cartilage. J. Biol. Chem. 1981, 256, 5921−5. (13) Burleigh, A.; Chanalaris, A.; Gardiner, M. D.; Driscoll, C.; Boruc, O.; Saklatvala, J.; Vincent, T. L. Joint immobilization prevents murine osteoarthritis and reveals the highly mechanosensitive nature of protease expression in vivo. Arthritis Rheum. 2012, 64, 2278−88. (14) Campbell, C. J. The healing of cartilage defects. Clin. Orthop. Relat. Res. 1969, 64, 45−63. (15) Fuller, J. A.; Ghadially, F. N. Ultrastructural observations on surgically produced partial-thickness defects in articular cartilage. Clin. Orthop. Relat. Res. 1972, 86, 193−205. (16) Mankin, H. J. The response of articular cartilage to mechanical injury. J. Bone Jt. Surg., Am. Vol. 1982, 64, 460−6. (17) Laufer, S. Osteoarthritis therapyare there still unmet needs? Rheumatology 2004, 43, i9−15. (18) Adams, M. E. Hype about glucosamine. Lancet 1999, 354, 353− 4. (19) Bennett, A. N.; Crossley, K. M.; Brukner, P. D.; Hinman, R. S. Predictors of symptomatic response to glucosamine in knee osteoarthritis: an exploratory study. Br. J. Sports Med. 2007, 41, 415−9. (20) Braham, R.; Dawson, B.; Goodman, C. The effect of glucosamine supplementation on people experiencing regular knee pain. Br. J. Sports Med. 2003, 37, 45−9. (21) Cerrato, P. L. Can these compounds curb arthritis? RN 1998, 61, 57−8. (22) da Camara, C. C.; Dowless, G. V. Glucosamine sulfate for osteoarthritis. Ann. Pharmacother. 1998, 32, 580−7. (23) Hughes, R.; Carr, A. A randomized, double-blind, placebocontrolled trial of glucosamine sulphate as an analgesic in osteoarthritis of the knee. Rheumatology 2002, 41, 279−84. (24) Cibere, J.; Kopec, J. A.; Thorne, A.; Singer, J.; Canvin, J.; Robinson, D. B.; Pope, J.; Hong, P.; Grant, E.; Esdaile, J. M. Randomized, double-blind, placebo-controlled glucosamine discontinuation trial in knee osteoarthritis. Arthritis Rheum. 2004, 51, 738−45. (25) Lee, Y. H.; Woo, J. H.; Choi, S. J.; Ji, J. D.; Song, G. G. Effect of glucosamine or chondroitin sulfate on the osteoarthritis progression: a meta-analysis. Rheumatol. Int. 2010, 30, 357−63. (26) Goldberg, R.; Schroeder, A.; Barenholz, Y.; Klein, J. Interactions between adsorbed hydrogenated soy phosphatidylcholine (HSPC) vesicles at physiologically high pressures and salt concentrations. Biophys. J. 2011, 100, 2403−11. (27) Goldberg, R.; Klein, J. Liposomes as lubricants: beyond drug delivery. Chem. Phys. Lipids 2012, 165, 374−81. (28) Raviv, U.; Klein, J. Fluidity of bound hydration layers. Science 2002, 297, 1540−3. (29) Afoke, N. Y. P.; Byers, P. D.; Hutton, W. C. Contact pressures in the human hip joint. J. Bone Jt. Surg., Br. Vol. 1987, 69, 536−41. (30) Hodge, W. A.; Fijan, R. S.; Carlson, K. L.; Burgess, R. G.; Harris, W. H.; Mann, R. W. Contact pressures in the human hip joint measured in vivo. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 2879−83.
5. CONCLUSIONS HSPC liposomes with GAS inside the vesicle adsorb spontaneously to form a close-packed liposome monolayercovered surface on a negatively charged substrate (mica). These layers are highly stable under water (H2O/GAS) and salt solution (NaNO3/GAS) upon compression and shear and provide very good lubrication (μ ≈ 10−4) up to the physiologically highest pressures of the major joints (P ≫ 100 atm); although at sufficiently high pressures, one might expect this mechanism to break down.56 The NaNO3/GAS configuration is interesting from a physiological perspective because it is at physiological salt concentrations and so resembles (to an important extent) the interaction between layers of PC lipids (which constitute the liposome membranes), particularly the shear and friction interaction between them. As far as GAS is used for OA treatment, we can say clearly that its presence in the liposomes does not perturb the very efficient lubrication by the highly hydrated phosphocholine groups, which has been adduced as being especially relevant in a biological lubrication context.60
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Author Contributions
A.G.-K. carried out the experiments and data analysis; A.G.-K., S.J., R.G., and J.K conceived the study. The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We thank the European Research Council (Advanced Grant Hydration Lube), the Israel Science Foundation, the Minerva Foundation (via a Fellowship to S.J.), and the McCutchen Foundation for their support of this work. This work was partly enabled by the historic generosity of the Harold Perlman family.
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