Contribution of Proteoglycan Osmotic Swelling Pressure to the Compressive Properties of Articular Cartilage

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2011 Aug 17

PMID 21843483

Citations 48

Authors

Eunhee Han

Silvia S Chen

Stephen M Klisch

Robert L Sah

Affiliations

Soon will be listed here.

Abstract

The negatively charged proteoglycans (PG) provide compressive resistance to articular cartilage by means of their fixed charge density (FCD) and high osmotic pressure (π(PG)), and the collagen network (CN) provides the restraining forces to counterbalance π(PG). Our objectives in this work were to: 1), account for collagen intrafibrillar water when transforming biochemical measurements into a FCD-π(PG) relationship; 2), compute π(PG) and CN contributions to the compressive behavior of full-thickness cartilage during bovine growth (fetal, calf, and adult) and human adult aging (young and old); and 3), predict the effect of depth from the articular surface on π(PG) in human aging. Extrafibrillar FCD (FCD(EF)) and π(PG) increased with bovine growth due to an increase in CN concentration, whereas PG concentration was steady. This maturation-related increase was amplified by compression. With normal human aging, FCD(EF) and π(PG) decreased. The π(PG)-values were close to equilibrium stress (σ(EQ)) in all bovine and young human cartilage, but were only approximately half of σ(EQ) in old human cartilage. Depth-related variations in the strain, FCD(EF), π(PG), and CN stress profiles in human cartilage suggested a functional deterioration of the superficial layer with aging. These results suggest the utility of the FCD-π(PG) relationship for elucidating the contribution of matrix macromolecules to the biomechanical properties of cartilage.

Citing Articles

Pivotal roles of biglycan and decorin in regulating bone mass, water retention, and bone toughness.

Hua R, Han Y, Ni Q, Fajardo R, Iozzo R, Ahmed R Bone Res. 2025; 13(1):2.

PMID: 39743559 PMC: 11693767. DOI: 10.1038/s41413-024-00380-2.

Cell Adhesion and Local Cytokine Control on Protein-Functionalized PNIPAM-co-AAc Hydrogel Microcarriers.

Rauer S, Stuwe L, Steinbeck L, de Toledo M, Fischer G, Wennemaring S Small. 2024; 21(2):e2404183.

PMID: 39535368 PMC: 11735893. DOI: 10.1002/smll.202404183.

Meniscus gene expression profiling of inner and outer zone meniscus tissue compared to cartilage and passaged monolayer meniscus cells.

Fei K, Andress B, Kelly A, Chasse D, McNulty A Sci Rep. 2024; 14(1):27423.

PMID: 39521910 PMC: 11550462. DOI: 10.1038/s41598-024-78580-3.

Cationic-motif-modified exosomes for mRNA delivery to retinal photoreceptors.

Millan Cotto H, Pathrikar T, Hakim B, Baby H, Zhang H, Zhao P J Mater Chem B. 2024; 12(30):7384-7400.

PMID: 38946491 PMC: 11323772. DOI: 10.1039/d4tb00849a.

High quality repair of osteochondral defects in rats using the extracellular matrix of antler stem cells.

Wang Y, Chu W, Zhai J, Wang W, He Z, Zhao Q World J Stem Cells. 2024; 16(2):176-190.

PMID: 38455106 PMC: 10915955. DOI: 10.4252/wjsc.v16.i2.176.

References

Armstrong C, Mow V . Variations in the intrinsic mechanical properties of human articular cartilage with age, degeneration, and water content. J Bone Joint Surg Am. 1982; 64(1):88-94. View

Sweet M, Thonar E, Immelman A . Regional distribution of water and glycosaminoglycan in immature articular cartilage. Biochim Biophys Acta. 1977; 500(1):173-86. DOI: 10.1016/0304-4165(77)90057-5. View

Maroudas A, Wachtel E, Grushko G, KATZ E, Weinberg P . The effect of osmotic and mechanical pressures on water partitioning in articular cartilage. Biochim Biophys Acta. 1991; 1073(2):285-94. DOI: 10.1016/0304-4165(91)90133-2. View

Basser P, Grodzinsky A . The Donnan model derived from microstructure. Biophys Chem. 1993; 46(1):57-68. DOI: 10.1016/0301-4622(93)87007-j. View

Thomas G, Asanbaeva A, Vena P, Sah R, Klisch S . A nonlinear constituent based viscoelastic model for articular cartilage and analysis of tissue remodeling due to altered glycosaminoglycan-collagen interactions. J Biomech Eng. 2009; 131(10):101002. PMC: 2966345. DOI: 10.1115/1.3192139. View

Mauck R, Soltz M, Wang C, Wong D, Chao P, Valhmu W . Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng. 2000; 122(3):252-60. DOI: 10.1115/1.429656. View

Schinagl R, Gurskis D, Chen A, Sah R . Depth-dependent confined compression modulus of full-thickness bovine articular cartilage. J Orthop Res. 1997; 15(4):499-506. DOI: 10.1002/jor.1100150404. View

Belcher C, Yaqub R, Fawthrop F, Bayliss M, Doherty M . Synovial fluid chondroitin and keratan sulphate epitopes, glycosaminoglycans, and hyaluronan in arthritic and normal knees. Ann Rheum Dis. 1997; 56(5):299-307. PMC: 1752377. DOI: 10.1136/ard.56.5.299. View

Bathe M, Rutledge G, Grodzinsky A, Tidor B . Osmotic pressure of aqueous chondroitin sulfate solution: a molecular modeling investigation. Biophys J. 2005; 89(4):2357-71. PMC: 1366736. DOI: 10.1529/biophysj.105.067918. View

10.

Morgelin M, Heinegard D, Engel J, Paulsson M . The cartilage proteoglycan aggregate: assembly through combined protein-carbohydrate and protein-protein interactions. Biophys Chem. 1994; 50(1-2):113-28. DOI: 10.1016/0301-4622(94)85024-0. View

11.

Klisch S, Chen S, Sah R, Hoger A . A growth mixture theory for cartilage with application to growth-related experiments on cartilage explants. J Biomech Eng. 2003; 125(2):169-79. DOI: 10.1115/1.1560144. View

12.

Williams R, Comper W . Osmotic flow caused by polyelectrolytes. Biophys Chem. 1990; 36(3):223-34. DOI: 10.1016/0301-4622(90)80028-6. View

13.

Basser P, Schneiderman R, Bank R, Wachtel E, Maroudas A . Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique. Arch Biochem Biophys. 1998; 351(2):207-19. DOI: 10.1006/abbi.1997.0507. View

14.

Thonar E, Sweet M . Maturation-related changes in proteoglycans of fetal articular cartilage. Arch Biochem Biophys. 1981; 208(2):535-47. DOI: 10.1016/0003-9861(81)90542-7. View

15.

Moger C, Arkill K, Barrett R, Bleuet P, Ellis R, Green E . Cartilage collagen matrix reorientation and displacement in response to surface loading. J Biomech Eng. 2009; 131(3):031008. DOI: 10.1115/1.3049478. View

16.

Buschmann M, Grodzinsky A . A molecular model of proteoglycan-associated electrostatic forces in cartilage mechanics. J Biomech Eng. 1995; 117(2):179-92. DOI: 10.1115/1.2796000. View

17.

Temple M, Bae W, Chen M, Lotz M, Amiel D, Coutts R . Age- and site-associated biomechanical weakening of human articular cartilage of the femoral condyle. Osteoarthritis Cartilage. 2007; 15(9):1042-52. DOI: 10.1016/j.joca.2007.03.005. View

18.

Maroudas A . Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature. 1976; 260(5554):808-9. DOI: 10.1038/260808a0. View

19.

Canal Guterl C, Hung C, Ateshian G . Electrostatic and non-electrostatic contributions of proteoglycans to the compressive equilibrium modulus of bovine articular cartilage. J Biomech. 2010; 43(7):1343-50. PMC: 2900255. DOI: 10.1016/j.jbiomech.2010.01.021. View

20.

Eisenberg S, Grodzinsky A . The kinetics of chemically induced nonequilibrium swelling of articular cartilage and corneal stroma. J Biomech Eng. 1987; 109(1):79-89. DOI: 10.1115/1.3138647. View