Abstract
The changing distributions of collagens and glycosaminoglycans have been studied at the attachments of the medial collateral ligament during postnatal development. The ligament is of particular interest because it has a fibrocartilaginous attachment to the femoral epiphysis, but a fibrous one to the tibial metaphysis. Ligaments were examined in rats killed at birth and at 2, 4, 6, 8, 10, 20, 30, 45, 60, 90 and 120 days after birth. Cryosections were immunolabelled with monoclonal and polyclonal antibodies against types I and II collagen, chondroitin 4 and 6 sulfate, dermatan and keratan sulfate. Although the ligament is attached at both ends to bones that develop from cartilage, there was a striking difference in collagen labelling. Type II collagen was only found in spicules of calcified cartilage in bone beneath the tibial enthesis after ossification had commenced, but there was a continuous band of labelling at all stages of development at the femoral enthesis. Initially, the cartilage at the femoral attachment lacked type I collagen, but by 45 days labelling was continuous from ligament to bone. Continuity of labelling was seen much earlier at the tibial enthesis, as soon as bone had formed. There were also marked changes in glycosaminoglycan distribution. Keratan sulfate was present at both entheses up to 45 days, but only at the femoral enthesis thereafter. Both attachments labelled throughout life for dermatan sulfate, but chondroitin 4 and 6 sulfate were only found at the femoral end. The results suggest that enthesial cartilage at the femoral attachment was initially derived from the cartilaginous bone rudiment but was quickly eroded on its deep surface by endochondral ossification as bone formed at the attachment site. It was replaced by fibrocartilage developing in the ligament. This mechanism allows enthesis cartilage/fibrocartilage to contribute to the growth of a bone at a secondary centre of ossification in addition to dissipating stress at the ligament-bone junction.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Benjamin M, Ralphs JR (1995) Functional and developmental anatomy of tendons and ligaments. In: Gordon SL, Blair SJ, Fine LJ (eds) Repetitive motion disorders of the upper extremity. American Academy of Orthopaedic Surgeons, Rosemont, pp 185–203
Benjamin M, Evans EJ, Rao RD, Findlay JA, Pemberton DJ (1991a) Quantitative differences in the histology of the attachment zones of the meniscal horns in the knee joint of man. J Anat 177: 127–134
Benjamin M, Tyers R, Ralphs JR (1991b) Age-related changes in tendon fibrocartilage. J Anat 179: 127–136
Benjamin M, Newell RLM, Evans EJ, Ralphs JR, Pemberton DJ (1992) The structure of the insertions of the tendons of biceps brachii, triceps and brachialis in elderly dissecting room cadavers. J Anat 180: 327–332
Beresford WA (1981) Chondroid bone, secondary cartilage and metaplasia. Urban & Schwarzenberg, Baltimore Munich
Biermann H (1957) Die Knochenbildung im Bereich periostaler-diaphysärer Sehnen- und Bandansätze. Z Zellforsch 46: 635–671
Booth FW, Tipton CM (1970) Ligamentous strength measurements in pre-pubescent and pubescent rats. Growth 34: 177–185
Caterson B, Christner JE, Baker JR (1983) Identification of a monoclonal antibody that specifically recognizes corneal and skeletal keratan sulfate. J Biol Chem 258: 8848–8854
Caterson B, Christner JE, Baker JR, Couchman JR (1985) Production and characterization of monoclonal antibodies directed against connective-tissue proteoglycans. Fed Proc 44: 386–393
Dolgo-Saburoff B (1929) Über Ursprung und Insertion der Skeletmuskeln. Anat Anz 68: 80–87
Dörlf J (1980) Migration of tendinous insertions. I. Cause and mechanism. J Anat 131: 179–195
Evans EJ, Benjamin M, Pemberton DJ (1990) Fibrocartilage in the attachment zones of the quadriceps tendon and patellar ligament of man. J Anat 171: 155–162
Ferreti A, Ippolito E, Mariani P, Puddu G (1983) Jumper's knee. Am J Sports Med 11: 58–62
Hardingham TE, Fosang AJ, Dudhia J (1992) Aggrecan, the chondroitin sulfate/keratan sulfate proteoglycan from cartilage. In: Kuettner K, Schleyerbach R, Peyron JG, Hascall VC (eds) Articular cartilage and osteoarthritis. Raven Press, New York, pp 5–20
Hedlund H, Mengarelli Widholm S, Heinegard D, Reinholt FP, Svensson O (1994) Fibromodulin distribution and association with collagen. Matrix Biol 14: 227–232
Hurov JR (1986) Soft-tissue bone interface: how do attachments of muscles, tendons, and ligaments change during growth? A light microscopic study. J Morphol 189: 313–325
Ippolito E, Postacchini F (1981) Rupture and disinsertion of the proximal attachment of the adductor longus tendon. Case report with histochemical and ultrastructural study. Ital J Orthop Traumatol 7: 79–85
Jones JR, Smibert JG, McCullough CJ, Price AB, Hutton WC (1987) Tendon implantation into bone: an experimental study. J Hand Surg [Br] 12: 306–312
Knese K-H (1979) Stützgewebe und Skelettsystem. In: Möllendorff W von (ed) Handbuch der mikroskopische Anatomie des Menschen II/5. Springer, Berlin Heidelberg New York
Knese K-H, Biermann H (1958) Die Knochenbildung an Sehnen-und Bandansätzen im Bereich ursprünglich chondraler Apophysen. Z Zellforsch 49: 142–187
Leonhardt H, Tillmann B, Töndury G, Zilles K (1987) Anatomie des Menschen. Lehrbuch und Atlas. Band I Bewegungsapparat. Thieme, Stuttgart New York
Matyas JR, Bodie D, Andersen M, Frank CB (1990) The developmental morphology of a “periosteal” ligament insertion: growth and maturation of the tibial insertion of the rabbit medial collateral ligament. J Orthop Res 8: 412–424
Merrilees MJ, Flint MH (1980) Ultrastructural study of tension and pressure zones in a rabbit flexor tendon. Am J Anat 157: 87–106
Müller W (1982) Das Knie. Form, Funktion und ligamentäre Wiederherstellungschirurgie. Springer, Berlin Heidelberg New York
Petersen H (1930) Die Organe des Skelettsystems. In: Möllendorff W von (ed) Handbuch der mikroskopische Anatomie des Menschen 2. Springer, Berlin Heidelberg New York, pp 521–678
Ploetz E (1938) Funktioneller Bay und funktionelle Anpassung der Gleitsehnen. Z Orthop Ihre Grenzgeb 67: 212–234
Rada JA, Cornuet PK, Hassell JR (1993) Regulation of corneal collagen fibrillogenesis in vitro by corneal proteoglycan (lumican and decorin) core proteins. Exp Eye Res 56: 635–648
Ralphs JR, Benjamin M (1994) The joint capsule: structure, composition, ageing and disease. J Anat 184: 503–509
Ralphs JR, Tyers RNS, Benjamin M (1992) Development of functionally distinct fibrocartilages at two sites in the quadriceps tendon of the rat: the suprapatella and the attachment to the patella. Anat Embryol 185: 181–187
Rufai A, Benjamin M, Ralphs JR (1992) Development and ageing of phenotypically distinct fibrocartilages associated with the rat Achilles tendon. Anat Embryol 186: 611–618
Rufai A, Benjamin M, Ralphs JR (1995) The development of fibrocartilage in the rat intervertebral disc. Anat Embryol 192: 53–62
Schneider H (1956) Zur Struktur der Sehnenansatzzonen. Z Anat: 119: 431–456
Shapiro F, Holtrop ME, Glimcher MJ (1977) Organization and cellular biology of the perichondrial ossification groove of Ranvier. J Bone Joint Surg [Am] 59: 703–723
Tipton CM, Matthes RD, Martin RK (1978) Influence of age and sex on the strength of bone-ligament junctions in knee joints of rats. J Bone Joint Surg [Am] 60: 230–234
Venn G, Mason RM (1985) Absence of keratan sulphate from skeletal tissues of mouse and rat. Biochem J 228: 443–450
Vialle-Presles MJ, Hartmann DJ, Franc S, Herbage D (1989) Immunohistochemical study of the biological fate of a subcutaneous bovine collagen implant in rat. Histochemistry 91: 177–184
Vogel KG, Koob TJ (1989) Structural specialization in tendons under compression. Int Rev Cytol 115: 267–293
Vogel KG, Sandy JD, Pogany G, Robbins JR (1994) Aggrecan in bovine tendon. Matrix Biol 14: 171–179
Wei X, Messner K (1996) The postnatal development of the insertions of the medial collateral ligament in the rat knee. Anat Embryol 193: 53–59
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gao, J., Messner, K., Ralphs, J.R. et al. An immunohistochemical study of enthesis development in the medial collateral ligament of the rat knee joint. Anat Embryol 194, 399–406 (1996). https://doi.org/10.1007/BF00198542
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00198542