Boundary Lubrication of Articular Cartilage: Contribution of Hyaluronan in Health and Injury

Healthy articular cartilage provides low friction properties to the synovial joint through both fluid film and boundary lubrication. Boundary lubrication, mediated by synovial fluid (SF), is important in reducing articulation-induced shear and wear. SF is composed of molecules including hyaluronan (HA), proteoglycan-4 (PRG4), and surface active phospholipids (SAPL) that have been shown to contribute to boundary lubrication. Joint injury predisposes articular cartilage to deterioration, and the mechanism of this may involve impairment of boundary lubrication function, possibly due to altered concentrations of HA, PRG4, and/or SAPL. However, clear relationships between the composition—boundary lubrication function of SF in health and injury, particularly at physiological test surfaces, remains to be established. Therefore, the goal of this dissertation was to further the understanding of the contributions of SF macromolecules, with a focus on HA, to the boundary lubrication of articular cartilage under normal and pathophysiologic conditions, and to what extent chemical augmentation of injured SF by HA can restore lubrication function of SF and articular cartilage.

SF lubrication function and composition were altered coordinately after acute joint injury. Steady-state friction coefficients were higher, while HA concentration and molecular weight (MW) were shifted to lower levels in injury SF. Supplementation in vitro of the abnormal SF with HA of physiologic MW and concentration led to a marked recovery of boundary lubrication function. Articular cartilage lubrication by HA was markedly dependent on concentration and MW, approaching the low friction coefficients of native SF particularly at the MW and concentration of HA found in normal SF. The depletion of HA from SF led to a marked increase in friction coefficients for both normal and injury SF. Additionally, lubrication function of the HA-depleted SF was recoverable to normal levels upon repletion with high MW HA.

Collectively, these results elucidate the role of HA as a boundary lubricant for articular cartilage, contributing to the understanding of the altered low-friction properties of cartilage following joint injury, and may also aid in the development of targeted clinical treatments and repair strategies designed to restore failed joint lubrication and prevent further cartilage damage.

Year	Entry
1970	Maroudas A. Distribution and diffusion of solutes in articular cartilage. Biophys J. May 1970;10(5):365-379.
1976	Maroudas A. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature. April 29, 1976;260(5554):808-809.
1979	Maroudas A. Physicochemical properties of articular cartilage. In: Freeman MAR, ed. Adult Articular Cartilage. 2nd ed. Kent, England: Pitman Medical; 1979:215-290.
2003	Browner B, Jupiter J, Levine A, Trafton P, eds. Skeletal Trauma: Basic Science, Management, and Reconstruction. Vol 2. 3rd ed. Philadelphia, PA: Saunders; 2003.
1983	Ahmed AM, Burke DL. In-vitro of measurement of static pressure distribution in synovial joints, I: tibial surface of the knee. J Biomech Eng. August 1983;105(3):216-225.
1970	Morrison JB. The mechanics of the knee joint in relation to normal walking. J Biomech. January 1970;3(1):51-61.
1968	Linn FC. Lubrication of animal joints, II: the mechanism. J Biomech. August 1, 1968;1(3):193.
1968	Maroudas A. Physicochemical properties of cartilage in the light of ion exchange theory. Biophys J. May 1968;8(5):575-595.
1979	Urban JPG, Maroudas A, Bayliss MT, Dillon J. Swelling pressures of proteoglycans at the concentrations found in cartilaginous tissues. Biorheology. 1979;16(6):447-464.
1976	Malcom LL. An Experimental Investigation of the Frictional and Deformational Responses of Articular Cartilage Interfaces to Static and Dynamic Loading [PhD thesis]. San Diego (UCSD), University of California; 1976.
2007	Schmidt TA, Gastelum NS, Nguyen QT, Schumacher BL, Sah RL. Boundary lubrication of articular cartilage: role of synovial fluid constituents. Arthritis Rheum. March 2007;56(3):882-891.
1997	Buckwalter JA, Mankin HJ. Articular cartilage, II: degeneration and osteoarthrosis, repair, regeneration, and transplantation. J Bone Joint Surg. April 1997;79A(4):612-632.
2007	Schmidt TA, Sah RL. Effect of synovial fluid on boundary lubrication of articular cartilage. Osteoarthritis Cartilage. January 2007;15(1):35-47.
1968	Walker PS, Dowson D, Longfield MD, Wright V. "Boosted lubrication" in synovial joints by fluid entrapment and enrichment. Ann Rheum Dis. 1968;27(6):512-520.
2005	Ateshian GA, Mow VC. Friction, lubrication, and wear of articular cartilage and diarthrodial joints. In: Mow VC, Huiskes R, eds. Basic Orthopaedic Biomechanics & Mechano-Biology. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2005:447-494.
1997	Buckwalter JA, Mankin HJ. Articular cartilage, I: tissue design and chondrocyte-matrix interactions. J Bone Joint Surg. April 1997;79A(4):600-611.
1994	Schumacher BL, Block JA, Schmid TM, Aydelotte MB, Kuettner KE. A novel proteoglycan synthesized and secreted by chondrocytes of the superficial zone of articular cartilage. Arch Biochem Biophys. May 1994;311(1):144-152.
2009	Gleghorn JP, Jones ARC, Flannery CR, Bonassar LJ. Boundary mode lubrication of articular cartilage by recombinant human lubricin. J Orthop Res. June 2009;27(6):771-777.
2005	Mow VC, Gu WY, Chen FH. Structure and function of articular cartilage and meniscus. In: Mow VC, Huiskes R, eds. Basic Orthopaedic Biomechanics & Mechano-Biology. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2005:181-258.
2001	Jay GD, Tantravahi U, Britt DE, Barrach HJ, Cha C-J. Homology of lubricin and superficial zone protein (SZP): products of megakaryocyte stimulating factor (MSF) gene expression by human synovial fibroblasts and articular chondrocytes localized to chromosome 1q25. J Orthop Res. July 2001;19(4):677-687.
1999	Schumacher BL, Hughes CE, Kuettner KE, Caterson B, Aydelotte MB. Immunodetection and partial cDNA sequence of the proteoglycan, superficial zone protein, synthesized by cells lining synovial joints. J Orthop Res. January 1999;17(1):110-120.
1979	Muir IHM. Biochemistry. In: Freeman MAR, ed. Adult Articular Cartilage. 2nd ed. Kent, England: Pitman Medical; 1979:145-214.
1979	Swanson SAV. Friction ,wear and lubrication. In: Freeman MAR, ed. Adult Articular Cartilage. 2nd ed. Kent, England: Pitman Medical; 1979:415-460.
2008	Gleghorn JP, Bonassar LJ. Lubrication mode analysis of articular cartilage using Stribeck surfaces. J Biomech. 2008;41(9):1910-1918.
1981	Swann DA, Slayter HS, Silver FH. The molecular structure of lubricating glycoprotein-i, the boundary lubricant for articular cartilage. J Biol Chem. June 10, 1981;256(11):5921-5925.

Year

Entry

1970

Maroudas A. Distribution and diffusion of solutes in articular cartilage. Biophys J. May 1970;10(5):365-379.

1976

Maroudas A. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature. April 29, 1976;260(5554):808-809.

1979

Maroudas A. Physicochemical properties of articular cartilage. In: Freeman MAR, ed. Adult Articular Cartilage. 2nd ed. Kent, England: Pitman Medical; 1979:215-290.

2003

Browner B, Jupiter J, Levine A, Trafton P, eds. Skeletal Trauma: Basic Science, Management, and Reconstruction. Vol 2. 3rd ed. Philadelphia, PA: Saunders; 2003.

1983

Ahmed AM, Burke DL. In-vitro of measurement of static pressure distribution in synovial joints, I: tibial surface of the knee. J Biomech Eng. August 1983;105(3):216-225.