The effects of proteolytic enzymes on the mechanical properties of adult human articular cartilage

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Kempson, G. E.^1,3; Tuke, M. A.¹; Dingle, J. T.²; Barrett, A. J.²; Horsefield, P. H.²

The effects of proteolytic enzymes on the mechanical properties of adult human articular cartilage

Biochim Biophys Acta. May 28, 1976;428(3):741-760

© Elsevier Scientific Publishing Company, Amsterdam

Affiliations

¹The Biomechanics Laboratory, Mechanical Engineering Department, Imperial College of Science and Technology, London

²The Tissue Physiology Department, Strangeways Research Laboratory, Wort's Causeway, Cambridge (U.K.)

³Present address: Department of Medical Engineering, Room E86, East Wing, Southampton General Hospital, Southampton S094XY, England
Abstract

The effects of the lysosomal proteinase cathepsin D on the mechanical properties of adult human articulage were examined in detail in 7 joints within the age rangee 21 to 72 years. The results of preliminary study on the effects of the lysosomal proteinase cathepsin B1 and clostridial collagenase on the mechanical properties of cartilage are also presented.

Cartilage which had been incubated with either cathepsin D or cathepsin B1 showed increased deformation in unixial compression perpendicular to the articular surface.

The enzyme-treated cartilage also showed decreased tensile stiffness at low values of stress. This effect was more pronounced in specimens from the deeper zone of cartilage than in specimens from the superficial zone. It was also more pronounced in specimens which were aligned perpendicular to the predominant alignment of the collagen fibres in the superficial zone than in specimens which were parallel to the collagen fibres.

At higher stresses the tensile stiffness of the treated cartilage was not significantly different from that of the untreated tissue. The tensile fracture stress of the cartilage was not significantly reduced by the action of cathepsin D.

In contrast to the effects observed with the cathepsins, the preliminary results obtained by incubating cartilage for 24 h with clostridial collagenase showed that both the tensile stiffness and the fracture stress were considerably lower than the corresponding values for the untreated tissue.

Biochemical analysis of the incubation media, and the specimens, reveled that a large proportion of the proteoglycans was released from the cartilage by each of the freeze enzymes. The proportion of the total collagen which was released from the cartilage was different for each enzyme: cathepsin D released between 0 and 1.5 per cent, cathepsin B1 released between 2.3 and 4.3 per cent and collagenase relesed between 5.3 and 27.8 per cent of the collagen after 24 h.
Links

DOI: 10.1016/0304-4165(76)90205-1

PubMed: 1276179

WoS: A1976BT72300024
History

Received: 1975-09-5

Cited Works (4)

Year	Entry
1970	Muir H, Bullough P, Maroudas A. The distribution of collagen in human articular cartilage with some of its physiological implications. J Bone Joint Surg. August 1970;52B(3):554-563.
1971	Kempson GE, Spivey CJ, Swanson SAV, Freeman MAR. Patterns of cartilage stiffness on normal and degenerate human femoral heads. J Biomech. December 1971;4(6):597-609.
1973	Kempson GE, Muir H, Pollard C, Tuke M. The tensile properties of the cartilage of human femoral condyles related to the content of collagen and glycosaminoglycans. Biochim Biophys Acta. February 28, 1973;297(2):456-472.
1970	Kempson GE, Muir H, Swanson SAV, Freeman MAR. Correlations between stiffness and the chemical constituents of cartilage on the human femoral head. Biochim Biophys Acta. July 21, 1970;215(1):70-77.

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1979	Kempson GE. Mechanical properties of articular cartilage. In: Freeman MAR, ed. Adult Articular Cartilage. 2nd ed. Kent, England: Pitman Medical; 1979:333-414.
2003	Ateshian GA, Hung CT. Functional properties of native articular cartilage. In: Guilak F, Butler DL, Goldstein SA, Mooney DJ, eds. Functional Tissue Engineering. New York, NY: Inc., Springer-Verlag; 2003:46-68.
2003	Hu JCY, Athanasiou KA. The role of mechanical forces in tissue engineering of articular cartilage. In: Guilak F, Butler DL, Goldstein SA, Mooney DJ, eds. Functional Tissue Engineering. New York, NY: Inc., Springer-Verlag; 2003:227-242.
2000	Grodzinsky AJ, Levenston ME, Jin M, Frank EH. Cartilage tissue remodeling in response to mechanical forces. Annu Rev Biomed Eng. 2000;2:691-713.
1995	Bonassar LJ, Frank EH, Murray JC, Paguio CG, Moore VL, Lark MW, Sandy JD, Wu J-J, Eyre DR, Grodzinsky AJ. Changes in cartilage composition and physical properties due to stromelysin degradation. Arthritis Rheum. February 1995;38(2):173-183.
2007	Asanbaeva A, Masuda K, Thonar EJ-MA, Klisch SM, Sah RL. Mechanisms of cartilage growth: modulation of balance between proteoglycan and collagen in vitro using chondroitinase ABC. Arthritis Rheum. January 2007;56(1):188-198.
1978	Caterson B, Lowther DA. Changes in the metabolism of the proteoglycans from sheep articular cartilage in response to mechanical stress. Biochim Biophys Acta. May 17, 1978;540(3):412-422.
1991	Kempson GE. Age-related changes in the tensile properties of human articular cartilage: a comparative study between the femoral head of the hip joint and the talus of the ankle joint. Biochim Biophys Acta. October 31, 1991;1075(3):223-230.
1993	Setton LA, Zhu W, Mow VC. The biphasic poroviscoelastic behavior of articular cartilage: role of the surface zone in governing the compressive behavior. J Biomech. April–May 1993;26(4-5):581-592.
1998	Bachrach NM, Mow VC, Guilak F. Incompressibility of the solid matrix of articular cartilage under high hydrostatic pressures. J Biomech. May 1998;31(5):445-451.
1986	Mak AF. The apparent viscoelastic behavior of articular cartilage: the contributions from the intrinsic matrix viscoelasticity and interstitial fluid flows. J Biomech Eng. May 1986;108(2):123-130.
1987	Eisenberg SR, Grodzinsky AJ. The kinetics of chemically induced nonequilibrium swelling of articular cartilage and corneal stroma. J Biomech Eng. February 1987;109(1):79-89.
1998	Wren TAL, Carter DR. A microstructural model for the tensile constitutive and failure behavior of soft skeletal connective tissues. J Biomech Eng. February 1998;120(1):55-61.
1980	Roth V, Mow VC. The intrinsic tensile behavior of the matrix of bovine articular cartilage and its variation with age. J Bone Joint Surg. October 1980;62A(7):1102-1117.
1981	Lee RC, Frank EH, Grodzinsky AJ, Roylance DK. Oscillatory compressional behavior of articular cartilage and its associated electromechanical properties. J Biomech Eng. November 1981;103(2):280-292.
1987	Frank EH, Grodzinsky AJ, Koob TJ, Eyre DR. Streaming potentials: a sensitive index of enzymatic degradation in articular cartilage. J Orthop Res. 1987;5(4):497-508.
1990	Schmidt MB, Mow VC, Chun LE, Eyre DR. Effects of proteoglycan extraction on the tensile behavior of articular cartilage. J Orthop Res. May 1990;8(3):353-363.
1998	Cohen NP, Foster RJ, Mow VC. Composition and dynamics of articular cartilage: structure, function, and maintaining healthy state. J Orthop Sports Phys Ther. October 1998;28(4):203-215.
2007	Moutos FT, Freed LE, Guilak F. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat Mater. February 2007;6(2):162-167.
2008	Ofek G, Revell CM, Hu JC, Allison DD, Grande-Allen KJ, Athanasiou KA. Matrix development in self-assembly of articular cartilage. PLoS One. July 2008;3(7):e2795.
1994	Skaggs DL, Weidenbaum M, Iatridis JC, Ratcliffe A, Mow VC. Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine. June 15, 1994;19(12):1310-1319.
2011	Bansal PN. Contrast Enhanced Computed Tomographic Imaging of Articular Cartilage: Interrelationships With Biochemical and Biomechanical Properties [PhD thesis]. Boston University; 2011.
1993	Setton LA. Effects of Intrinsic Viscoelasticity and Ion-Induced Swelling on the Mechanical Behavior of Articular Cartilage: Theory and Experiments [PhD thesis]. Columbia University; 1993.
1996	Iatridis JC. Biomechanics of the Anulus Fibrosus and Nucleus Pulposus of the Human Lumbar Intervertebral Disc and the Effects of Degeneration [PhD thesis]. Columbia University; 1996.
2000	Soltz MA. Investigation of a Boundary Friction Model for Articular Cartilage: Effects of Interstitial Fluid Pressurization and Surface Topography [PhD thesis]. Columbia University; 2000.
2001	Wang C. Digital Video Microscopy-Based Determination of Cartilage Inhomogeneity, Anisotropy and Tension -Compression Nonlinearity: Implications on Chondrocyte Environment [PhD thesis]. Columbia University; 2001.
2003	Mauck RL. Functional Tissue Engineering of Articular Cartilage: The Effect of Physical Forces on the in Vitro Growth of Engineered Constructs [PhD thesis]. Columbia University; 2003.
2005	Park S. Interstitial Fluid Flow-Dependent and Flow-Independent Mechanical and Tribological Response of Articular Cartilage [PhD thesis]. Columbia University; 2005.
2006	Chahine NO. Multi-Scale Measurements of the Mechanical and Transport Properties of Native and Engineered Articular Cartilage [PhD thesis]. Columbia University; 2006.
2007	Jiang J. The Role of Cellular Interactions in Osteochondral Graft Design and the Maintenance of a Stable Osteochondral Interface [PhD thesis]. Columbia University; 2007.
2009	Canal Guterl C. Contact Mechanics of Articular Layers: 2D Strain Fields and Their Relation to Tissue Inhomogeneity [PhD thesis]. Columbia University; 2009.
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2009	Moutos FT. Biomimetic Composite Scaffolds for the Functional Tissue Engineering of Articular Cartilage [PhD thesis]. Duke University; 2009.
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1987	Frank EH. Electromechanics of Normal and Degenerated Cartilage: Poroelastic Behavior and Electrokinetic Mechanisms [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; May 1987.
1995	Bonassar LJ. Matrix Metalloproteinase Activity and Inhibition in Articular Cartilage: Effects on Composition and Biophysical Properties and Relevance to Osteoarthritis [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; February 1995.
1996	Berkenblit SI. Spatial Localization of Cartilage Degradation Using Electromechanical Surface Spectroscopy With Variable Wavelength and Frequency [PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; June 1996.
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2006	Allen KD. Mechanical Characterization, Gene Expression, and Biosynthesis of the Porcine TMJ Disc for the Purposes of Tissue Engineering [PhD thesis]. Houston, TX: Rice University; June 2006.
2009	Ofek G. Biomechanics of the Single Chondrocyte and Its Developing Extracellular Matrix [PhD thesis]. Houston, TX: Rice University; May 2009.
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1999	Chang DG. Structure and Function Relationships of Articular Cartilage in Osteoarthritis [PhD thesis]. San Diego (UCSD), University of California; 1999.
2005	Temple MM. Age- and Site-Associated Biomechanical Weakening of Human Articular Cartilage: Relationship to Cellularity, Wear, Matrix Fragmentation and the Progression to Osteoarthritis [PhD thesis]. San Diego (UCSD), University of California; 2005.
2006	Asanbaeva A. Cartilage Growth and Remodeling: Modulation of Growth Phenotype and Tensile Integrity [PhD thesis]. San Diego (UCSD), University of California; 2006.
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