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Joint Capsule Collagen in Osteoarthrosis

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Joint Capsule Collagen in Osteoarthrosis Ann Rheum Dis: first published as 10.1136/ard.32.6.510 on 1 November 1973. Downloaded from Ann. rheum. Dis. (1973), 32, 510 Joint capsule collagen in osteoarthrosis C. HERBERT, M. I. V. JAYSON, AND A. J. BAILEY From the Department ofMedicine, University ofBristol, the Royal National Hospitalfor Rheumatic Diseases, Bath, and the Agricultural Research Council, Meat Research Institute, Langford, Bristol It has long been recognized that although osteoarth- and stability of the capsular collagen could lead to rosis is characterized by degenerative changes in the the observed symptoms. articular cartilage and bones, changes in the capsule Recent studies have established that the stability play an important part in the symptoms. The capsule of the collagen fibre depends upon the formation of becomes thickened and lacks its normal pliability, inter-molecular cross-links between the tropocollagen thus restricting normal movement (Gade, 1947; molecules making up the fibre (Bailey, 1968; Traub Apley, 1969) and resulting in pain in the joint. and Piez, 1971). These cross-links are formed Similarly, Jayson (1969) described a series of patients extracellularly through reaction of aldehydes derived with arthralgia and increased joint capsule stiffness. from specific lysine and hydroxylysine on the collagen Incision, or partial removal of the osteoarthritic molecule (see Scheme). capsule, relieves the pain and improves the range of There is now a well-documented pattern of evolu- movement and degree of deformity (Lloyd-Roberts, tion of these inter-molecular cross-links. The links 1953; Gade, 1947). The joint cavity and articular initially formed are labile Schiff-bases and may be by copyright. surfaces have no pain receptors whilst the capsule is stabilized and detected by reduction with tritiated richly supplied with pain fibres (Gardner, 1948; borohydride. Using this technique they have now Kellgren and Samuel, 1950), strongly suggesting that been characterized in normal skin, tendon, bone, and the stiffening of the capsule leads to pressure on the cartilage collagen (Fowler and Bailey, 1972), each pain receptors (Apley, 1969). The mechanical tissue revealing a unique distribution of these stiffness of the capsule depends to a large extent on reduciblecross-links. These labile bonds are, however, the fibrous protein collagen. Changes in the quantity only intermediates and are found in highest concen- http://ard.bmj.com/ Scheme Formation ofcross-links Peptide chain CH2 CH2 CH2 CH2 CH2 CH2I CH2 CH2 UCH2 CH2 CH2 CH2 on September 28, 2021 by guest. Protected enzyme II UH2 CH2 CHO> CH2 11 NaBH4 NH2 NH2 N > NH CH2 CH2 CH-OH CH-OH CH-OH CH2 CH2 CH2 CH2I CH2 CH2 I Peptide bound Schiff-base Reduced cross-link hydroxylysine cross-link Hydroxylysinonorleucine (1B2) Accepted for publication April 3, 1973 Paper presented to Heberden Society, November 24, 1972 Ann Rheum Dis: first published as 10.1136/ard.32.6.510 on 1 November 1973. Downloaded from Joint capsule collagen in osteoarthrosis 511 trations during the rapid growth period and have 1970). All the eluent from the column was collected in virtually disappeared by maturity (Bailey and 5-ml. fractions, using an automatic fraction collector. Shimokomaki, 1972) to form stable non-reducible Each fraction was then analysed for tritium activity by cross-links, the structure of which has not yet been taking aliquot (0-2 ml.), adding Bray's (1960) solution (3 ml.), and counting in a Packard Scintillation Counter. elucidated. This pattern has been established with The identity of the radioactive fractions was confirmed by each of the above tissues and it seemed likely that, if analysis of a portion on the Beckman Amino Acid a similar pattern occurred in joint capsule collagen, Analyser, using an extended (60 cm.) basic column. The it would be possible to detect any abnormalities in normal amino acids were located bypaperchromatography the collagen cross-linking in osteoarthrosis. This paper of the fractions against known standards. reports that, in osteoarthritic joints, the changes in the capsules are due to thelaying down ofnew collagen Treatment with D-penicillamine rather than to degeneration or alteration of the Samples of extensively washed osteoarthritic capsules were immersed in a solution of 0-1 or 0-001 M D- collagen already present, suggesting that it may be penicillamine (0 9 per cent NaCI; pH 7-4) for 48 hours at possible to cleave these new bonds and relieve the 380 C. Osteoarthritic capsules incubated under similar pain. conditions, but in the absence of D-penicillamine, acted as controls. To prevent bacterial contamination, the solutions were covered in a layer of toluene. Both the Material and methods treated and control samples were then analysed for Specimens of hip joint capsule were obtained from fifteen reducible cross-links and solubility changes. cadavers within 24 hours of death (age range 0 to 75 yrs). Gross observation, clinical notes, x-rays, and a study of (a) REDUCIBLE CROSS-LINKS the dissected specimens satisfied us that the joints were The treated and control samples were washed in distilled normal. water and reduced with potassium borohydride as Capsules from osteoarthritic joints (12) were specimens described above and the effect on the reducible cross-links obtained at surgery for osteoarthrosis of the hip in adult recorded. subjects (age range 30 to 70 yrs). The material was always by copyright. obtained from the same location in the joint. The hip (b) SOLUBILITY capsule was chosen because osteoarthrosis in this joint The treated and control samples were dialysed overnight frequently demands operation. to remove salt and the insoluble residue which remained Articular cartilage was dissected from the unaffected was freeze-dried and weighed. areas of the surface of the head of the femur from osteo- arthritic subjects. Preparation of intact collagen fibres Results The capsule was cleaned of adhering fat and muscular Changes with age in the reducible cross-links ofcapsule tissue and shredded in an M.S.E. Ato-Mix homogenizer (Fig. 1, overleaf) http://ard.bmj.com/ and washed with copious amounts of isotonic saline (0 9 per cent NaCl; pH 7 4) to remove soluble protein and The chromatographic elution pattern of the radio- glycosaminoglycan. Hydroxyproline determinations active components obtained from borotritide reduced showed the tissue to be over 90 per cent collagen. joint capsule (Fig. la) was found to be very similar to that previously obtained for tendon. The major Reduction of collagen fibres reducible cross-links were shown to be present in Samples (250 mg. freeze-dried tissue) of the intact collagen joint capsule, dehydro-dihydroxylysinonorleucine fibres were suspended in 0 9 per cent NaCl (pH 7 4) and (dehydro-diOH-LNL), and dehydrohydroxylysino- on September 28, 2021 by guest. Protected reduced with tritiated potassium borohydride (KB3H4) norleucine (dehydro-OH-LNL). A smaller but diluted with non-radioactive KBH4 to 10 mCi/mmol. significant proportion of an additional cross-link (30-1 weight ratio collagen: KBH4). For direct comparison present was the as yet uncharacterized Fraction C. of tissue of different ages, all samples were reduced With increasing age of the capsule, the proportion of concurrently, the KB3H4 being dissolved in the saline (0°C) these Schiff-base cross-links was found to decrease, and equal portions of the solutions being used for the whilst the reduction. The reaction was allowed to proceed for 1 hr, lysyl carbohydrate components (Fraction after which time acetic acid was added to a final pH 4 and A) increased until, at about 20 to 25 years of age, the the mixture dialysed against distilled water overnight, Schiff-bases had virtually disappeared (Fig. lb). freeze-dried, and weighed. Analysis of reducible cross-links in osteoarthritic Identification of the cross-links capsule collagen The weighed samples were hydrolysed in boiling 6N HCI Capsules obtained from patients covering the age for 24 hr. The HCI was removed by evaporation in vacuo, range 30 to 70 yrs were found (Fig. 1 c) to possess a and the hydrolysate then analysed by ion-exchange high proportion of the two reduced cross-links, chromatography, using the Technicon analyser with diOH-LNL and OH-LNL previously shown to be pyridine-formate buffers (Bailey, Peach, and Fowler, absent in all normal subjects over the age of 20 yrs. 512 Annals of the Rheumatic Diseases Ann Rheum Dis: first published as 10.1136/ard.32.6.510 on 1 November 1973. Downloaded from B1 A 2X10- B2 5X103 A A A A A AA A Ilxl0. A2PeTX103 AA E A Al C- 0 C~1 IA A A IA Phe Tyr Hylys Lys 3X10 v 2X10. 0 A2 c- -.r_ Al v2X10O lX10- E A A A' Phe Tyr Hylys Lys > - 1 0 20 40 60 80 Age (years) FIG. 2 Variation inproduction ofreducible intermolecular by copyright. cross-links (B1 + B2) in relation to the total amount of collagen with increasing age in normal subjects (o-*) and osteoarthritic subjects (A). 0 100 200 300 400 500 Elution volume (ml) 2X103 an B1 FIG. 1 Typical distribution of radioactive components c obtainedfrom an acid hydrolysate ofjoint capsule collagen reduced with tritiated borohydride and separated on a Technicon Amino Acid Analyser. (a) Normal joint capsule CL 2 X103 from subject 8 yrs old. (b) Normal joint capsule collagen http://ard.bmj.com/ over 30 yrs old. (c) Osteoarthritic joint capsule from subject 2 collagenfrom subject over 30 yrs old. Positions ofreducible B12 8 intermolecular crosslinks B1, B2, and C shown in relation u to the usual amino acids. A A A A 100 2001 I 300 t 400 '00 0- Elution volume (ml) All osteoarthritic joints so far examined have Phe Tyr Hylys Lys exhibited this unusual pattern. Obviously the t- >I_10 proportion of these is dependent on the age at onset on September 28, 2021 by guest.
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