Contribution of glycosaminoglycans to viscoelastic tensile behavior of human ligament

Journal of Applied Physiology

Volumn 106, Issue 2, 2009, Pages 423-431

  Lujan, Trevor J ^a   Underwood, Clayton J ^a   Jacobs, Nathan T ^a   Weiss, Jeffrey A ^a,b  

^a University of Utah   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Decorin; Dermatan sulfate; Material properties; Polyethylene glycol; Tendon

Indexed keywords

CHONDROITIN ABC LYASE; COLLAGEN FIBER; COLLAGEN FIBRIL; GLYCOSAMINOGLYCAN; FIBRILLAR COLLAGEN; WATER;

ARTICLE; CADAVER; ENZYMATIC DEGRADATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN TISSUE; KNEE LIGAMENT; LIGAMENT; MATERIALS TESTING; PRIORITY JOURNAL; TENSILE STRENGTH; TISSUE CHARACTERIZATION; TISSUE STRUCTURE; VISCOELASTICITY; WATER CONTENT; BIOMECHANICS; METABOLISM; MIDDLE AGED; REPRODUCIBILITY; TIME; VISCOSITY; YOUNG MODULUS;

BIOMECHANICS; CADAVER; CHONDROITIN ABC LYASE; ELASTIC MODULUS; FIBRILLAR COLLAGENS; GLYCOSAMINOGLYCANS; HUMANS; MEDIAL COLLATERAL LIGAMENT, KNEE; MIDDLE AGED; REPRODUCIBILITY OF RESULTS; TENSILE STRENGTH; TIME FACTORS; VISCOSITY; WATER;

EID: 61949271766     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.90748.2008     Document Type: Article

References (61)

1. Al Jamal R, Roughley PJ, Ludwig MS. Effect of glycosaminoglycan degradation on lung tissue viscoelasticity. Am J Physiol Lung Cell Mol Physiol 280: L306-L315, 2001. (Pubitemid 32473223)
2. Amiel D, Frank C, Harwood F, Fronek J, Akeson W. Tendons and ligaments: a morphological and biochemical comparison. J Orthop Res 1: 257-265, 1984. (Pubitemid 14173922)
3. Bonifasi-Lista C, Lake SP, Small MS, Weiss JA. Viscoelastic properties of the human medial collateral ligament under longitudinal, transverse and shear loading. J Orthop Res 23: 67-76, 2005. (Pubitemid 40045079)
4. Boorman RS, Norman T, Matsen FA 3rd, Clark JM. Using a freeze substitution fixation technique and histological crimp analysis for characterizing regions of strain in ligaments loaded in situ. J Orthop Res 24: 793-799, 2006.
5. Bray DF, Frank CB, Bray RC. Cytochemical evidence for a proteoglycan-associated filamentous network in ligament extracellular matrix. J Orthop Res 8: 1-12, 1990.
6. Butler SL, Kohles SS, Thielke RJ, Chen C, Vanderby R Jr. Interstitial fluid flow in tendons or ligaments: a porous medium finite element simulation. Med Biol Eng Comput 35: 742-746, 1997. (Pubitemid 27519205)
7. Chahine NO, Chen FH, Hung CT, Ateshian GA. Direct measurement of osmotic pressure of glycosaminoglycan solutions by membrane osmometry at room temperature. Biophys J 89: 1543-1550, 2005.
8. Chimich D, Shrive N, Frank C, Marchuk L, Bray R. Water content alters viscoelastic behaviour of the normal adolescent rabbit medial collateral ligament. J Biomech 25: 831-837, 1992.
9. Ciarletta P, Micera S, Accoto D, Dario P. A novel microstructural approach in tendon viscoelastic modelling at the fibrillar level. J Biomech 39: 2034-2042, 2006. (Pubitemid 44038725)
10. Davey KJ, Skegg DC. The effects of high concentrations of an electrolyte on the swelling of non-metabolizing tissue slices. J Physiol 212: 641-653, 1971.
11. Elliott DM, Robinson PS, Gimbel JA, Sarver JJ, Abboud JA, Iozzo RV, Soslowsky LJ. Effect of altered matrix proteins on quasilinear viscoelastic properties in transgenic mouse tail tendons. Ann Biomed Eng 31: 599-605, 2003.
12. Findley W, Lai J, Onaran K. Creep and Relaxation of Nonlinear Viscoelastic Materials, with an Introduction to Linear Viscoelasticity. Amsterdam: North Holland, 1976.
13. Fung YC. Biomechanics: Mechanical Properties of Living Tissues. New York: Springer, 1993.
14. Gandley RE, McLaughlin MK, Koob TJ, Little SA, McGuffee LJ. Contribution of chondroitin-dermatan sulfate-containing proteoglycans to the function of rat mesenteric arteries. Am J Physiol Heart Circ Physiol 273: H952-H960, 1997.
15. Hansen KA, Weiss JA, Barton JK. Recruitment of tendon crimp with applied tensile strain. J Biomech Eng 124: 72-77, 2002.
16. Hardingham TE, Muir H, Kwan MK, Lai WM, Mow VC. Viscoelastic properties of proteoglycan solutions with varying proportions present as aggregates. J Orthop Res 5: 36-46, 1987. (Pubitemid 17038853)
17. Hascall VC, Riolo RL, Hayward J Jr, and Reynolds CC. Treatment of bovine nasal cartilage proteoglycan with chondroitinases from Flavobacterium heparinum and Proteus vulgaris. J Biol Chem 247: 4521-4528, 1972.
18. Haut RC, Powlison AC. The effects of test environment and cyclic stretching on the failure properties of human patellar tendons. J Orthop Res 8: 532-540, 1990.
19. Henninger HB, Maas SA, Underwood CJ, Whitaker RT, Weiss JA. Spatial distribution and orientation of dermatan sulfate in human medial collateral ligament. J Struct Biol 158: 33-45, 2007.
20. Huang CY, Mow VC, Ateshian GA. The role of flow-independent viscoelasticity in the biphasic tensile and compressive responses of articular cartilage. J Biomech Eng 123: 410-417, 2001.
21. Huang Y, Meek KM. Swelling studies on the cornea and sclera: the effects of pH and ionic strength. Biophys J 77: 1655-1665, 1999. (Pubitemid 129752962)
22. Ilic MZ, Carter P, Tyndall A, Dudhia J, Handley CJ. Proteoglycans and catabolic products of proteoglycans present in ligament. Biochem J 385: 381-388, 2005. (Pubitemid 40165070)
23. Koob TJ. Effects of chondroitinase-ABC on proteoglycans and swelling properties of fibrocartilage in bovine flexor tendon. J Orthop Res 7: 219-227, 1989.
24. Koob TJ, Vogel KG. Site-related variations in glycosaminoglycan content and swelling properties of bovine flexor tendon. J Orthop Res 5: 414-424, 1987.
25. Laasanen MS, Toyras J, Korhonen RK, Rieppo J, Saarakkala S, Nieminen MT, Hirvonen J, Jurvelin JS. Biomechanical properties of knee articular cartilage. Biorheology 40: 133-140, 2003.
26. Lai WM, Hou JS, Mow VC. A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng 113: 245-258, 1991.
27. Lanir Y, Salant EL, Foux A. Physico-chemical and microstructural changes in collagen fiber bundles following stretch in-vitro. Biorheology 25: 591-603, 1988. (Pubitemid 18216225)
28. Liu X, Yeh ML, Lewis JL, Luo ZP. Direct measurement of the rupture force of single pair of decorin interactions. Biochem Biophys Res Commun 338: 1342-1345, 2005. (Pubitemid 41608400)
29. Lujan TJ, Lake SP, Plaizier TA, Ellis BJ, Weiss JA. Simultaneous measurement of three-dimensional joint kinematics and ligament strains with optical methods. J Biomech Eng 127: 193-197, 2005.
30. Lujan TJ, Underwood CJ, Henninger HB, Thompson BM, Weiss JA. Effect of dermatan sulfate glycosaminoglycans on the quasi-static material properties of the human medial collateral ligament. J Orthop Res 25: 894-903, 2007.
31. Lujan TJ, Underwood CJ, Jacobs N, Weiss JA. Tissue swelling during extended material testing of ligaments (Abstract). ASME Summer Bioengineering Conference, Keystone Resort, CO, 2007.
32. Matyas JR, Anton MG, Shrive NG, Frank CB. Stress governs tissue phenotype at the femoral insertion of the rabbit MCL. J Biomech 28: 147-157, 1995.
33. Mijailovich SM, Stamenovic D, Brown R, Leith DE, Fredberg JJ. Dynamic moduli of rabbit lung tissue and pigeon ligamentum propatagiale undergoing uniaxial cyclic loading. J Appl Physiol 76: 773-782, 1994. (Pubitemid 24075625)
34. Millesi H, Reihsner R, Hamilton G, Mallinger R, Menzel EJ. Biomechanical properties of normal tendons, normal palmar aponeuroses, and tissues from patients with Dupuytren's disease subjected to elastase and chondroitinase treatment. Clin Biomech (Bristol, Avon) 10: 29-35, 1995.
35. Moon DK, Woo SL, Takakura Y, Gabriel MT, Abramowitch SD. The effects of refreezing on the viscoelastic and tensile properties of ligaments. J Biomech 39: 1153-1157, 2006.
36. Pioletti DP, Rakotomanana LR, Leyvraz PF. Strain rate effect on the mechanical behavior of the anterior cruciate ligament-bone complex. Med Eng Phys 21: 95-100, 1999.
37. Pogany G, Hernandez DJ, Vogel KG. The in vitro interaction of proteoglycans with type I collagen is modulated by phosphate. Arch Biochem Biophys 313: 102-111, 1994. (Pubitemid 124007665)
38. Provenzano PP, Heisey D, Hayashi K, Lakes R, Vanderby R Jr. Subfailure damage in ligament: a structural and cellular evaluation. J Appl Physiol 92: 362-371, 2002. (Pubitemid 34670025)
39. Puxkandl R, Zizak I, Paris O, Keckes J, Tesch W, Bernstorff S, Purslow P, Fratzl P. Viscoelastic properties of collagen: synchrotron radiation investigations and structural model. Philos Trans R Soc Lond B Biol Sci 357: 191-197, 2002. (Pubitemid 34276210)
40. Quapp KM, Weiss JA. Material characterization of human medial collateral ligament. J Biomech Eng 120: 757-763, 1998.
41. Raspanti M, Congiu T, Guizzardi S. Structural aspects of the extracellular matrix of the tendon: an atomic force and scanning electron microscopy study. Arch Histol Cytol 65: 37-43, 2002. (Pubitemid 34456597)
42. Raspanti M, Viola M, Sonaggere M, Tira ME, Tenni R. Collagen fibril structure is affected by collagen concentration and decorin. Biomacromolecules 8: 2087-2091, 2007.
43. Redaelli A, Vesentini S, Soncini M, Vena P, Mantero S, Montevecchi FM. Possible role of decorin glycosaminoglycans in fibril to fibril force transfer in relative mature tendons-a computational study from molecular to microstructural level. J Biomech 36: 1555-1569, 2003. (Pubitemid 37117361)
44. Robinson JR. Control of water content of respiring kidney slices by sodium chloride and polyethylene glycol. J Physiol 282: 285-294, 1978.
45. Robinson PS, Lin TW, Reynolds PR, Derwin KA, Iozzo RV, Soslowsky LJ. Strain-rate sensitive mechanical properties of tendon fascicles from mice with genetically engineered alterations in collagen and decorin. J Biomech Eng 126: 252-257, 2004.
46. Rubin MB, Bodner SR. A three-dimensional nonlinear model for dissipative response of soft tissue. Int J Solids Struct 39: 5081-5099, 2002.
47. Schmidt MB, Mow VC, Chun LE, Eyre DR. Effects of proteoglycan extraction on the tensile behavior of articular cartilage. J Orthop Res 8: 353-363, 1990.
48. Schuirmann DJ. A comparison of the two one-sided tests procedure and the power approach for assessing the equivalence of average bioavailability. J Pharmacokinet Biopharm 15: 657-680, 1987.
49. Scott JE. Elasticity in extracellular matrix "shape modules" of tendon, cartilage, etc. A sliding proteoglycan-filament model. J Physiol 553: 335-343, 2003.
50. Scott JE. Proteodermatan and proteokeratan sulfate (decorin, lumican/ fibromodulin) proteins are horseshoe shaped. Implications for their interactions with collagen. Biochemistry 35: 8795-8799, 1996.
51. Scott JE, Thomlinson AM. The structure of interfibrillar proteoglycan bridges (shape modules) in extracellular matrix of fibrous connective tissues and their stability in various chemical environments. J Anat 192: 391-405, 1998.
52. Sun DD, Guo XE, Likhitpanichkul M, Lai WM, Mow VC. The influence of the fixed negative charges on mechanical and electrical behaviors of articular cartilage under unconfined compression. J Biomech Eng 126: 6-16, 2004. (Pubitemid 38649187)
53. Sverdlik A, Lanir Y. Time-dependent mechanical behavior of sheep digital tendons, including the effects of preconditioning. J Biomech Eng 124: 78-84, 2002. (Pubitemid 34165118)
54. Thornton GM, Shrive NG, Frank CB. Altering ligament water content affects ligament pre-stress and creep behaviour. J Orthop Res 19: 845-851, 2001.
55. Tiderius CJ, Olsson LE, Nyquist F, Dahlberg L. Cartilage glycosaminoglycan loss in the acute phase after an anterior cruciate ligament injury: delayed gadolinium-enhanced magnetic resonance imaging of cartilage and synovial fluid analysis. Arthritis Rheum 52: 120-127, 2005. (Pubitemid 40129240)
56. Vogel KG, Paulsson M, Heinegard D. Specific inhibition of type I and type II collagen fibrillogenesis by the small proteoglycan of tendon. Biochem J 223: 587-597, 1984. (Pubitemid 15209051)
57. Woo SLY, Johnson GA, Smith BA. Mathematical modeling of ligaments and tendons. J Biomech Eng 115: 468-473, 1993.
58. Woo SLY, Orlando CA, Camp JT, Akeson WH. Effects of postmortem storage by freezing on ligament tensile behavior. J Biomech 19: 399-404, 1986.
59. Woo SL, Debski RE, Withrow JD, Janaushek MA. Biomechanics of knee ligaments. Am J Sports Med 27: 533-543, 1999.
60. Yamagata T, Saito H, Habuchi O, Suzuki S. Purification and properties of bacterial chondroitinases and chondrosulfatases. J Biol Chem 243: 1523-1535, 1968.
61. Zhu W, Mow VC, Koob TJ, Eyre DR. Viscoelastic shear properties of articular cartilage and the effects of glycosidase treatments. J Orthop Res 11: 771-781, 1993. (Pubitemid 24040158)