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Erschienen in: Osteoporosis International 9/2013

01.09.2013 | Original Article

Differences in non-enzymatic glycation and collagen cross-links between human cortical and cancellous bone

verfasst von: L. Karim, S. Y. Tang, G. E. Sroga, D. Vashishth

Erschienen in: Osteoporosis International | Ausgabe 9/2013

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Abstract

Summary

It is important to establish the relationship between pentosidine and advanced glycation endproducts (AGEs) in bone. We found the relationship between pentosidine and AGEs and their magnitude of accumulation were dependent on bone’s surface-to-volume ratio. Results illustrate the importance of measuring pentosidine and AGEs separately in cancellous and cortical bone.

Introduction

Accumulation of collagen cross-links (AGEs) produced by non-enzymatic glycation deteriorates bone’s mechanical properties and fracture resistance. Although a single AGE, pentosidine, is commonly used as a representative marker, it is unclear whether it quantitatively reflects total fluorescent AGEs in bone. The goal of this study was to establish the relationship between pentosidine and total AGEs in cancellous and cortical bone.

Methods

Pentosidine and total AGEs were quantified in 170 human bone samples. Total fluorescent AGEs were measured in 28 additional cancellous and cortical bone specimens of the same apparent volume that were incubated in control or in vitro glycation solutions. Correlations between pentosidine and total AGEs and differences between cortical and cancellous groups were determined.

Results

Pentosidine was correlated with total AGEs in cancellous bone (r = 0.53, p < 0.0001) and weakly correlated in cortical bone (r = 0.23, p < 0.05). There was more pentosidine (p < 0.01) and total AGEs (p < 0.001) in cancellous than in cortical bone. The in vitro glycation substudy showed that cancellous bone accumulated more AGEs than cortical bone (p < 0.05).

Conclusion

The relationship between pentosidine and total AGEs and their magnitude of accumulation differed in cancellous and cortical bone of the same apparent volume, and were dependent on the surface-to-volume ratios of each sample. It is important to consider the bone types as two separate entities, and it is crucial to quantify total AGEs in addition to pentosidine to allow for more comprehensive analysis of the effects of non-enzymatic glycation in bone.
Literatur
1.
Zurück zum Zitat Paul RG, Bailey AJ (1996) Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. Int J Biochem Cell Biol 28:1297–1310PubMedCrossRef Paul RG, Bailey AJ (1996) Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. Int J Biochem Cell Biol 28:1297–1310PubMedCrossRef
2.
Zurück zum Zitat Bailey AJ, Paul RG, Knott L (1998) Mechanisms of maturation and ageing of collagen. Mech Ageing Dev 106:1–56PubMedCrossRef Bailey AJ, Paul RG, Knott L (1998) Mechanisms of maturation and ageing of collagen. Mech Ageing Dev 106:1–56PubMedCrossRef
3.
Zurück zum Zitat Vashishth D (2007) The role of the collagen matrix in skeletal fragility. Curr Osteoporos Rep 5:62–66PubMedCrossRef Vashishth D (2007) The role of the collagen matrix in skeletal fragility. Curr Osteoporos Rep 5:62–66PubMedCrossRef
4.
Zurück zum Zitat Robins SP, Bailey AJ (1972) Age-related changes in collagen: the identification of reducible lysine-carbohydrate condensation products. Biochem Biophys Res Commun 48:76–84PubMedCrossRef Robins SP, Bailey AJ (1972) Age-related changes in collagen: the identification of reducible lysine-carbohydrate condensation products. Biochem Biophys Res Commun 48:76–84PubMedCrossRef
5.
Zurück zum Zitat Knott L, Bailey AJ (1998) Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 22:181–187PubMedCrossRef Knott L, Bailey AJ (1998) Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 22:181–187PubMedCrossRef
6.
Zurück zum Zitat Ahmed N, Argirov OK, Minhas HS, Cordeiro CA, Thornalley PJ (2002) Assay of advanced glycation endproducts (AGEs): surveying AGEs by chromatographic assay with derivatization by 6-aminoquinolyl-N-hydroxysuccinimidyl-carbamate and application to Nepsilon-carboxymethyl-lysine- and Nepsilon-(1-carboxyethyl)lysine-modified albumin. Biochem J 364:1–14PubMed Ahmed N, Argirov OK, Minhas HS, Cordeiro CA, Thornalley PJ (2002) Assay of advanced glycation endproducts (AGEs): surveying AGEs by chromatographic assay with derivatization by 6-aminoquinolyl-N-hydroxysuccinimidyl-carbamate and application to Nepsilon-carboxymethyl-lysine- and Nepsilon-(1-carboxyethyl)lysine-modified albumin. Biochem J 364:1–14PubMed
7.
Zurück zum Zitat Tang SY, Zeenath U, Vashishth D (2007) Effects of non-enzymatic glycation on cancellous bone fragility. Bone 40:1144–1151PubMedCrossRef Tang SY, Zeenath U, Vashishth D (2007) Effects of non-enzymatic glycation on cancellous bone fragility. Bone 40:1144–1151PubMedCrossRef
8.
Zurück zum Zitat Saito M, Marumo K, Fujii K, Ishioka N (1997) Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal Biochem 253:26–32PubMedCrossRef Saito M, Marumo K, Fujii K, Ishioka N (1997) Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal Biochem 253:26–32PubMedCrossRef
9.
Zurück zum Zitat Sroga GE, Vashishth D (2011) UPLC methodology for identification and quantitation of naturally fluorescent crosslinks in proteins: a study of bone collagen. J Chromatogr B Analyt Technol Biomed Life Sci 879:379–385PubMedCrossRef Sroga GE, Vashishth D (2011) UPLC methodology for identification and quantitation of naturally fluorescent crosslinks in proteins: a study of bone collagen. J Chromatogr B Analyt Technol Biomed Life Sci 879:379–385PubMedCrossRef
10.
Zurück zum Zitat Vashishth D (2009) Advanced glycation end-products and bone fractures. IBMS BoneKEy 6:268–278CrossRef Vashishth D (2009) Advanced glycation end-products and bone fractures. IBMS BoneKEy 6:268–278CrossRef
11.
Zurück zum Zitat Saito M, Marumo K (2010) Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21:195–214PubMedCrossRef Saito M, Marumo K (2010) Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21:195–214PubMedCrossRef
12.
Zurück zum Zitat Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone 31:1–7PubMedCrossRef Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone 31:1–7PubMedCrossRef
13.
Zurück zum Zitat Hernandez CJ, Tang SY, Baumbach BM, Hwu PB, Sakkee AN, van der Ham F, DeGroot J, Bank RA, Keaveny TM (2005) Trabecular microfracture and the influence of pyridinium and non-enzymatic glycation-mediated collagen cross-links. Bone 37:825–832PubMedCrossRef Hernandez CJ, Tang SY, Baumbach BM, Hwu PB, Sakkee AN, van der Ham F, DeGroot J, Bank RA, Keaveny TM (2005) Trabecular microfracture and the influence of pyridinium and non-enzymatic glycation-mediated collagen cross-links. Bone 37:825–832PubMedCrossRef
14.
Zurück zum Zitat Dyer DG, Blackledge JA, Thorpe SR, Baynes JW (1991) Formation of pentosidine during nonenzymatic browning of proteins by glucose. Identification of glucose and other carbohydrates as possible precursors of pentosidine in vivo. J Biol Chem 266:11654–11660PubMed Dyer DG, Blackledge JA, Thorpe SR, Baynes JW (1991) Formation of pentosidine during nonenzymatic browning of proteins by glucose. Identification of glucose and other carbohydrates as possible precursors of pentosidine in vivo. J Biol Chem 266:11654–11660PubMed
15.
Zurück zum Zitat Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17:319–336PubMedCrossRef Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17:319–336PubMedCrossRef
16.
Zurück zum Zitat Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP (2001) Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone 28:195–201PubMedCrossRef Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP (2001) Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone 28:195–201PubMedCrossRef
17.
Zurück zum Zitat Gross J (1958) Studies on the formation of collagen. I. Properties and fractionation of neutral salt extracts of normal guinea pig connective tissue. J Exp Med 107:247–263PubMedCrossRef Gross J (1958) Studies on the formation of collagen. I. Properties and fractionation of neutral salt extracts of normal guinea pig connective tissue. J Exp Med 107:247–263PubMedCrossRef
18.
Zurück zum Zitat Norman TL, Yeni YN, Brown CU, Wang Z (1998) Influence of microdamage on fracture toughness of the human femur and tibia. Bone 23:303–306PubMedCrossRef Norman TL, Yeni YN, Brown CU, Wang Z (1998) Influence of microdamage on fracture toughness of the human femur and tibia. Bone 23:303–306PubMedCrossRef
19.
Zurück zum Zitat Odetti P, Rossi S, Monacelli F, Poggi A, Cirnigliaro M, Federici M, Federici A (2005) Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci 1043:710–717PubMedCrossRef Odetti P, Rossi S, Monacelli F, Poggi A, Cirnigliaro M, Federici M, Federici A (2005) Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci 1043:710–717PubMedCrossRef
20.
Zurück zum Zitat Viguet-Carrin S, Roux JP, Arlot ME, Merabet Z, Leeming DJ, Byrjalsen I, Delmas PD, Bouxsein ML (2006) Contribution of the advanced glycation end product pentosidine and of maturation of type I collagen to compressive biomechanical properties of human lumbar vertebrae. Bone 39:1073–1079PubMedCrossRef Viguet-Carrin S, Roux JP, Arlot ME, Merabet Z, Leeming DJ, Byrjalsen I, Delmas PD, Bouxsein ML (2006) Contribution of the advanced glycation end product pentosidine and of maturation of type I collagen to compressive biomechanical properties of human lumbar vertebrae. Bone 39:1073–1079PubMedCrossRef
21.
Zurück zum Zitat Tang SY, Allen MR, Phipps R, Burr DB, Vashishth D (2009) Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos Int 20:887–894PubMedCrossRef Tang SY, Allen MR, Phipps R, Burr DB, Vashishth D (2009) Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos Int 20:887–894PubMedCrossRef
22.
Zurück zum Zitat Ding M, Hvid I (2000) Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone 26:291–295PubMedCrossRef Ding M, Hvid I (2000) Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone 26:291–295PubMedCrossRef
23.
Zurück zum Zitat Müller R, Gerber SC, Hayes WC (1998) Micro-compression: a novel technique for the nondestructive assessment of local bone failure. Technol Health Care 6:433–444PubMed Müller R, Gerber SC, Hayes WC (1998) Micro-compression: a novel technique for the nondestructive assessment of local bone failure. Technol Health Care 6:433–444PubMed
24.
Zurück zum Zitat Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P (1999) Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14:1167–1174PubMedCrossRef Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P (1999) Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14:1167–1174PubMedCrossRef
25.
Zurück zum Zitat Karim L, Vashishth D (2012) Heterogeneous glycation of cancellous bone and its association with bone quality and fragility. PLoS One 7:e35047PubMedCrossRef Karim L, Vashishth D (2012) Heterogeneous glycation of cancellous bone and its association with bone quality and fragility. PLoS One 7:e35047PubMedCrossRef
26.
Zurück zum Zitat Valcourt U, Merle B, Gineyts E, Viguet-Carrin S, Delmas PD, Garnero P (2007) Non-enzymatic glycation of bone collagen modifies osteoclastic activity and differentiation. J Biol Chem 282:5691–5703PubMedCrossRef Valcourt U, Merle B, Gineyts E, Viguet-Carrin S, Delmas PD, Garnero P (2007) Non-enzymatic glycation of bone collagen modifies osteoclastic activity and differentiation. J Biol Chem 282:5691–5703PubMedCrossRef
27.
Zurück zum Zitat Hildebrand T, Rüegsegger P (1997) Quantification of bone microarchitecture with the structure model index. Comput Methods Biomech Biomed Eng 1:15–23CrossRef Hildebrand T, Rüegsegger P (1997) Quantification of bone microarchitecture with the structure model index. Comput Methods Biomech Biomed Eng 1:15–23CrossRef
28.
Zurück zum Zitat Mundy GR (2000) Pathogenesis of osteoporosis and challenges for drug delivery. Adv Drug Deliv Rev 42:165–173PubMedCrossRef Mundy GR (2000) Pathogenesis of osteoporosis and challenges for drug delivery. Adv Drug Deliv Rev 42:165–173PubMedCrossRef
Metadaten
Titel
Differences in non-enzymatic glycation and collagen cross-links between human cortical and cancellous bone
verfasst von
L. Karim
S. Y. Tang
G. E. Sroga
D. Vashishth
Publikationsdatum
01.09.2013
Verlag
Springer London
Erschienen in
Osteoporosis International / Ausgabe 9/2013
Print ISSN: 0937-941X
Elektronische ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-013-2319-4

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