Abstract
The collagen fibrillar architectures in the general matrix of cartilage slices removed from both normal and osteoarthritic femoral heads were examined by both differential interference light microscopy and scanning electron microscopy. Whereas the normal general matrix contained a finely differentiated pseudo-random weave of fibrils developed from an interconnected array of radial elements, the osteoarthritic general matrix was characterised by the presence of structurally distinct regions consisting of strongly aligned radial bundles of fibrils and associated intense tangles or ‘knotted’ features. Simple structural models were developed to explore possible transformation structures based on two different types of interconnectivity in the three-dimensional fibrillar network. These models support the hypothesis that the distinctive ultrastructural features of the osteoarthritic general matrix can develop as a consequence of largely passive degradative changes occurring in the fibrillar weave originally present in the normal matrix. This could, in principle, occur independently of any new structure that might develop as a consequence of any upregulation of collagen associated with the osteoarthritic process.
Keywords: OA cartilage, fibrillar transformation model
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- Aigner T., Glückert K., von der Mark K. Activation of fibrillar collagen synthesis and phenotypic modulation of chondrocytes in early human osteoarthritic cartilage lesions. Osteoarthritis Cartilage. 1997 May;5(3):183–189. doi: 10.1016/s1063-4584(97)80013-1. [DOI] [PubMed] [Google Scholar]
- Bank R. A., Krikken M., Beekman B., Stoop R., Maroudas A., Lafeber F. P., te Koppele J. M. A simplified measurement of degraded collagen in tissues: application in healthy, fibrillated and osteoarthritic cartilage. Matrix Biol. 1997 Nov;16(5):233–243. doi: 10.1016/s0945-053x(97)90012-3. [DOI] [PubMed] [Google Scholar]
- Billinghurst R. C., Dahlberg L., Ionescu M., Reiner A., Bourne R., Rorabeck C., Mitchell P., Hambor J., Diekmann O., Tschesche H. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J Clin Invest. 1997 Apr 1;99(7):1534–1545. doi: 10.1172/JCI119316. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brandt K. D. Insights into the natural history of osteoarthritis provided by the cruciate-deficient dog. An animal model of osteoarthritis. Ann N Y Acad Sci. 1994 Sep 6;732:199–205. doi: 10.1111/j.1749-6632.1994.tb24735.x. [DOI] [PubMed] [Google Scholar]
- Broom N. D. An enzymatically induced structural transformation in articular cartilage. Its significance with respect to matrix breakdown. Arthritis Rheum. 1988 Feb;31(2):210–218. doi: 10.1002/art.1780310209. [DOI] [PubMed] [Google Scholar]
- Broom N. D. Further insights into the structural principles governing the function of articular cartilage. J Anat. 1984 Sep;139(Pt 2):275–294. [PMC free article] [PubMed] [Google Scholar]
- Broom N. D., Poole C. A. Articular cartilage collagen and proteoglycans. Their functional interdependency. Arthritis Rheum. 1983 Sep;26(9):1111–1119. doi: 10.1002/art.1780260909. [DOI] [PubMed] [Google Scholar]
- Broom N. D. Structural consequences of traumatizing articular cartilage. Ann Rheum Dis. 1986 Mar;45(3):225–234. doi: 10.1136/ard.45.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Broom N. D. The Third George Swanson Christie memorial lecture. Connective tissue function and malfunction: a biomechanical perspective. Pathology. 1988 Apr;20(2):93–104. doi: 10.3109/00313028809066618. [DOI] [PubMed] [Google Scholar]
- Broom N. D. The altered biomechanical state of human femoral head osteoarthritic articular cartilage. Arthritis Rheum. 1984 Sep;27(9):1028–1039. doi: 10.1002/art.1780270910. [DOI] [PubMed] [Google Scholar]
- Broom N. D. The altered biomechanical state of human femoral head osteoarthritic articular cartilage. Arthritis Rheum. 1984 Sep;27(9):1028–1039. doi: 10.1002/art.1780270910. [DOI] [PubMed] [Google Scholar]
- Broom N. D. The collagenous architecture of articular cartilage--a synthesis of ultrastructure and mechanical function. J Rheumatol. 1986 Feb;13(1):142–152. [PubMed] [Google Scholar]
- Bullough P. G., Yawitz P. S., Tafra L., Boskey A. L. Topographical variations in the morphology and biochemistry of adult canine tibial plateau articular cartilage. J Orthop Res. 1985;3(1):1–16. doi: 10.1002/jor.1100030101. [DOI] [PubMed] [Google Scholar]
- Chen M. H., Broom N. D. Concerning the ultrastructural origin of large-scale swelling in articular cartilage. J Anat. 1999 Apr;194(Pt 3):445–461. doi: 10.1046/j.1469-7580.1999.19430445.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen M. H., Broom N. On the ultrastructure of softened cartilage: a possible model for structural transformation. J Anat. 1998 Apr;192(Pt 3):329–341. doi: 10.1046/j.1469-7580.1998.19230329.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Diab M., Wu J. J., Eyre D. R. Collagen type IX from human cartilage: a structural profile of intermolecular cross-linking sites. Biochem J. 1996 Feb 15;314(Pt 1):327–332. doi: 10.1042/bj3140327. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dijkgraaf L. C., de Bont L. G., Boering G., Liem R. S. The structure, biochemistry, and metabolism of osteoarthritic cartilage: a review of the literature. J Oral Maxillofac Surg. 1995 Oct;53(10):1182–1192. doi: 10.1016/0278-2391(95)90632-0. [DOI] [PubMed] [Google Scholar]
- Dodge G. R., Poole A. R. Immunohistochemical detection and immunochemical analysis of type II collagen degradation in human normal, rheumatoid, and osteoarthritic articular cartilages and in explants of bovine articular cartilage cultured with interleukin 1. J Clin Invest. 1989 Feb;83(2):647–661. doi: 10.1172/JCI113929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eyre D. R., Apon S., Wu J. J., Ericsson L. H., Walsh K. A. Collagen type IX: evidence for covalent linkages to type II collagen in cartilage. FEBS Lett. 1987 Aug 17;220(2):337–341. doi: 10.1016/0014-5793(87)80842-6. [DOI] [PubMed] [Google Scholar]
- Hamerman D. Aging and osteoarthritis: basic mechanisms. J Am Geriatr Soc. 1993 Jul;41(7):760–770. doi: 10.1111/j.1532-5415.1993.tb07469.x. [DOI] [PubMed] [Google Scholar]
- Hollander A. P., Heathfield T. F., Webber C., Iwata Y., Bourne R., Rorabeck C., Poole A. R. Increased damage to type II collagen in osteoarthritic articular cartilage detected by a new immunoassay. J Clin Invest. 1994 Apr;93(4):1722–1732. doi: 10.1172/JCI117156. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hollander A. P., Pidoux I., Reiner A., Rorabeck C., Bourne R., Poole A. R. Damage to type II collagen in aging and osteoarthritis starts at the articular surface, originates around chondrocytes, and extends into the cartilage with progressive degeneration. J Clin Invest. 1995 Dec;96(6):2859–2869. doi: 10.1172/JCI118357. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hwang W. S., Li B., Jin L. H., Ngo K., Schachar N. S., Hughes G. N. Collagen fibril structure of normal, aging, and osteoarthritic cartilage. J Pathol. 1992 Aug;167(4):425–433. doi: 10.1002/path.1711670413. [DOI] [PubMed] [Google Scholar]
- Kuettner K. E. Biochemistry of articular cartilage in health and disease. Clin Biochem. 1992 Jun;25(3):155–163. doi: 10.1016/0009-9120(92)90224-g. [DOI] [PubMed] [Google Scholar]
- Lane J. M., Weiss C. Review of articular cartilage collagen research. Arthritis Rheum. 1975 Nov-Dec;18(6):553–562. doi: 10.1002/art.1780180605. [DOI] [PubMed] [Google Scholar]
- Maroudas A. I. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature. 1976 Apr 29;260(5554):808–809. doi: 10.1038/260808a0. [DOI] [PubMed] [Google Scholar]
- Maroudas A., Venn M. Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. II. Swelling. Ann Rheum Dis. 1977 Oct;36(5):399–406. doi: 10.1136/ard.36.5.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maroudas A., Ziv I., Weisman N., Venn M. Studies of hydration and swelling pressure in normal and osteoarthritic cartilage. Biorheology. 1985;22(2):159–169. doi: 10.3233/bir-1985-22206. [DOI] [PubMed] [Google Scholar]
- Miller E. J., Gay S. The collagens: an overview and update. Methods Enzymol. 1987;144:3–41. doi: 10.1016/0076-6879(87)44170-0. [DOI] [PubMed] [Google Scholar]
- Müller-Glauser W., Humbel B., Glatt M., Sträuli P., Winterhalter K. H., Bruckner P. On the role of type IX collagen in the extracellular matrix of cartilage: type IX collagen is localized to intersections of collagen fibrils. J Cell Biol. 1986 May;102(5):1931–1939. doi: 10.1083/jcb.102.5.1931. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson F., Dahlberg L., Laverty S., Reiner A., Pidoux I., Ionescu M., Fraser G. L., Brooks E., Tanzer M., Rosenberg L. C. Evidence for altered synthesis of type II collagen in patients with osteoarthritis. J Clin Invest. 1998 Dec 15;102(12):2115–2125. doi: 10.1172/JCI4853. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfander D., Rahmanzadeh R., Scheller E. E. Presence and distribution of collagen II, collagen I, fibronectin, and tenascin in rabbit normal and osteoarthritic cartilage. J Rheumatol. 1999 Feb;26(2):386–394. [PubMed] [Google Scholar]
- Pond M. J., Nuki G. Experimentally-induced osteoarthritis in the dog. Ann Rheum Dis. 1973 Jul;32(4):387–388. doi: 10.1136/ard.32.4.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poole C. A., Gilbert R. T., Herbage D., Hartmann D. J. Immunolocalization of type IX collagen in normal and spontaneously osteoarthritic canine tibial cartilage and isolated chondrons. Osteoarthritis Cartilage. 1997 May;5(3):191–204. doi: 10.1016/s1063-4584(97)80014-3. [DOI] [PubMed] [Google Scholar]
- Rizkalla G., Reiner A., Bogoch E., Poole A. R. Studies of the articular cartilage proteoglycan aggrecan in health and osteoarthritis. Evidence for molecular heterogeneity and extensive molecular changes in disease. J Clin Invest. 1992 Dec;90(6):2268–2277. doi: 10.1172/JCI116113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rüttner J. R., Spycher M. A. Electron microscopic investigations on aging and osteoarthrotic human cartilage. Preliminary report. Pathol Microbiol (Basel) 1968;31(1):14–24. doi: 10.1159/000162000. [DOI] [PubMed] [Google Scholar]
- Segawa K., Takiguchi R. Ultrastructural alteration of cartilaginous fibril arrangement in the rat mandibular condyle as revealed by high-resolution scanning electron microscopy. Anat Rec. 1992 Dec;234(4):493–499. doi: 10.1002/ar.1092340405. [DOI] [PubMed] [Google Scholar]
- Shlopov B. V., Lie W. R., Mainardi C. L., Cole A. A., Chubinskaya S., Hasty K. A. Osteoarthritic lesions: involvement of three different collagenases. Arthritis Rheum. 1997 Nov;40(11):2065–2074. doi: 10.1002/art.1780401120. [DOI] [PubMed] [Google Scholar]
- Vaughan L., Mendler M., Huber S., Bruckner P., Winterhalter K. H., Irwin M. I., Mayne R. D-periodic distribution of collagen type IX along cartilage fibrils. J Cell Biol. 1988 Mar;106(3):991–997. doi: 10.1083/jcb.106.3.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vignon E., Arlot M., Meunier P., Vignon G. Quantitative histological changes in osteoarthritic hip cartilage. Morphometric analysis of 29 osteoarthritic and 26 normal human femoral heads. Clin Orthop Relat Res. 1974;(103):269–278. [PubMed] [Google Scholar]
- Wu J. J., Eyre D. R. Covalent interactions of type IX collagen in cartilage. Connect Tissue Res. 1989;20(1-4):241–246. doi: 10.3109/03008208909023893. [DOI] [PubMed] [Google Scholar]
- Wu J. J., Eyre D. R. Structural analysis of cross-linking domains in cartilage type XI collagen. Insights on polymeric assembly. J Biol Chem. 1995 Aug 11;270(32):18865–18870. doi: 10.1074/jbc.270.32.18865. [DOI] [PubMed] [Google Scholar]
- Wu J. J., Woods P. E., Eyre D. R. Identification of cross-linking sites in bovine cartilage type IX collagen reveals an antiparallel type II-type IX molecular relationship and type IX to type IX bonding. J Biol Chem. 1992 Nov 15;267(32):23007–23014. [PubMed] [Google Scholar]
- van der Rest M., Mayne R. Type IX collagen proteoglycan from cartilage is covalently cross-linked to type II collagen. J Biol Chem. 1988 Feb 5;263(4):1615–1618. [PubMed] [Google Scholar]