Non-enzymic modification of tissue proteins by reducing sugars, the so-called Maillard reaction, is a prominent feature of aging. In articular cartilage, relatively high levels of the advanced glycation end product (AGE) pentosidine accumulate with age. Higher pentosidine levels have been associated with a stiffer collagen network in cartilage. However, even in cartilage, pentosidine levels themselves represent < 1 cross-link per 20 collagen molecules, and as such cannot be expected to contribute substantially to the increase in collagen network stiffness. In the present study, we investigated a broad range of Maillard reaction products in cartilage collagen in order to determine whether pentosidine serves as an adequate marker for AGE levels. Not only did the well-characterized AGEs pentosidine, Nε-(carboxymethyl)lysine, and Nε-(carboxyethyl)lysine increase with age in cartilage collagen (all P < 0.0001), but also general measures of AGE cross-linking, such as browning and fluorescence (both P < 0.0001), increased. The levels of these AGEs are all higher in cartilage collagen than in skin collagen. As a functional measure of glycation the digestibility of articular collagen by bacterial collagenase was investigated; digestibility decreased linearly with age, proportional to the extent of glycation. Furthermore, the arginine content and the sum of the hydroxylysine and lysine content of cartilage collagen decrease significantly with age (P < 0.0001 and P < 0.01 respectively), possibly due to modification by the Maillard reaction. The observed relationship between glycation and amino acid modification has not been reported previously in vivo. Our present results indicate that extensive accumulation of a variety of Maillard reaction products occurs in cartilage collagen with age. Altogether our results support the hypothesis that glycation contributes to stiffer and more brittle cartilage with advancing age.
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Research Article|
August 23 2000
Age-related accumulation of Maillard reaction products in human articular cartilage collagen
Nicole VERZIJL;
Nicole VERZIJL
*Gaubius Laboratory, Division of Vascular and Connective Tissue Research, TNO Prevention and Health, PO Box 2215, 2301 CE Leiden, The Netherlands
†Department of Rheumatology & Clinical Immunology, University Medical Center Utrecht, PO Box 85500, 3508 GA Utrecht, The Netherlands
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Jeroen DEGROOT;
Jeroen DEGROOT
*Gaubius Laboratory, Division of Vascular and Connective Tissue Research, TNO Prevention and Health, PO Box 2215, 2301 CE Leiden, The Netherlands
†Department of Rheumatology & Clinical Immunology, University Medical Center Utrecht, PO Box 85500, 3508 GA Utrecht, The Netherlands
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Esther OLDEHINKEL;
Esther OLDEHINKEL
*Gaubius Laboratory, Division of Vascular and Connective Tissue Research, TNO Prevention and Health, PO Box 2215, 2301 CE Leiden, The Netherlands
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Ruud A. BANK;
Ruud A. BANK
*Gaubius Laboratory, Division of Vascular and Connective Tissue Research, TNO Prevention and Health, PO Box 2215, 2301 CE Leiden, The Netherlands
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Suzanne R. THORPE;
Suzanne R. THORPE
‡Department of Chemistry and Biochemistry, University of South Carolina, Columbia, SC 29208, U.S.A.
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John W. BAYNES;
John W. BAYNES
‡Department of Chemistry and Biochemistry, University of South Carolina, Columbia, SC 29208, U.S.A.
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Michael T. BAYLISS;
Michael T. BAYLISS
§Department of Veterinary Basic Sciences, The Royal Veterinary College (University of London), Royal College Street, London NW1 0TU, U.K.
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Johannes W. J. BIJLSMA;
Johannes W. J. BIJLSMA
†Department of Rheumatology & Clinical Immunology, University Medical Center Utrecht, PO Box 85500, 3508 GA Utrecht, The Netherlands
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Floris P. J. G. LAFEBER;
Floris P. J. G. LAFEBER
†Department of Rheumatology & Clinical Immunology, University Medical Center Utrecht, PO Box 85500, 3508 GA Utrecht, The Netherlands
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Johan M. TEKOPPELE
Johan M. TEKOPPELE
1
*Gaubius Laboratory, Division of Vascular and Connective Tissue Research, TNO Prevention and Health, PO Box 2215, 2301 CE Leiden, The Netherlands
1To whom correspondence should be addressed (e-mail JM.TeKoppele@pg.tno.nl).
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Publisher: Portland Press Ltd
Received:
March 13 2000
Revision Received:
May 30 2000
Accepted:
June 23 2000
Online ISSN: 1470-8728
Print ISSN: 0264-6021
The Biochemical Society, London © 2000
2000
Biochem J (2000) 350 (2): 381–387.
Article history
Received:
March 13 2000
Revision Received:
May 30 2000
Accepted:
June 23 2000
Citation
Nicole VERZIJL, Jeroen DEGROOT, Esther OLDEHINKEL, Ruud A. BANK, Suzanne R. THORPE, John W. BAYNES, Michael T. BAYLISS, Johannes W. J. BIJLSMA, Floris P. J. G. LAFEBER, Johan M. TEKOPPELE; Age-related accumulation of Maillard reaction products in human articular cartilage collagen. Biochem J 1 September 2000; 350 (2): 381–387. doi: https://doi.org/10.1042/bj3500381
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