Molecular mechanisms of synovial joint lubrication

Abstract Current models for lubrication of synovial joints, and the nature of the cartilage surface, are briefly recalled. Direct friction studies between polymers attached to surfaces are then considered, particularly the very recent demonstration of extreme friction reduction enabled by hydrated ions and by charged polymers. It is proposed that the extremely efficient lubrication observed in living joints arises from the presence of a brush-like phase of charged macromolecules at the surface of the superficial zone. This phase forms when charged macromolecules, including lubricin, superficial-zone protein, and aggrecan, cross the interface between the superficial zone and the synovial cavity as they are secreted into the synovium from within the bulk of the cartilage, and, in particular, the feasibility of such brush-like surface-phases is examined in some detail. The molecular mechanisms for the reduction in friction are proposed to be similar to those recently revealed using surface force balance studies on lubrication by charged brushes.

[1]  Jacob Klein,et al.  Reduction of frictional forces between solid surfaces bearing polymer brushes , 1994, Nature.

[2]  H. Higaki,et al.  Adaptive multimode lubrication in natural synovial joints and artificial joints , 1998, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[3]  J. Carlsten,et al.  Concentration of collagen, aggrecan and cartilage oligomeric matrix protein (COMP) in synovial fluid from equine middle carpal joints. , 2010, Equine veterinary journal.

[4]  E. Kumacheva,et al.  Interfacial sliding of polymer-bearing surfaces , 1994 .

[5]  J. Klein,et al.  Evidence for reptation in an entangled polymer melt , 1978, Nature.

[6]  P. Gennes Scaling Concepts in Polymer Physics , 1979 .

[7]  P. Pincus,et al.  Interaction between surfaces with adsorbed polymers: poor solvents , 1982 .

[8]  G. Jay,et al.  Boundary lubrication by lubricin is mediated by O-linked β(1-3)Gal-GalNAc oligosaccharides , 2001, Glycoconjugate Journal.

[9]  R. M. Kenedi,et al.  Friction and Wear Studies of Articular Cartilage: A Scanning Electron Microscope Study , 1975 .

[10]  J. Israelachvili,et al.  Effects of ambient conditions on adsorbed surfactant and polymer monolayers , 1992 .

[11]  P. G. de Gennes,et al.  Polymer solutions near an interface. Adsorption and depletion layers , 1981 .

[12]  G. Jay,et al.  Characterization of a bovine synovial fluid lubricating factor. I. Chemical, surface activity and lubricating properties. , 1992, Connective tissue research.

[13]  T. Hardingham,et al.  Macromolecular diffusion of biological polymers measured by confocal fluorescence recovery after photobleaching. , 1998, Biophysical journal.

[14]  Tomiharu Matsushita,et al.  Surface grafting of artificial joints with a biocompatible polymer for preventing periprosthetic osteolysis , 2004, Nature materials.

[15]  J. Klein Entropic interactions: neutral and end-functionalized chains in confined geometries , 2000 .

[16]  Mark Bathe,et al.  A coarse-grained molecular model for glycosaminoglycans: application to chondroitin, chondroitin sulfate, and hyaluronic acid. , 2005, Biophysical journal.

[17]  J CHARNLEY,et al.  The Lubrication of Animal Joints in Relation to Surgical Reconstruction by Arthroplasty * , 1960, Annals of the rheumatic diseases.

[18]  B. Hills Surface‐active phospholipid: a Pandora’s box of clinical applications. Part II. Barrier and lubricating properties , 2002, Internal medicine journal.

[19]  K. Ikeuchi,et al.  Influence of proteoglycan contents and of tissue hydration on the frictional characteristics of articular cartilage , 2005, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[20]  J. Buckwalter,et al.  Articular Cartilage and Osteoarthritis , 1954 .

[21]  B. Hills Identity of the joint lubricant. , 2002, The Journal of rheumatology.

[22]  R. Schneiderman,et al.  Depth-dependent compressive properties of normal aged human femoral head articular cartilage: relationship to fixed charge density. , 2001, Osteoarthritis and cartilage.

[23]  E. Kumacheva,et al.  Simple liquids confined to molecularly thin layers. I. Confinement-induced liquid-to-solid phase transitions , 1998 .

[24]  H. Chmiel,et al.  On the rheology of blood and synovial fluids , 1980 .

[25]  A. Maroudas,et al.  Further studies on the composition of human femoral head cartilage. , 1980, Annals of the rheumatic diseases.

[26]  J. Klein,et al.  Normal and Shear Forces between Adsorbed and Gelled Layers of Chitosan, a Naturally Occurring Cationic Polyelectrolyte , 2004 .

[27]  S. Alexander,et al.  Adsorption of chain molecules with a polar head a scaling description , 1977 .

[28]  E. Kumacheva,et al.  Shear forces between sliding surfaces coated with polymer brushes : The high friction regime , 1998 .

[29]  U. Raviv,et al.  Fluidity of water and of hydrated ions confined between solid surfaces to molecularly thin films : Water in confined geometries , 2004 .

[30]  F H Silver,et al.  The molecular structure of lubricating glycoprotein-I, the boundary lubricant for articular cartilage. , 1981, The Journal of biological chemistry.

[31]  Richard M. Pashley,et al.  Hydration forces between mica surfaces in electrolyte solutions , 1982 .

[32]  M. Mörgelin,et al.  Age-related changes in the composition, the molecular stoichiometry and the stability of proteoglycan aggregates extracted from human articular cartilage. , 2003, The Biochemical journal.

[33]  A. Maroudas,et al.  Structure of proteoglycans from different layers of human articular cartilage. , 1983, The Biochemical journal.

[34]  C. McCutchen Sponge-hydrostatic and weeping bearings. , 1959, Nature.

[35]  D. Swann,et al.  The lubricating activity of human synovial fluids. , 1984, Arthritis and rheumatism.

[36]  S. Kobayashi,et al.  Cryoscanning electron microscopic study of the surface amorphous layer of articular cartilage. , 1995, Journal of anatomy.

[37]  H. Muir,et al.  Hyaluronic acid in human articular cartilage. Age-related changes in content and size. , 1988, The Biochemical journal.

[38]  Véronique Lefebvre,et al.  The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. , 2005, The Journal of clinical investigation.

[39]  P. Gennes Polymers at an interface. 2. Interaction between two plates carrying adsorbed polymer layers , 1982 .

[40]  D Dowson,et al.  "Boosted lubrication" in synovial joints by fluid entrapment and enrichment. , 1968, Annals of the rheumatic diseases.

[41]  J. Klein Shear, Friction, and Lubrication Forces Between Polymer-Bearing Surfaces , 1996 .

[42]  D. Dowson,et al.  The effect of stationary loading on the friction and boundary lubrication of articular cartilage in the mixed lubrication regime , 1995 .

[43]  U. Raviv,et al.  Fluidity of Bound Hydration Layers , 2002, Science.

[44]  Portland Press Ltd Delayed aggregation of proteoglycans in adult human articular cartilage , 1984 .

[45]  K. Kuettner,et al.  Articular cartilage superficial zone protein (SZP) is homologous to megakaryocyte stimulating factor precursor and Is a multifunctional proteoglycan with potential growth-promoting, cytoprotective, and lubricating properties in cartilage metabolism. , 1999, Biochemical and biophysical research communications.

[46]  Uri Raviv,et al.  Shear and Frictional Interactions between Adsorbed Polymer Layers in a Good Solvent , 2001 .

[47]  Duncan Dowson,et al.  The Rheology of Synovial Fluid and Some Potential Synthetic Lubricants for Degenerate Synovial Joints , 1978 .

[48]  P. Pincus,et al.  Colloid stabilization with grafted polyelectrolytes , 1991 .

[49]  B. Schumacher,et al.  Immunodetection and partial cDNA sequence of the proteoglycan, superficial zone protein, synthesized by cells lining synovial joints , 1999, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[50]  P. G. de Gennes,et al.  Polymers at an interface; a simplified view , 1987 .

[51]  A. Engel,et al.  Surface and subsurface morphology of bovine humeral articular cartilage as assessed by atomic force and transmission electron microscopy. , 1996, Journal of structural biology.

[52]  J. Klein Forces between mica surfaces bearing adsorbed macromolecules in liquid media , 1983 .

[53]  S. M. Kilbey,et al.  Shear Forces between Tethered Polymer Chains as a Function of Compression, Sliding Velocity, and Solvent Quality , 2003 .

[54]  B. Toole Cell Biology of Extracellular Matrix , 1981, Springer US.

[55]  K. Ishihara,et al.  Raman Spectroscopic Study on the Structure of Water in Aqueous Polyelectrolyte Solutions , 2000 .

[56]  E. Thonar,et al.  Hyaluronate in articular cartilage: Age-related changes , 1978, Calcified Tissue Research.

[57]  B. Hills,et al.  Surface-active phospholipid as the lubricating component of lubricin. , 1998, British journal of rheumatology.

[58]  R. Schneiderman,et al.  Aggrecan turnover in human articular cartilage: use of aspartic acid racemization as a marker of molecular age. , 1998, Archives of biochemistry and biophysics.

[59]  D. Dowson,et al.  Micro-Elastohydrodynamic Squeeze-Film Lubrication of Compliant Layered Surfaces Firmly Bonded to a Rigid Substrate , 1997 .

[60]  M. Laberge,et al.  Sliding Friction Analysis of Phosphatidylcholine as a Boundary Lubricant for Articular Cartilage , 1993, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[61]  A. Poole Proteoglycans in health and disease: structures and functions. , 1986, The Biochemical journal.

[62]  P. Luckham,et al.  Long-range attractive forces between two mica surfaces in an aqueous polymer solution , 1984, Nature.

[63]  Grest Interfacial Sliding of Polymer Brushes: A Molecular Dynamics Simulation. , 1996, Physical review letters.

[64]  S. Ali,et al.  Differences in the rates of aggregation of proteoglycans from human articular cartilage and chondrosarcoma. , 1983, Biochemical Journal.

[65]  J. Klein Surface Forces with Adsorbed and Grafted Polymers , 1988 .

[66]  P. Patwari,et al.  Individual cartilage aggrecan macromolecules and their constituent glycosaminoglycans visualized via atomic force microscopy. , 2003, Journal of structural biology.

[67]  M. Bayliss,et al.  The Organization of Aggrecan in Human Articular Cartilage , 2000, The Journal of Biological Chemistry.

[68]  K. Higashitani,et al.  Silica surfaces lubrication by hydrated cations adsorption from electrolyte solutions. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[69]  S. Milner,et al.  Polymer Brushes , 1991, Science.

[70]  G. Jay,et al.  Comparison of the boundary-lubricating ability of bovine synovial fluid, lubricin, and Healon. , 1998, Journal of biomedical materials research.

[71]  Jacob Klein,et al.  Shear of molecularly confined liquid crystals. 1. Orientation and transitions under confinement , 1997 .

[72]  F. Silver,et al.  The molecular structure and lubricating activity of lubricin isolated from bovine and human synovial fluids. , 1985, The Biochemical journal.

[73]  Robert L Sah,et al.  Synthesis of proteoglycan 4 by chondrocyte subpopulations in cartilage explants, monolayer cultures, and resurfaced cartilage cultures. , 2004, Arthritis and rheumatism.

[74]  J. Klein,et al.  Sliding friction with polymer brushes. , 2003, Physical review letters.

[75]  R. Jerome,et al.  Direct Measurements of Interactions between Hydrophobically Anchored Strongly Charged Polyelectrolyte Brushes , 2000 .

[76]  H. Jasin,et al.  Characterization of the macromolecular components of the articular cartilage surface , 1998, Rheumatology International.

[77]  J. Block,et al.  A novel proteoglycan synthesized and secreted by chondrocytes of the superficial zone of articular cartilage. , 1994, Archives of biochemistry and biophysics.

[78]  F. Albert Cotton,et al.  Advanced Inorganic Chemistry , 1999 .

[79]  M. Huggins Viscoelastic Properties of Polymers. , 1961 .

[80]  C. McCutchen The frictional properties of animal joints , 1962 .

[81]  K. Kendall,et al.  Surface energy and the contact of elastic solids , 1971, Proceedings of the Royal Society of London. A. Mathematical and Physical Sciences.

[82]  D. Heinegård,et al.  Identification and Characterization of Asporin , 2001, The Journal of Biological Chemistry.

[83]  G A Ateshian,et al.  A theoretical formulation for boundary friction in articular cartilage. , 1997, Journal of biomechanical engineering.

[84]  G. Ateshian,et al.  Removal of the superficial zone of bovine articular cartilage does not increase its frictional coefficient. , 2004, Osteoarthritis and cartilage.

[85]  T. Nakamura,et al.  Role of uppermost superficial surface layer of articular cartilage in the lubrication mechanism of joints , 2001, Journal of anatomy.

[86]  C. McCutchen,et al.  Mechanism of Animal Joints: Sponge-hydrostatic and Weeping Bearings , 1959, Nature.

[87]  Teruo Murakami,et al.  The Lubrication in Natural Synovial Joints and Joint Prostheses , 1990 .

[88]  J. Buckwalter,et al.  Age‐Related changes in cartilage proteoglycans: Quantitative electron microscopic studies , 1994, Microscopy research and technique.

[89]  O. Borisov,et al.  Diagram of the States of a Grafted Polyelectrolyte Layer , 1994 .

[90]  F. P. Bowden,et al.  Friction: An Introduction to Tribology , 1973 .

[91]  Gerard A. Ateshian,et al.  The Role of Interstitial Fluid Pressurization and Surface Porosities on the Boundary Friction of Articular Cartilage , 1998 .

[92]  Uri Raviv,et al.  Fluidity of water confined to subnanometre films , 2001, Nature.

[93]  G. Stachowiak,et al.  The morphology and composition of the superficial zone of mammalian articular cartilage , 1993 .

[94]  U. Steiner,et al.  Complete Wetting from Polymer Mixtures , 1992, Science.

[95]  D Dowson,et al.  Human joint lubrication. , 1969, Biomedical engineering.

[96]  K. Jacobson,et al.  The dynamic structure of the pericellular matrix on living cells , 1993, The Journal of cell biology.

[97]  Monika Kopacz,et al.  Experimental verification of the role of interstitial fluid pressurization in cartilage lubrication , 2004, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[98]  M. Doi Transition behaviour from de Gennes-type motion to Rouse's of a polymer chain in fixed network , 1975 .

[99]  D. C. Evans,et al.  The shear properties of Langmuir—Blodgett layers , 1982, Proceedings of the Royal Society of London. A. Mathematical and Physical Sciences.

[100]  J. Klein,et al.  Forces between polymer-bearing surfaces undergoing shear , 1991, Nature.

[101]  J. Peyron,et al.  Articular Cartilage and Osteoarthritis, Workshop Conference Hoechst Werk Kalle-Albert , 1993 .

[102]  J. Klein The Onset of Entangled Behavior in Semidilute and Concentrated Polymer Solutions , 1978 .

[103]  T. Witten,et al.  Stress relaxation in the lamellar copolymer mesophase , 1990 .

[104]  C. P. Winlove,et al.  Measurement of the charge properties of articular cartilage by an electrokinetic method , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[105]  M. Venn Variation of chemical composition with age in human femoral head cartilage. , 1978, Annals of the rheumatic diseases.

[106]  Gerard A. Ateshian,et al.  The Role of Osmotic Pressure and Tension-Compression Nonlinearity in the Frictional Response of Articular Cartilage , 2003 .

[107]  G. J. Fleer,et al.  Effect of Free Polymer on the Structure of a Polymer Brush and Interaction between Two Polymer Brushes , 1994 .

[108]  Van C. Mow,et al.  Recent Developments in Synovial Joint Biomechanics , 1980 .

[109]  J. Klein Interactions, Friction and Lubrication Between Polymer-Bearing Surfaces , 2001 .

[110]  J Fisher,et al.  The Influence of Loading Time and Lubricant on the Friction of Articular Cartilage , 1996, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[111]  I ap Gwynn,et al.  The ultrastructure of mouse articular cartilage: collagen orientation and implications for tissue functionality. A polarised light and scanning electron microscope study and review. , 2005, European cells & materials.

[112]  O. Guiselin Irreversible Adsorption of a Concentrated Polymer Solution , 1992 .

[113]  J. Klein,et al.  Tissue structure and macromolecular diffusion in umbilical cord. Immobilization of endogenous hyaluronic acid. , 1983, Biochimica et biophysica acta.

[114]  Uri Raviv,et al.  Lubrication by charged polymers , 2003, Nature.