Skip to main content
Erschienen in: Osteoporosis International 3/2006

01.03.2006 | Review

The role of collagen in bone strength

verfasst von: S. Viguet-Carrin, P. Garnero, P. D. Delmas

Erschienen in: Osteoporosis International | Ausgabe 3/2006

Einloggen, um Zugang zu erhalten

Abstract

Bone is a complex tissue of which the principal function is to resist mechanical forces and fractures. Bone strength depends not only on the quantity of bone tissue but also on the quality, which is characterized by the geometry and the shape of bones, the microarchitecture of the trabecular bones, the turnover, the mineral, and the collagen. Different determinants of bone quality are interrelated, especially the mineral and collagen, and analysis of their specific roles in bone strength is difficult. This review describes the interactions of type I collagen with the mineral and the contribution of the orientations of the collagen fibers when the bone is submitted to mechanical forces. Different processes of maturation of collagen occur in bone, which can result either from enzymatic or nonenzymatic processes. The enzymatic process involves activation of lysyl oxidase, which leads to the formation of immature and mature crosslinks that stabilize the collagen fibrils. Two type of nonenzymatic process are described in type I collagen: the formation of advanced glycation end products due to the accumulation of reducible sugars in bone tissue, and the process of racemization and isomerization in the telopeptide of the collagen. These modifications of collagen are age-related and may impair the mechanical properties of bone. To illustrate the role of the crosslinking process of collagen in bone strength, clinical disorders associated with bone collagen abnormalities and bone fragility, such as osteogenesis imperfecta and osteoporosis, are described.
Literatur
1.
Zurück zum Zitat Van der Rest M, Garrone R (1991) Collagen family proteins. FASEB J 5:2814–2823PubMed Van der Rest M, Garrone R (1991) Collagen family proteins. FASEB J 5:2814–2823PubMed
2.
Zurück zum Zitat Brodsky B, Shah NK (1995) The triple helix motif in proteins. FASEB J 9:1537–1546PubMed Brodsky B, Shah NK (1995) The triple helix motif in proteins. FASEB J 9:1537–1546PubMed
3.
Zurück zum Zitat Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20:33–43CrossRefPubMed Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20:33–43CrossRefPubMed
4.
Zurück zum Zitat Dominguez LJ, Barbagallo M, Moro L (2005) Collagen overglycosylation: a biochemical feature that may contribute to bone quality. Biochem Biophys Res Commun 330:1–4PubMed Dominguez LJ, Barbagallo M, Moro L (2005) Collagen overglycosylation: a biochemical feature that may contribute to bone quality. Biochem Biophys Res Commun 330:1–4PubMed
5.
Zurück zum Zitat Kuznetsova N and Leikin S (1999) Does the triple helical domain of type I collagen encode molecular recognition and fiber assembly while telopeptides serve as catalytic domains? Effect of proteolytic cleavage on fibrillogenesis and on collagen-collagen interaction in fibers. J Biol Chem 274:36083–36088PubMed Kuznetsova N and Leikin S (1999) Does the triple helical domain of type I collagen encode molecular recognition and fiber assembly while telopeptides serve as catalytic domains? Effect of proteolytic cleavage on fibrillogenesis and on collagen-collagen interaction in fibers. J Biol Chem 274:36083–36088PubMed
6.
Zurück zum Zitat Lamande SR, Bateman JF (1999) Procollagen folding and assembly: the role of endoplasmic reticulum enzymes and molecular chaperones. Semin Cell Dev Biol 10:455–464PubMed Lamande SR, Bateman JF (1999) Procollagen folding and assembly: the role of endoplasmic reticulum enzymes and molecular chaperones. Semin Cell Dev Biol 10:455–464PubMed
7.
Zurück zum Zitat Hendershot LM, Bulleid NJ (2000) Protein-specific chaperones: the role of HSP47 begins to gel. Curr Biol 10:912–915CrossRef Hendershot LM, Bulleid NJ (2000) Protein-specific chaperones: the role of HSP47 begins to gel. Curr Biol 10:912–915CrossRef
8.
Zurück zum Zitat Koivu J 1987 Identification of disulphides bonds in carboxy-terminal propeptides of human type I procollagen. FEBS Lett 212:229–232 Koivu J 1987 Identification of disulphides bonds in carboxy-terminal propeptides of human type I procollagen. FEBS Lett 212:229–232
9.
Zurück zum Zitat Bulleid NJ, Dalley JA, Lees JF 1997 The C-propeptide domain of procollagen can be replaced with a transmembrane domain without affecting trimer formation or collagen triple helix folding during biosynthesis. EMBO J 16:6694–6701 Bulleid NJ, Dalley JA, Lees JF 1997 The C-propeptide domain of procollagen can be replaced with a transmembrane domain without affecting trimer formation or collagen triple helix folding during biosynthesis. EMBO J 16:6694–6701
10.
Zurück zum Zitat Bachinger HP (1987) The influence of peptidyl-prolyl cis-trans isomerase on the in vitro folding of type III collagen. J Biol Chem 262:17144–17148PubMed Bachinger HP (1987) The influence of peptidyl-prolyl cis-trans isomerase on the in vitro folding of type III collagen. J Biol Chem 262:17144–17148PubMed
11.
Zurück zum Zitat Galat A, Metcalfe SM (1995) Peptidylproline cis/trans isomerases. Prog Biophys Mol Biol 63:67–118PubMed Galat A, Metcalfe SM (1995) Peptidylproline cis/trans isomerases. Prog Biophys Mol Biol 63:67–118PubMed
12.
Zurück zum Zitat Kivirikko KI, Myllyharju J (1998) Prolyl 4-hydroxylases and their protein disulfide isomerase subunit. Matrix Biol 16:357–368PubMed Kivirikko KI, Myllyharju J (1998) Prolyl 4-hydroxylases and their protein disulfide isomerase subunit. Matrix Biol 16:357–368PubMed
13.
Zurück zum Zitat Myllyharju J (2003) Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol 22:15–24PubMed Myllyharju J (2003) Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol 22:15–24PubMed
14.
Zurück zum Zitat Nagata K (1998) Expression and function of heat shock protein 47: a collagen-specific molecular chaperone in the endoplasmic reticulum. Matrix Biol 16:379–386PubMed Nagata K (1998) Expression and function of heat shock protein 47: a collagen-specific molecular chaperone in the endoplasmic reticulum. Matrix Biol 16:379–386PubMed
15.
Zurück zum Zitat Nagata K (2003) HSP47 as a collagen-specific molecular chaperone: function and expression in normal mouse development. Semin Cell Dev Biol 14:275–14282PubMed Nagata K (2003) HSP47 as a collagen-specific molecular chaperone: function and expression in normal mouse development. Semin Cell Dev Biol 14:275–14282PubMed
16.
Zurück zum Zitat Engel J, Prockop DJ (1991) The zipper-like folding of collagen triple helices and the effects of mutations that disrupt the zipper. Annu Rev Biophys Biophys Chem 20:137–152PubMed Engel J, Prockop DJ (1991) The zipper-like folding of collagen triple helices and the effects of mutations that disrupt the zipper. Annu Rev Biophys Biophys Chem 20:137–152PubMed
17.
Zurück zum Zitat Niyibizi C, Eyre DR (1994) Structural characteristics of cross-linking sites in type V collagen of bone chain specificities and heterotypic links to type I collagen. Eur J Biochem 224:943–950CrossRefPubMed Niyibizi C, Eyre DR (1994) Structural characteristics of cross-linking sites in type V collagen of bone chain specificities and heterotypic links to type I collagen. Eur J Biochem 224:943–950CrossRefPubMed
18.
Zurück zum Zitat Niyibizi C, Eyre DR (1989) Bone type V collagen: chain composition and location of a trypsin cleavage site. Connect Tissue Res 20:247–250PubMed Niyibizi C, Eyre DR (1989) Bone type V collagen: chain composition and location of a trypsin cleavage site. Connect Tissue Res 20:247–250PubMed
19.
Zurück zum Zitat Baum J and Brodsky B (1999) Folding of peptide models of collagen and misfolding in disease. Curr Opin Struct Biol 9:122–128CrossRefPubMed Baum J and Brodsky B (1999) Folding of peptide models of collagen and misfolding in disease. Curr Opin Struct Biol 9:122–128CrossRefPubMed
20.
Zurück zum Zitat Koivu J, Myllyla R, Helaakoski T, Pihlajaniemi T, Tasanen K, Kivirikko KI (1987) A single polypeptide acts both as the beta subunit of prolyl 4-hydroxylase and as a protein disulfide-isomerase. J Biol Chem 262:6447–9PubMed Koivu J, Myllyla R, Helaakoski T, Pihlajaniemi T, Tasanen K, Kivirikko KI (1987) A single polypeptide acts both as the beta subunit of prolyl 4-hydroxylase and as a protein disulfide-isomerase. J Biol Chem 262:6447–9PubMed
21.
Zurück zum Zitat John DC, Grant ME, Bulleid NJ (1993) Cell-free synthesis and assembly of prolyl 4-hydroxylase: the role of the beta-subunit (PDI) in preventing misfolding and aggregation of the alpha-subunit. EMBO J 12:1587–1595PubMed John DC, Grant ME, Bulleid NJ (1993) Cell-free synthesis and assembly of prolyl 4-hydroxylase: the role of the beta-subunit (PDI) in preventing misfolding and aggregation of the alpha-subunit. EMBO J 12:1587–1595PubMed
22.
Zurück zum Zitat Privalov PL (1982) Stability of proteins. Proteins which do not present a single cooperative system. Adv Protein Chem 35:1–104PubMed Privalov PL (1982) Stability of proteins. Proteins which do not present a single cooperative system. Adv Protein Chem 35:1–104PubMed
23.
Zurück zum Zitat Bella J, Brodsky B, Berman HM (1995) Hydration structure of a collagen peptide. Structure 3:893–906CrossRefPubMed Bella J, Brodsky B, Berman HM (1995) Hydration structure of a collagen peptide. Structure 3:893–906CrossRefPubMed
24.
Zurück zum Zitat Vranka JA, Sakai LY, Bachinger HP (2004) Prolyl 3-hydroxylase 1, enzyme characterization and identification of a novel family of enzymes. J Biol Chem. 279:23615–21 Vranka JA, Sakai LY, Bachinger HP (2004) Prolyl 3-hydroxylase 1, enzyme characterization and identification of a novel family of enzymes. J Biol Chem. 279:23615–21
25.
Zurück zum Zitat Valtavaara M, Szpirer C, Szpirer J, Myllyla R (1998) Primary structure, tissue distribution, and chromosomal localization of a novel isoform of lysyl hydroxylase (lysyl hydroxylase 3). J Biol Chem 273:12881–12886CrossRefPubMed Valtavaara M, Szpirer C, Szpirer J, Myllyla R (1998) Primary structure, tissue distribution, and chromosomal localization of a novel isoform of lysyl hydroxylase (lysyl hydroxylase 3). J Biol Chem 273:12881–12886CrossRefPubMed
26.
Zurück zum Zitat Wang C, Luosujarvi H, Heikkinen J, Risteli M, Uitto L, Myllyla R (2002) The third activity for lysyl hydroxylase 3: galactosylation of hydroxylysyl residues in collagens in vitro. Matrix Biol 21:559–566CrossRefPubMed Wang C, Luosujarvi H, Heikkinen J, Risteli M, Uitto L, Myllyla R (2002) The third activity for lysyl hydroxylase 3: galactosylation of hydroxylysyl residues in collagens in vitro. Matrix Biol 21:559–566CrossRefPubMed
27.
Zurück zum Zitat Passoja K, Rautavuoma K, Ala-Kokko L, Kosonen T, Kivirikko KI (1998) Cloning and characterization of a third lysyl hydroxylase isoform. Proc Natl Acad Sci USA 95:10482–10486PubMed Passoja K, Rautavuoma K, Ala-Kokko L, Kosonen T, Kivirikko KI (1998) Cloning and characterization of a third lysyl hydroxylase isoform. Proc Natl Acad Sci USA 95:10482–10486PubMed
28.
Zurück zum Zitat Mercer DK, Nicol PF, Kimbembe C, Robins SP (2003) Identification, expression and tissue distribution of three rat lysyl hydroxylase isoforms. Biochem Biophys Res Commun 307:803–809CrossRefPubMed Mercer DK, Nicol PF, Kimbembe C, Robins SP (2003) Identification, expression and tissue distribution of three rat lysyl hydroxylase isoforms. Biochem Biophys Res Commun 307:803–809CrossRefPubMed
29.
Zurück zum Zitat Bank RA, Robins SP, Wijmenga C, Breslau-Siderius LJ, Bardoel AF, van der Sluijs HA, Pruijs HE, TeKoppele JM (1999) Defective collagen cross-linking in bone, but not in ligament or cartilage, in Bruck syndrome: indication for a bone specific telopeptide lysyl hydroxylase on chromosome 17. Proc Natl Acad Sci USA 96:1054–1058PubMed Bank RA, Robins SP, Wijmenga C, Breslau-Siderius LJ, Bardoel AF, van der Sluijs HA, Pruijs HE, TeKoppele JM (1999) Defective collagen cross-linking in bone, but not in ligament or cartilage, in Bruck syndrome: indication for a bone specific telopeptide lysyl hydroxylase on chromosome 17. Proc Natl Acad Sci USA 96:1054–1058PubMed
30.
Zurück zum Zitat Ha-Vinh R, Alanay Y, Bank RA, Campos-Xavier AB, Zankl A, Superti-Furga A, Bonafe L (2004) Phenotypic and molecular characterization of Bruck syndrome (osteogenesis imperfecta with contractures of the large joints) caused by a recessive mutation in PLOD2. Am J Med Genet A 131A:115–120CrossRef Ha-Vinh R, Alanay Y, Bank RA, Campos-Xavier AB, Zankl A, Superti-Furga A, Bonafe L (2004) Phenotypic and molecular characterization of Bruck syndrome (osteogenesis imperfecta with contractures of the large joints) caused by a recessive mutation in PLOD2. Am J Med Genet A 131A:115–120CrossRef
31.
Zurück zum Zitat Bailey AJ, Wotton SF, Sims TJ, Thompson PW (1992) Post translational modifications in the collagen of human osteoporotic femoral head. Biochem Biophys Res Commun 185:801–805CrossRefPubMed Bailey AJ, Wotton SF, Sims TJ, Thompson PW (1992) Post translational modifications in the collagen of human osteoporotic femoral head. Biochem Biophys Res Commun 185:801–805CrossRefPubMed
32.
Zurück zum Zitat Harwood R, Grant ME, Jackson DS (1974) Collagen biosynthesis. Characterization of subcellular fractions from embyonic chick fibroblasts and the intracellular localization of protocollagen prolyl and protocollagen lysyl hydroxylases. Biochem J 144:123–130PubMed Harwood R, Grant ME, Jackson DS (1974) Collagen biosynthesis. Characterization of subcellular fractions from embyonic chick fibroblasts and the intracellular localization of protocollagen prolyl and protocollagen lysyl hydroxylases. Biochem J 144:123–130PubMed
33.
Zurück zum Zitat Harwood R, Grant ME, Jackson DS (1975) Studies on the glycosylation of hydroxylysine residues during collagen biosynthesis and the subcellular localization of collagen galactosyltransferase and collagen glucosyltransferase in tendon and cartilage cells. Biochem J 152:291–302PubMed Harwood R, Grant ME, Jackson DS (1975) Studies on the glycosylation of hydroxylysine residues during collagen biosynthesis and the subcellular localization of collagen galactosyltransferase and collagen glucosyltransferase in tendon and cartilage cells. Biochem J 152:291–302PubMed
34.
Zurück zum Zitat Gineyts E, Garnero P, Delmas PD (2001) Urinary excretion of glucosyl-galactosyl pyridinoline: a specific biochemical marker of synovium degradation. Rheumatology (Oxford) 40:315–323 Gineyts E, Garnero P, Delmas PD (2001) Urinary excretion of glucosyl-galactosyl pyridinoline: a specific biochemical marker of synovium degradation. Rheumatology (Oxford) 40:315–323
35.
Zurück zum Zitat Segrest JP, CunninghamLW (1970) Variations in human urinary O-hydroxylysyl glycoside levels and their relationship to collagen metabolism. J Clin Invest 49:1497–1509PubMedCrossRef Segrest JP, CunninghamLW (1970) Variations in human urinary O-hydroxylysyl glycoside levels and their relationship to collagen metabolism. J Clin Invest 49:1497–1509PubMedCrossRef
36.
Zurück zum Zitat Pinnell SR, Fox R, Krane SM (1971) Human collagens: differences in glycosylated hydroxylysines in skin and bone. Biochim Biophys Acta 229:119–122PubMed Pinnell SR, Fox R, Krane SM (1971) Human collagens: differences in glycosylated hydroxylysines in skin and bone. Biochim Biophys Acta 229:119–122PubMed
37.
Zurück zum Zitat Smith-Mungo L, Kagan HM (1998) Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol 16:387–398CrossRefPubMed Smith-Mungo L, Kagan HM (1998) Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol 16:387–398CrossRefPubMed
38.
Zurück zum Zitat Maki JM, Tikkanen H, Kivirikko KI (2001) Cloning and characterization of the fifth human lysyl oxidase enzyme: the third member of the lysyl oxidase related subfamily with four scavenger repector cystein-rich domains. Matrix Biol 20:493–496CrossRefPubMed Maki JM, Tikkanen H, Kivirikko KI (2001) Cloning and characterization of the fifth human lysyl oxidase enzyme: the third member of the lysyl oxidase related subfamily with four scavenger repector cystein-rich domains. Matrix Biol 20:493–496CrossRefPubMed
39.
Zurück zum Zitat Csiszar K (2001) Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol 70:1–32PubMed Csiszar K (2001) Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol 70:1–32PubMed
40.
Zurück zum Zitat Atsawasuwan P, Mochida Y, Parisuthiman D, Yamauchi M (2005) Expression of lysyl oxidase isoforms in MC3T3-E1 osteoblastic cells. Biochem Biophys Res Commun 327:1042–1046CrossRefPubMed Atsawasuwan P, Mochida Y, Parisuthiman D, Yamauchi M (2005) Expression of lysyl oxidase isoforms in MC3T3-E1 osteoblastic cells. Biochem Biophys Res Commun 327:1042–1046CrossRefPubMed
41.
Zurück zum Zitat Wang SX, Mure M, Medzihradszky KF, Burlingame AL, Brown DE, Dooley DM, Smith AJ, Kagan HM, Klinman JP (1996) A crosslinked cofactor in lysyl oxidase: redox function for amino acid side chains Science 273:1078–1084 Wang SX, Mure M, Medzihradszky KF, Burlingame AL, Brown DE, Dooley DM, Smith AJ, Kagan HM, Klinman JP (1996) A crosslinked cofactor in lysyl oxidase: redox function for amino acid side chains Science 273:1078–1084
42.
Zurück zum Zitat Robins SP, Shimokomaki M, Bailey AJ (1973) The chemistry of the collagen crosslinks. Age-related changes in the reducible components of intact bovine collagen fibres. Biochem J 131:771–780PubMed Robins SP, Shimokomaki M, Bailey AJ (1973) The chemistry of the collagen crosslinks. Age-related changes in the reducible components of intact bovine collagen fibres. Biochem J 131:771–780PubMed
43.
Zurück zum Zitat Eyre DR, Paz MA, Gallop PM (1984) Cross-linking in collagen and elastin. Annu. Rev Biochem 53:717–748CrossRef Eyre DR, Paz MA, Gallop PM (1984) Cross-linking in collagen and elastin. Annu. Rev Biochem 53:717–748CrossRef
44.
Zurück zum Zitat Eyre DR, Dickson IR, Van Ness K (1988) Collagen cross-linking in human bone and articular cartilage. Age-related changes in the content of mature hydroxypyridinium residues. Biochem J 252:495–500PubMed Eyre DR, Dickson IR, Van Ness K (1988) Collagen cross-linking in human bone and articular cartilage. Age-related changes in the content of mature hydroxypyridinium residues. Biochem J 252:495–500PubMed
45.
Zurück zum Zitat Eyre DR, Oguchi H (1980) The hydroxypyridinium crosslinks of skeletal collagen: their measurement, properties and a proposed pathway of formation. Biochem Biophys Res Commun 92:403–410CrossRefPubMed Eyre DR, Oguchi H (1980) The hydroxypyridinium crosslinks of skeletal collagen: their measurement, properties and a proposed pathway of formation. Biochem Biophys Res Commun 92:403–410CrossRefPubMed
46.
Zurück zum Zitat Robins SP, Ducan A (1983) Cross-linking of the collagen. Location of pyridinoline in bovine articular cartilage at two sites of the molecules. Biochem J 215:167–173PubMed Robins SP, Ducan A (1983) Cross-linking of the collagen. Location of pyridinoline in bovine articular cartilage at two sites of the molecules. Biochem J 215:167–173PubMed
47.
Zurück zum Zitat Fujimori E (1985) Ultraviolet light- and ozone-induced changes in pyridinoline, a trisubstituted 3-hydroxypyridinium crosslink of collagen. Biochim Biophys Acta 828:104–106PubMed Fujimori E (1985) Ultraviolet light- and ozone-induced changes in pyridinoline, a trisubstituted 3-hydroxypyridinium crosslink of collagen. Biochim Biophys Acta 828:104–106PubMed
48.
Zurück zum Zitat Colwell A, Hamer A, Blumsohn A, Eastell R (1996) To determine the effects of ultraviolet light, natural light and ionizing radiation on pyridinium cross-links in bone and urine using high-performance liquid chromatography. Eur J Clin Invest 26:1107–1114CrossRefPubMed Colwell A, Hamer A, Blumsohn A, Eastell R (1996) To determine the effects of ultraviolet light, natural light and ionizing radiation on pyridinium cross-links in bone and urine using high-performance liquid chromatography. Eur J Clin Invest 26:1107–1114CrossRefPubMed
49.
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 253:26–32CrossRefPubMed 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 253:26–32CrossRefPubMed
50.
Zurück zum Zitat Moro L, Romanello M, Favia A, Lamanna MP, Lozupone E (2000) Posttranslational modifications of bone collagen type I are related to the function of rat femoral regions. Calcif Tissue Int 66:151–156CrossRefPubMed Moro L, Romanello M, Favia A, Lamanna MP, Lozupone E (2000) Posttranslational modifications of bone collagen type I are related to the function of rat femoral regions. Calcif Tissue Int 66:151–156CrossRefPubMed
51.
Zurück zum Zitat Bailey AJ, Peach CM (1968) Isolation and structural identification of a labile intermolecular crosslink in collagen Biochem Biophys Res Commun 33:812–819 Bailey AJ, Peach CM (1968) Isolation and structural identification of a labile intermolecular crosslink in collagen Biochem Biophys Res Commun 33:812–819
52.
Zurück zum Zitat Barnes MJ, Constable BJ, Morton LF, Kodicek E (1971) Hydroxylysine in the N-terminal regions of the 1- and 2-chains of various collagens. Biochem J 125:433–437PubMed Barnes MJ, Constable BJ, Morton LF, Kodicek E (1971) Hydroxylysine in the N-terminal regions of the 1- and 2-chains of various collagens. Biochem J 125:433–437PubMed
53.
Zurück zum Zitat Knott L, Whitehead CC, Fleming RH, Bailey AJ (1995) Biochemical changes in the collagenous matrix of osteoporotic avian bone. Biochem J 310:1045–1051PubMed Knott L, Whitehead CC, Fleming RH, Bailey AJ (1995) Biochemical changes in the collagenous matrix of osteoporotic avian bone. Biochem J 310:1045–1051PubMed
54.
Zurück zum Zitat Kuypers R, Tyler M, Kurth LB, Jenkins ID, Horgan DJ (1992) Identification of the loci of the collagen-associated Ehrlich chromogen in type I collagen confirms its role as a trivalent cross-link. Biochem J 283:129–136PubMed Kuypers R, Tyler M, Kurth LB, Jenkins ID, Horgan DJ (1992) Identification of the loci of the collagen-associated Ehrlich chromogen in type I collagen confirms its role as a trivalent cross-link. Biochem J 283:129–136PubMed
55.
Zurück zum Zitat Ristelli J, Eriksen H, Risteli L, Mansell JP, Bayley AJ (1994) Pyrrolic crosslinks are as abundant in human bone type I collagen as pyridinolines. J Bone Miner Res 9(Suppl 1):S186 Ristelli J, Eriksen H, Risteli L, Mansell JP, Bayley AJ (1994) Pyrrolic crosslinks are as abundant in human bone type I collagen as pyridinolines. J Bone Miner Res 9(Suppl 1):S186
56.
Zurück zum Zitat Bailey AJ, Knott L (1999) Molecular changes in bone collagen in osteoporosis and osteoarthritis in the elderly. Exp Gerontol 1999 34:337–351 Bailey AJ, Knott L (1999) Molecular changes in bone collagen in osteoporosis and osteoarthritis in the elderly. Exp Gerontol 1999 34:337–351
57.
Zurück zum Zitat Eyre DR (1987) Collagen cross-linking amino acids. Methods Enzymol 144:115–139PubMed Eyre DR (1987) Collagen cross-linking amino acids. Methods Enzymol 144:115–139PubMed
58.
Zurück zum Zitat Hanson DA, Eyre DR (1996) Molecular site specificity of pyridinoline and pyrrole crosslinks in type I collagen of human bone. J Biol Chem 271:26508–26516CrossRefPubMed Hanson DA, Eyre DR (1996) Molecular site specificity of pyridinoline and pyrrole crosslinks in type I collagen of human bone. J Biol Chem 271:26508–26516CrossRefPubMed
59.
Zurück zum Zitat Knott L, Bailey AJ (1998) Collagen cross-links in mineralising tissues : a review of their chemistry, function, and clinical relevance. Bone 22:181–187CrossRefPubMed Knott L, Bailey AJ (1998) Collagen cross-links in mineralising tissues : a review of their chemistry, function, and clinical relevance. Bone 22:181–187CrossRefPubMed
60.
Zurück zum Zitat Bailey AJ, Paul RG, Knott L (1998) Mechanisms of maturation and ageing of collagen. Mech Ageing Dev 106:1–56CrossRefPubMed Bailey AJ, Paul RG, Knott L (1998) Mechanisms of maturation and ageing of collagen. Mech Ageing Dev 106:1–56CrossRefPubMed
61.
Zurück zum Zitat Eyre DR, Glimcher MJ (1973) Analysis of a crosslinked peptide from calf bone collagen: evidence that hydroxylysyl glycoside participates in the crosslink. Biochem Biophys Res Commun 52:663–671CrossRefPubMed Eyre DR, Glimcher MJ (1973) Analysis of a crosslinked peptide from calf bone collagen: evidence that hydroxylysyl glycoside participates in the crosslink. Biochem Biophys Res Commun 52:663–671CrossRefPubMed
62.
Zurück zum Zitat Robins SP, Bailey AJ (1974) Isolation and characterization of glycosyl derivatives of the reducible cross-links in collagens. FEBS Lett 38:334–336CrossRefPubMed Robins SP, Bailey AJ (1974) Isolation and characterization of glycosyl derivatives of the reducible cross-links in collagens. FEBS Lett 38:334–336CrossRefPubMed
63.
Zurück zum Zitat Lapolla A, Traldi P, Fedele D (2005) Importance of measuring products of non-enzymatic glycation of proteins. Clin Biochem. 2005 38:103–115 Lapolla A, Traldi P, Fedele D (2005) Importance of measuring products of non-enzymatic glycation of proteins. Clin Biochem. 2005 38:103–115
64.
Zurück zum Zitat Wolff SP,Dean RT (1987) Glucose autoxidation and protein modification. The potential role of “autoxidative glycosylation” in diabetes. Biochem J 245:243–50PubMed Wolff SP,Dean RT (1987) Glucose autoxidation and protein modification. The potential role of “autoxidative glycosylation” in diabetes. Biochem J 245:243–50PubMed
65.
Zurück zum Zitat Sell DR, Monnier VM (1989) Structure elucidation of a senescence crosslink from human extracellular matrix: implication of pentoses in the aging process. J Biol Chem 264:21597–21602PubMed Sell DR, Monnier VM (1989) Structure elucidation of a senescence crosslink from human extracellular matrix: implication of pentoses in the aging process. J Biol Chem 264:21597–21602PubMed
66.
Zurück zum Zitat Monnier VM, Cerami A (1983) Detection of nonenzymatic browning products in the human lens. Biochim Biophys Acta 760:97–103PubMed Monnier VM, Cerami A (1983) Detection of nonenzymatic browning products in the human lens. Biochim Biophys Acta 760:97–103PubMed
67.
Zurück zum Zitat Markesbery WR (1997) Oxidative stress hypothesis in Alzheimer’s disease. Free Ra Biol Med 23:134–147CrossRef Markesbery WR (1997) Oxidative stress hypothesis in Alzheimer’s disease. Free Ra Biol Med 23:134–147CrossRef
68.
Zurück zum Zitat Brownlee M, Cerami A, Vlassara H (1988) Advanced glycosysalation end products in tissue and the biochemical basis of diabetic complications. N Engl J Med 318:1315–1321PubMedCrossRef Brownlee M, Cerami A, Vlassara H (1988) Advanced glycosysalation end products in tissue and the biochemical basis of diabetic complications. N Engl J Med 318:1315–1321PubMedCrossRef
69.
Zurück zum Zitat DeGroot J, Verzijl N, Wenting-Van Wijk MJ, Bank RA, Lafeber FP, Bijlsma JW, TeKoppele JM (2001) Age-related decrease in susceptibility of human articular cartilage to matrix metalloproteinase-mediated degradation: the role of advanced glycation end products. Arthritis Rheum 44:2562–2571CrossRefPubMed DeGroot J, Verzijl N, Wenting-Van Wijk MJ, Bank RA, Lafeber FP, Bijlsma JW, TeKoppele JM (2001) Age-related decrease in susceptibility of human articular cartilage to matrix metalloproteinase-mediated degradation: the role of advanced glycation end products. Arthritis Rheum 44:2562–2571CrossRefPubMed
70.
Zurück zum Zitat Brownlee M (1994) Lilly Lecture 1993. Glycation and diabetic complications. Diabetes 43:836–841PubMed Brownlee M (1994) Lilly Lecture 1993. Glycation and diabetic complications. Diabetes 43:836–841PubMed
71.
Zurück zum Zitat Katayama Y, Akatsu T, Yamamoto M, Kugai N, Nagata N (1996) Role of nonenzymatic glycosylation of type I collagen in diabetic osteopenia. J Bone Miner Res 11:931–937PubMed Katayama Y, Akatsu T, Yamamoto M, Kugai N, Nagata N (1996) Role of nonenzymatic glycosylation of type I collagen in diabetic osteopenia. J Bone Miner Res 11:931–937PubMed
72.
Zurück zum Zitat Miyata T, Kawai R, Taketomi S, Sprague SM (1996) Possible involvement of advanced glycation end-products in bone resorption. Nephrol Dial Transplant 11:54S-57S Miyata T, Kawai R, Taketomi S, Sprague SM (1996) Possible involvement of advanced glycation end-products in bone resorption. Nephrol Dial Transplant 11:54S-57S
73.
Zurück zum Zitat Verzijl N, DeGroot J, Ben ZC, Brau-Benjamin O, Maroudas A, Bank RA, Mizrahi J, Schalkwijk CG, Thorpe SR, Baynes JW, Bijlsma JW, Lafeber FP, TeKoppele JM (2002) Crosslinking by advanced glycation end products increases the stiffness of the collagen network in human articular cartilage: a possible mechanism through which age is a risk factor for osteoarthritis. Arthritis Rheum 46:114–123CrossRefPubMed Verzijl N, DeGroot J, Ben ZC, Brau-Benjamin O, Maroudas A, Bank RA, Mizrahi J, Schalkwijk CG, Thorpe SR, Baynes JW, Bijlsma JW, Lafeber FP, TeKoppele JM (2002) Crosslinking by advanced glycation end products increases the stiffness of the collagen network in human articular cartilage: a possible mechanism through which age is a risk factor for osteoarthritis. Arthritis Rheum 46:114–123CrossRefPubMed
74.
Zurück zum Zitat Chen AC, Temple MM, Ng DM, Verzijl N, DeGroot J, TeKoppele JM, Sah RL (2002) Induction of advanced glycation end products and alterations of the tensile properties of articular cartilage. Arthritis Rheum 46:3212–3217CrossRefPubMed Chen AC, Temple MM, Ng DM, Verzijl N, DeGroot J, TeKoppele JM, Sah RL (2002) Induction of advanced glycation end products and alterations of the tensile properties of articular cartilage. Arthritis Rheum 46:3212–3217CrossRefPubMed
75.
Zurück zum Zitat Tomasek JJ, Meyers SW, Basinger JB, Green DT, Shew RL (1994) Diabetic and age-related enhancement of collagen-linked fluorescence in cortical bone of rats. Life Sci 55:855–861CrossRefPubMed Tomasek JJ, Meyers SW, Basinger JB, Green DT, Shew RL (1994) Diabetic and age-related enhancement of collagen-linked fluorescence in cortical bone of rats. Life Sci 55:855–861CrossRefPubMed
76.
Zurück zum Zitat Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone 31:1–7CrossRefPubMed Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone 31:1–7CrossRefPubMed
77.
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 28:195–201CrossRefPubMed Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP (2001) Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone 28:195–201CrossRefPubMed
78.
Zurück zum Zitat Clarke S (1987) Propensity for spontaneous succinimide formation from aspartyl and asparaginyl residues in cellular proteins. Int J Pept Protein Res 30:808–821PubMedCrossRef Clarke S (1987) Propensity for spontaneous succinimide formation from aspartyl and asparaginyl residues in cellular proteins. Int J Pept Protein Res 30:808–821PubMedCrossRef
79.
Zurück zum Zitat Maroudas A, Bayliss MT, Uchitel-Kaushansky N, Schneiderman R, Gilav E (1998) Aggrecan turnover in human articular cartilage: use of aspartic acid racemization as a marker of molecular age. Arch Biochem Biophys 350:61–71CrossRefPubMed Maroudas A, Bayliss MT, Uchitel-Kaushansky N, Schneiderman R, Gilav E (1998) Aggrecan turnover in human articular cartilage: use of aspartic acid racemization as a marker of molecular age. Arch Biochem Biophys 350:61–71CrossRefPubMed
80.
Zurück zum Zitat Saido TC, Iwatsubo T, Mann DM, Shimada H, Ihara Y, Kawashima S. (1995) Dominant and differential deposition of distinct beta-amyloid peptide species, A beta N3(pE), in senile plaques. Neuron 14:457–466CrossRefPubMed Saido TC, Iwatsubo T, Mann DM, Shimada H, Ihara Y, Kawashima S. (1995) Dominant and differential deposition of distinct beta-amyloid peptide species, A beta N3(pE), in senile plaques. Neuron 14:457–466CrossRefPubMed
81.
Zurück zum Zitat Fledelius C, Johnsen AH, Cloos PA, Bonde M, Qvist P (1997) Characterisation of urinary degradation products derived from type I collagen. Identification of a beta-isomerized Asp-Gly sequence within the C-terminal telopeptide (alpha1) region. J Biol Chem 272:9755–9763CrossRefPubMed Fledelius C, Johnsen AH, Cloos PA, Bonde M, Qvist P (1997) Characterisation of urinary degradation products derived from type I collagen. Identification of a beta-isomerized Asp-Gly sequence within the C-terminal telopeptide (alpha1) region. J Biol Chem 272:9755–9763CrossRefPubMed
82.
Zurück zum Zitat Roher AE, Lowenson JD, Clarke S, Wolkow C, Wang R, Cotter RJ, Reardon IM, Zurcher-Neely HA, Heinrikson RL, Ball MJ (1993) Structural alterations in the peptide backbone of beta-amyloid core protein may account for its deposition and stability in Alzheimer’s disease. J Biol Chem 268:3072–3083PubMed Roher AE, Lowenson JD, Clarke S, Wolkow C, Wang R, Cotter RJ, Reardon IM, Zurcher-Neely HA, Heinrikson RL, Ball MJ (1993) Structural alterations in the peptide backbone of beta-amyloid core protein may account for its deposition and stability in Alzheimer’s disease. J Biol Chem 268:3072–3083PubMed
83.
Zurück zum Zitat Geiger T and Clarke S (1987) Deamination, isomerization, and racemization at asparaginyl and aspartyl residues in peptides. Succinimide-linked reactions that contribute to protein degradation. J Biol Chem 262:785–794PubMed Geiger T and Clarke S (1987) Deamination, isomerization, and racemization at asparaginyl and aspartyl residues in peptides. Succinimide-linked reactions that contribute to protein degradation. J Biol Chem 262:785–794PubMed
84.
Zurück zum Zitat Gineyts E, Cloos PA, Borel O, Grimaud L, Delmas PD, Garnero P (2000) Racemization and isomerisation of type I collagen C-telopeptides in human bone and soft tissues : assessment of tissue turnover. Biochem J 345:481–485CrossRefPubMed Gineyts E, Cloos PA, Borel O, Grimaud L, Delmas PD, Garnero P (2000) Racemization and isomerisation of type I collagen C-telopeptides in human bone and soft tissues : assessment of tissue turnover. Biochem J 345:481–485CrossRefPubMed
85.
Zurück zum Zitat Tomiyama T, Asano S, Furiya Y, Shirasawa T, Endo N, Mori H (1994) Racemization of Asp23 residue affects the aggregation of Alzheimer amyloid beta protein analogues. J Biol Chem 269:10205–10208PubMed Tomiyama T, Asano S, Furiya Y, Shirasawa T, Endo N, Mori H (1994) Racemization of Asp23 residue affects the aggregation of Alzheimer amyloid beta protein analogues. J Biol Chem 269:10205–10208PubMed
86.
Zurück zum Zitat Cloos PA, Fledelius C (2000) Collagen fragments in urine derived from bone resorption are highly racemized and isomerised: a biological clock of protein aging with clinical potential. Biochem J 345:473–480CrossRefPubMed Cloos PA, Fledelius C (2000) Collagen fragments in urine derived from bone resorption are highly racemized and isomerised: a biological clock of protein aging with clinical potential. Biochem J 345:473–480CrossRefPubMed
87.
Zurück zum Zitat Shimizu T, Fukuda H, Murayama S, Izumiyama N, Shirasawa T. (2002) Isoaspartate formation at position 23 of amyloid beta peptide enhanced fibril formation and deposited onto senile plaques and vascular amyloids in Alzheimer’s disease. J Neurosci Res 70:451–461CrossRefPubMed Shimizu T, Fukuda H, Murayama S, Izumiyama N, Shirasawa T. (2002) Isoaspartate formation at position 23 of amyloid beta peptide enhanced fibril formation and deposited onto senile plaques and vascular amyloids in Alzheimer’s disease. J Neurosci Res 70:451–461CrossRefPubMed
88.
Zurück zum Zitat Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:595–608CrossRefPubMed Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:595–608CrossRefPubMed
89.
Zurück zum Zitat Ottani V, Raspanti M, Ruggeri A (2001) Collagen structure and functional implications. Micron 32:251–260CrossRefPubMed Ottani V, Raspanti M, Ruggeri A (2001) Collagen structure and functional implications. Micron 32:251–260CrossRefPubMed
90.
Zurück zum Zitat Fratzl P, Paris O, Klaushofer K, Landis WJ (1996) Bone mineralization in an osteogenesis imperfecta mouse model studied by small-angle x-ray scattering. J Clin Invest 97:396–402PubMedCrossRef Fratzl P, Paris O, Klaushofer K, Landis WJ (1996) Bone mineralization in an osteogenesis imperfecta mouse model studied by small-angle x-ray scattering. J Clin Invest 97:396–402PubMedCrossRef
91.
Zurück zum Zitat Vetter U, Eanes ED, Kopp JB, Termine JD, Robey PG (1991) Changes in apatite crystal size in bones of patients with osteogenesis imperfecta. Calcif Tissue Int 49:248–250PubMed Vetter U, Eanes ED, Kopp JB, Termine JD, Robey PG (1991) Changes in apatite crystal size in bones of patients with osteogenesis imperfecta. Calcif Tissue Int 49:248–250PubMed
92.
Zurück zum Zitat Traub W, Arad T, Vetter U, Weiner S (1994) Ultrastructural studies of bones from patients with osteogenesis imperfecta. Matrix Biol 14:337–345CrossRefPubMed Traub W, Arad T, Vetter U, Weiner S (1994) Ultrastructural studies of bones from patients with osteogenesis imperfecta. Matrix Biol 14:337–345CrossRefPubMed
93.
Zurück zum Zitat Marotti G, Muglia MA, Palumbo C (1994) Structure and function of lamellar bone. Clin Rheumatol 13 Suppl 1:63–68 Marotti G, Muglia MA, Palumbo C (1994) Structure and function of lamellar bone. Clin Rheumatol 13 Suppl 1:63–68
94.
95.
Zurück zum Zitat Currey JD (1988) The effect of porosity and mineral content on the Young’s modulus of elasticity of compact bone. J Biochem 21:131–139 Currey JD (1988) The effect of porosity and mineral content on the Young’s modulus of elasticity of compact bone. J Biochem 21:131–139
96.
Zurück zum Zitat Currey JD, Brear K, Zioupos P (1996) The effects of aging and changes in mineral content in degrading the toughness of human femora. J Biomech 29:257–260CrossRefPubMed Currey JD, Brear K, Zioupos P (1996) The effects of aging and changes in mineral content in degrading the toughness of human femora. J Biomech 29:257–260CrossRefPubMed
97.
Zurück zum Zitat Boskey AL, Wright TM, Blank RD (1999) Collagen and bone strength. J Bone Miner Res 14:330–335PubMed Boskey AL, Wright TM, Blank RD (1999) Collagen and bone strength. J Bone Miner Res 14:330–335PubMed
98.
Zurück zum Zitat Wang X, Bank RA, TeKoppele JM, Agrawal CM (2001) The role of collagen in determining bone mechanical properties. J Orthop Res 19:1021–1026CrossRefPubMed Wang X, Bank RA, TeKoppele JM, Agrawal CM (2001) The role of collagen in determining bone mechanical properties. J Orthop Res 19:1021–1026CrossRefPubMed
99.
Zurück zum Zitat Zioupos P, Currey JD, Hamer AJ (1999) The role of collagen in the declining mechanical properties of aging human cortical bone. J Biomed Mater Res 45:108–116CrossRefPubMed Zioupos P, Currey JD, Hamer AJ (1999) The role of collagen in the declining mechanical properties of aging human cortical bone. J Biomed Mater Res 45:108–116CrossRefPubMed
100.
Zurück zum Zitat Thompson JB, Kindt JH, Drake B, Hansma HG, Morse DE, Hansma PK (2001) Bone indentation recovery time correlates with bond reforming time. Nature 414:773–776CrossRefPubMed Thompson JB, Kindt JH, Drake B, Hansma HG, Morse DE, Hansma PK (2001) Bone indentation recovery time correlates with bond reforming time. Nature 414:773–776CrossRefPubMed
101.
Zurück zum Zitat Zioupos P (2001) human bone: factors affecting its biomechanical properties and the role of collagen. J Biomater Appl 15:187–229CrossRefPubMed Zioupos P (2001) human bone: factors affecting its biomechanical properties and the role of collagen. J Biomater Appl 15:187–229CrossRefPubMed
102.
Zurück zum Zitat Currey JD, Foreman J, Laketic I, Mitchell J, Pegg DE, Reilly GC (1997) Effects of ionizing radiation on the mechanical properties of human bone. J Orthop Res 15:111–117CrossRefPubMed Currey JD, Foreman J, Laketic I, Mitchell J, Pegg DE, Reilly GC (1997) Effects of ionizing radiation on the mechanical properties of human bone. J Orthop Res 15:111–117CrossRefPubMed
103.
Zurück zum Zitat Currey JD (2003) Role of collagen and other organics in the mechanical properties of bone. Osteoporos Int 14:S29-S36CrossRef Currey JD (2003) Role of collagen and other organics in the mechanical properties of bone. Osteoporos Int 14:S29-S36CrossRef
104.
Zurück zum Zitat Fantner GE, Birkedal H, Kindt JH, Hassenkam T, Weaver JC, Cutroni JA, Bosma BL, Bawazer L, Finch MM, Cidade GA, Morse DE, Stucky GD, Hansma PK (2004) Influence of the degradation of the organic matrix on the microscopic fracture behavior of trabecular bone. Bone 35:1013–1022CrossRefPubMed Fantner GE, Birkedal H, Kindt JH, Hassenkam T, Weaver JC, Cutroni JA, Bosma BL, Bawazer L, Finch MM, Cidade GA, Morse DE, Stucky GD, Hansma PK (2004) Influence of the degradation of the organic matrix on the microscopic fracture behavior of trabecular bone. Bone 35:1013–1022CrossRefPubMed
105.
Zurück zum Zitat Hert J, Fiala P, Petrtyl M (1994) Osteon orientation of the diaphysis of the long bones in man. Bone 15:269–277CrossRefPubMed Hert J, Fiala P, Petrtyl M (1994) Osteon orientation of the diaphysis of the long bones in man. Bone 15:269–277CrossRefPubMed
106.
Zurück zum Zitat Martin RB, Burr DB, Sharkey NA (1998) Skeletal tissue mechanics. Springer, Berlin Heidelberg New York Martin RB, Burr DB, Sharkey NA (1998) Skeletal tissue mechanics. Springer, Berlin Heidelberg New York
107.
Zurück zum Zitat Martin RB and Boardman DL (1993) The effects of collagen fiber orientation, porosity, density, and mineralization on bovine cortical bone bending properties. J Biomech 26:1047–1054PubMed Martin RB and Boardman DL (1993) The effects of collagen fiber orientation, porosity, density, and mineralization on bovine cortical bone bending properties. J Biomech 26:1047–1054PubMed
108.
Zurück zum Zitat Puustjarvi K, Nieminen J, Rasanen T, Hyttinen M, Helminen HJ, Kroger H, Huuskonen J, Alhava E, Kovanen V (2003) Do more highly organized collagen fibrils increase bone mechanical strength in loss of mineral density after one-year running training? J Bone Miner Res 14:321–329 Puustjarvi K, Nieminen J, Rasanen T, Hyttinen M, Helminen HJ, Kroger H, Huuskonen J, Alhava E, Kovanen V (2003) Do more highly organized collagen fibrils increase bone mechanical strength in loss of mineral density after one-year running training? J Bone Miner Res 14:321–329
109.
Zurück zum Zitat Oxlund H, Barckman M, Ortoft G, Andreassen TT (1995) Reduced concentrations of collagen cross-links are associated with reduced strength of bone. Bone 17:365S–371SPubMed Oxlund H, Barckman M, Ortoft G, Andreassen TT (1995) Reduced concentrations of collagen cross-links are associated with reduced strength of bone. Bone 17:365S–371SPubMed
110.
Zurück zum Zitat Lees S, Hanson D, Page E, Mook HA (1994) Comparison of dosage-dependent effects of beta-aminopropionitrile, sodium fluoride, and hydrocortisone on selected physical properties of cortical bone. J Bone Miner Res 9:1377–1389PubMed Lees S, Hanson D, Page E, Mook HA (1994) Comparison of dosage-dependent effects of beta-aminopropionitrile, sodium fluoride, and hydrocortisone on selected physical properties of cortical bone. J Bone Miner Res 9:1377–1389PubMed
111.
Zurück zum Zitat Masse PG, Rimnac CM, Yamauchi M, Coburn SP, Rucker RB, Howell DS, Boskey AL (1996) Pyridoxine deficiency affects biomechanical properties of chick tibial bone. Bone 18:567–574CrossRefPubMed Masse PG, Rimnac CM, Yamauchi M, Coburn SP, Rucker RB, Howell DS, Boskey AL (1996) Pyridoxine deficiency affects biomechanical properties of chick tibial bone. Bone 18:567–574CrossRefPubMed
112.
Zurück zum Zitat Opsahl W, Zeronian H, Ellison M, Lewis D, Rucker RB, Riggins RS (1982) Role of copper in collagen cross-linking and its influence on selected mechanical properties on selected mechanical properties of chick bone and tendon. J Nutr 112:708–716PubMed Opsahl W, Zeronian H, Ellison M, Lewis D, Rucker RB, Riggins RS (1982) Role of copper in collagen cross-linking and its influence on selected mechanical properties on selected mechanical properties of chick bone and tendon. J Nutr 112:708–716PubMed
113.
Zurück zum Zitat Banse X, Devogelaer JP, Lafosse A, Sims TJ, Grynpas M, Bailey AJ (2002) Cross-link profile of bone collagen correlates with structural organization of trabeculae. Bone 31:70–76CrossRefPubMed Banse X, Devogelaer JP, Lafosse A, Sims TJ, Grynpas M, Bailey AJ (2002) Cross-link profile of bone collagen correlates with structural organization of trabeculae. Bone 31:70–76CrossRefPubMed
114.
Zurück zum Zitat Banse X, Sims TJ, Bailey AJ (2002) Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res 17:1621–1628PubMed Banse X, Sims TJ, Bailey AJ (2002) Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res 17:1621–1628PubMed
115.
Zurück zum Zitat Uzawa K, Grzesik WJ, Nishiura T, Kuznetsov SA, Robey PG, Brenner DA, Yamauchi M (1999) Differential expression of human lysyl hydroxylase genes, lysine hydroxylation, and cross-linking of type I collagen during osteoblastic differentiation in vitro. J Bone Miner Res 14:1272–1280PubMed Uzawa K, Grzesik WJ, Nishiura T, Kuznetsov SA, Robey PG, Brenner DA, Yamauchi M (1999) Differential expression of human lysyl hydroxylase genes, lysine hydroxylation, and cross-linking of type I collagen during osteoblastic differentiation in vitro. J Bone Miner Res 14:1272–1280PubMed
116.
Zurück zum Zitat Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M (2004) Lysyl hydroxylase-2b directs collagen cross-linking pathways in MC3T3-E1 cells. J Bone Miner Res 19:1349–1355PubMed Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M (2004) Lysyl hydroxylase-2b directs collagen cross-linking pathways in MC3T3-E1 cells. J Bone Miner Res 19:1349–1355PubMed
117.
Zurück zum Zitat Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M (2005) Overexpression of lysyl hydroxylase-2b leads to defective collagen fibrillogenesis and matrix mineralization. J Bone Miner Res 20:81–87PubMed Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M (2005) Overexpression of lysyl hydroxylase-2b leads to defective collagen fibrillogenesis and matrix mineralization. J Bone Miner Res 20:81–87PubMed
118.
Zurück zum Zitat Vashishth D, Wu P, Gibson GJ (2003) Age-related loss in bone toughness is explained by non-enzymatic glycation of collagen. 49th annual meeting of the Orthopaedic Research Society, New Orleans Vashishth D, Wu P, Gibson GJ (2003) Age-related loss in bone toughness is explained by non-enzymatic glycation of collagen. 49th annual meeting of the Orthopaedic Research Society, New Orleans
119.
Zurück zum Zitat Boxberger J, Vashishth D (2003) Nonenzymatic glycation affects bone fracture by modifying creep and inelastic properties of collagen. 49th annual meeting of the Orthopaedic Research Society, New Orleans Boxberger J, Vashishth D (2003) Nonenzymatic glycation affects bone fracture by modifying creep and inelastic properties of collagen. 49th annual meeting of the Orthopaedic Research Society, New Orleans
120.
Zurück zum Zitat Wu P, Koharski C, Nonnemann H, Vashishth D (2003) Loading of non-enzymatically glycated and damaged bone results in an instantaneous fracture. 49th annual meeting of the Orthopaedic Research Society, New Orleans Wu P, Koharski C, Nonnemann H, Vashishth D (2003) Loading of non-enzymatically glycated and damaged bone results in an instantaneous fracture. 49th annual meeting of the Orthopaedic Research Society, New Orleans
121.
Zurück zum Zitat Garnero P, Proust Y, Borel O, Gineyts E, Duboeuf F, Solberg H, Delmas P (2003) Collagen crosslinking modifies the mechanical properties of cortical bone. J Bone Miner Res 18(Suppl 2):S196 Garnero P, Proust Y, Borel O, Gineyts E, Duboeuf F, Solberg H, Delmas P (2003) Collagen crosslinking modifies the mechanical properties of cortical bone. J Bone Miner Res 18(Suppl 2):S196
122.
Zurück zum Zitat Garnero P, Borel O, Gineyts E, Duboeuf F, Christiansen C, Delmas P (2004) The degree of posttranslational modifications of collagen is an important determinant of the toughness of cortical bone. J Bone Miner Res 19(Suppl 1):S220 Garnero P, Borel O, Gineyts E, Duboeuf F, Christiansen C, Delmas P (2004) The degree of posttranslational modifications of collagen is an important determinant of the toughness of cortical bone. J Bone Miner Res 19(Suppl 1):S220
124.
Zurück zum Zitat Kirsch E, Krieg T, Remberger K, Fendel H, Bruckner P, Muller PK (1981) Disorder of collagen metabolism in a patient with osteogenesis imperfecta (lethal type): increased degree of hydroxylation of lysine in collagen type I and III. Eur J Clin Invest 11:39–47PubMed Kirsch E, Krieg T, Remberger K, Fendel H, Bruckner P, Muller PK (1981) Disorder of collagen metabolism in a patient with osteogenesis imperfecta (lethal type): increased degree of hydroxylation of lysine in collagen type I and III. Eur J Clin Invest 11:39–47PubMed
125.
Zurück zum Zitat Grabner B, Landis WJ, Roschger P, Rinnerthaler S, Peterlik H, Klaushofer K, Fratzl P (2001) Age- and genotype-dependence of bone material properties in the osteogenesis imperfecta murine model (oim). Bone 29:453–457CrossRefPubMed Grabner B, Landis WJ, Roschger P, Rinnerthaler S, Peterlik H, Klaushofer K, Fratzl P (2001) Age- and genotype-dependence of bone material properties in the osteogenesis imperfecta murine model (oim). Bone 29:453–457CrossRefPubMed
126.
Zurück zum Zitat Jepsen KJ, Schaffler MB, Kuhn JL, Goulet RW, Bonadio J, Goldstein SA (1997) Type I collagen mutation alters the strength and fatigue behavior of Mov 13 cortical tissue. J Biomech 30:1141–1147CrossRefPubMed Jepsen KJ, Schaffler MB, Kuhn JL, Goulet RW, Bonadio J, Goldstein SA (1997) Type I collagen mutation alters the strength and fatigue behavior of Mov 13 cortical tissue. J Biomech 30:1141–1147CrossRefPubMed
127.
Zurück zum Zitat Pereira RF, Hume EL, Halford KW, Prockop DJ (1995) Bone fragility in transgenic mice expressing a mutated gene for type I procollagen (COL1A1) parallels the age-dependent phenotype of human osteogenesis imperfecta. J Bone Miner Res 10:1837–1843PubMed Pereira RF, Hume EL, Halford KW, Prockop DJ (1995) Bone fragility in transgenic mice expressing a mutated gene for type I procollagen (COL1A1) parallels the age-dependent phenotype of human osteogenesis imperfecta. J Bone Miner Res 10:1837–1843PubMed
128.
Zurück zum Zitat Garnero P, Fledelius C, Gineyts E, Serre CM, Vignot E, Delmas PD (1997) Decreased beta-isomerization of the C-terminal telopeptide of type I collagen alpha 1 chain in Paget’s disease of bone. J Bone Miner Res 12:1407–1415PubMed Garnero P, Fledelius C, Gineyts E, Serre CM, Vignot E, Delmas PD (1997) Decreased beta-isomerization of the C-terminal telopeptide of type I collagen alpha 1 chain in Paget’s disease of bone. J Bone Miner Res 12:1407–1415PubMed
129.
Zurück zum Zitat Garnero P, Gineyts E, Schaffer AV, Seaman J, Delmas PD (1998) Measurement of urinary excretion of nonisomerized an beta-isomerized forms of type I collagen breackdown products to monitor the effects of the bisphosphonate zoledronate in Paget’s disease. Arthritis Rheum 41:354–360CrossRefPubMed Garnero P, Gineyts E, Schaffer AV, Seaman J, Delmas PD (1998) Measurement of urinary excretion of nonisomerized an beta-isomerized forms of type I collagen breackdown products to monitor the effects of the bisphosphonate zoledronate in Paget’s disease. Arthritis Rheum 41:354–360CrossRefPubMed
130.
Zurück zum Zitat Mikkonen L, Tuominen T and Kulonen E (1960) Collagen fractions in lathyritic rats. Bioch Pharma 3:181–183CrossRef Mikkonen L, Tuominen T and Kulonen E (1960) Collagen fractions in lathyritic rats. Bioch Pharma 3:181–183CrossRef
131.
Zurück zum Zitat Lees S, Barnard S, Mook H (1987) Neutron studies of collagen in lathyritic bone. Int J Biol Macromol 9:32–38CrossRef Lees S, Barnard S, Mook H (1987) Neutron studies of collagen in lathyritic bone. Int J Biol Macromol 9:32–38CrossRef
132.
Zurück zum Zitat Grant SF, Reid DM, Blake G, Herd R, Fogelman I, Ralston SH (1996) Reduced bone density and osteoporosis associated with a polymorphic Sp1 binding site in the collagen type I alpha 1 gene. Nature Genet 14:40–45CrossRef Grant SF, Reid DM, Blake G, Herd R, Fogelman I, Ralston SH (1996) Reduced bone density and osteoporosis associated with a polymorphic Sp1 binding site in the collagen type I alpha 1 gene. Nature Genet 14:40–45CrossRef
133.
Zurück zum Zitat Mann V and Ralston SH (2003) Meta-analysis of COL1A1 Sp1 polymorphism in relation to bone mineral density and osteoporotic fracture. Bone 32:711–717CrossRefPubMed Mann V and Ralston SH (2003) Meta-analysis of COL1A1 Sp1 polymorphism in relation to bone mineral density and osteoporotic fracture. Bone 32:711–717CrossRefPubMed
134.
Zurück zum Zitat Mann V, Hobson EE, Li B, Stewart TL, Grant SF, Robins SP, Aspden RM, Ralston SH (2001) A COL1A Sp1 binding site polymorphism predisposes to osteoporotic fracture by affecting bone density and quality. J Clin Invest 107:899–907PubMed Mann V, Hobson EE, Li B, Stewart TL, Grant SF, Robins SP, Aspden RM, Ralston SH (2001) A COL1A Sp1 binding site polymorphism predisposes to osteoporotic fracture by affecting bone density and quality. J Clin Invest 107:899–907PubMed
135.
Zurück zum Zitat Uitterlinden AG, Burger H, Huang Q, Yue F, McGuigan FE, Grant SF, Hofman A, van Leeuwen JP, Pols HA, Ralston SH (1998) Relation of alleles of the collagen type I alpha1 gene to bone density and the risk of osteoporotic fractures in postmenopausal women. N Engl J Med 338:1016–1021CrossRefPubMed Uitterlinden AG, Burger H, Huang Q, Yue F, McGuigan FE, Grant SF, Hofman A, van Leeuwen JP, Pols HA, Ralston SH (1998) Relation of alleles of the collagen type I alpha1 gene to bone density and the risk of osteoporotic fractures in postmenopausal women. N Engl J Med 338:1016–1021CrossRefPubMed
136.
Zurück zum Zitat Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR (2001) Older women with diabetes have an increased risk of fractures: a prospective study. J Clin Endocrinol Metab 86:32–38CrossRefPubMed Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR (2001) Older women with diabetes have an increased risk of fractures: a prospective study. J Clin Endocrinol Metab 86:32–38CrossRefPubMed
137.
Zurück zum Zitat Nicodemus KK, Folsom AR (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197PubMed Nicodemus KK, Folsom AR (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197PubMed
138.
Zurück zum Zitat Keegan TH, Kelsey JL, Sidney S, Quesenberry CP Jr (2002) Foot problems as risk factors of fractures. Am J Epidemiol 155:926–931CrossRefPubMed Keegan TH, Kelsey JL, Sidney S, Quesenberry CP Jr (2002) Foot problems as risk factors of fractures. Am J Epidemiol 155:926–931CrossRefPubMed
139.
Zurück zum Zitat Reddy KG, Stehno-bittel L, Hamade S, Enwemeka CS (2001) The biomechanical integrity of bone in experimemtal diabetes. Diabetes Res Cli Pract 54:1–8CrossRef Reddy KG, Stehno-bittel L, Hamade S, Enwemeka CS (2001) The biomechanical integrity of bone in experimemtal diabetes. Diabetes Res Cli Pract 54:1–8CrossRef
140.
Zurück zum Zitat Verhaeghe J, Suiker AM, Einhorn TA, Geusens P, Visser WJ, Van Herck E, Van Bree R, Magitsky S, Bouillon R (1994) Brittle bones in spontaneously diabetic female rats cannot be predicted by bone mineral measurements: studies in diabetic and ovariectomized rats. J Bone Miner Res 9:1657–1667PubMedCrossRef Verhaeghe J, Suiker AM, Einhorn TA, Geusens P, Visser WJ, Van Herck E, Van Bree R, Magitsky S, Bouillon R (1994) Brittle bones in spontaneously diabetic female rats cannot be predicted by bone mineral measurements: studies in diabetic and ovariectomized rats. J Bone Miner Res 9:1657–1667PubMedCrossRef
141.
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 28:1297–1310CrossRefPubMed 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 28:1297–1310CrossRefPubMed
142.
Zurück zum Zitat Sanada H, Shikata J, Hamamoto H, Ueba Y, Yamamuro T, Takeda T (1978) Changes in collagen cross-linking and lysyl oxidase by estrogen. Biochim Biophys Acta 541:408–413PubMed Sanada H, Shikata J, Hamamoto H, Ueba Y, Yamamuro T, Takeda T (1978) Changes in collagen cross-linking and lysyl oxidase by estrogen. Biochim Biophys Acta 541:408–413PubMed
143.
Zurück zum Zitat Feres-Filho EJ, Choi YJ, Han X, Takala TE, Trackman PC (1995) Pre-translational and post-translational regulation of lysyl oxidase by transforming growth-factor-beta-1 in osteoblastic MC3T3-E1 cells. J Biol Chem 270:30797–30803CrossRefPubMed Feres-Filho EJ, Choi YJ, Han X, Takala TE, Trackman PC (1995) Pre-translational and post-translational regulation of lysyl oxidase by transforming growth-factor-beta-1 in osteoblastic MC3T3-E1 cells. J Biol Chem 270:30797–30803CrossRefPubMed
144.
Zurück zum Zitat Seitzer U, Batge B, Acil Y, Muller PK (1995) Transforming growth-factor beta 1 influences lysyl hydroxylation of collagen I and reduces steady-state level of lysyl hydroxylase mRNA in human osteoblast-like cells. Eur J Clin Invest 25:959–966PubMed Seitzer U, Batge B, Acil Y, Muller PK (1995) Transforming growth-factor beta 1 influences lysyl hydroxylation of collagen I and reduces steady-state level of lysyl hydroxylase mRNA in human osteoblast-like cells. Eur J Clin Invest 25:959–966PubMed
145.
Zurück zum Zitat Kowitz J, Knippel M, Schuhr T, Mach J (1997) Alteration in the extent of collagen I hydroxylation, isolated from femoral heads of women with a femoral neck fracture caused by osteoporosis. Calcif Tissue Int 60:501–505CrossRefPubMed Kowitz J, Knippel M, Schuhr T, Mach J (1997) Alteration in the extent of collagen I hydroxylation, isolated from femoral heads of women with a femoral neck fracture caused by osteoporosis. Calcif Tissue Int 60:501–505CrossRefPubMed
146.
Zurück zum Zitat Batge B, Diebold J, Stein H, Bodo M, Muller PK (1992) Compositionnal analysis of the collagenous bone matrix. A study on adult normal and osteopenic bone tissue. Eur J Clin Invest 22:805–812PubMed Batge B, Diebold J, Stein H, Bodo M, Muller PK (1992) Compositionnal analysis of the collagenous bone matrix. A study on adult normal and osteopenic bone tissue. Eur J Clin Invest 22:805–812PubMed
147.
Zurück zum Zitat Bailey AJ, Wotton SF, Sims TJ, Thompson PW (1993) Biochemical changes in the collagen of human osteoporotic bone matrix. Connect Tissue Res 29:119–132PubMed Bailey AJ, Wotton SF, Sims TJ, Thompson PW (1993) Biochemical changes in the collagen of human osteoporotic bone matrix. Connect Tissue Res 29:119–132PubMed
148.
Zurück zum Zitat Torre-Blanco A, Adachi E, Hojima Y, Wootton JA, Minor RR, Prockop DJ (1992) Temperature induced post-translational over-modification of type I collagen. Effects of over-modification of the protein on the rate of cleavage by procollagen N-proteinase and on self-assembly of collagen into fibrils. J Biol Chem 267:2650–2655PubMed Torre-Blanco A, Adachi E, Hojima Y, Wootton JA, Minor RR, Prockop DJ (1992) Temperature induced post-translational over-modification of type I collagen. Effects of over-modification of the protein on the rate of cleavage by procollagen N-proteinase and on self-assembly of collagen into fibrils. J Biol Chem 267:2650–2655PubMed
149.
Zurück zum Zitat Oxlund H, Mosekilde L, Ortoft G (1996) Reduced concentration of collagen reducible crosslinks in human trabecular bone with respect to age and osteoporosis. Bone 19:479–484CrossRefPubMed Oxlund H, Mosekilde L, Ortoft G (1996) Reduced concentration of collagen reducible crosslinks in human trabecular bone with respect to age and osteoporosis. Bone 19:479–484CrossRefPubMed
150.
Zurück zum Zitat Paschalis EP, Shane E, Lyritis G, Skarantavos G, Mendelsohn R, Boskey AL (2004) Bone fragility and collagen cross-links. J Bone Miner Res 19:2000–2004PubMed Paschalis EP, Shane E, Lyritis G, Skarantavos G, Mendelsohn R, Boskey AL (2004) Bone fragility and collagen cross-links. J Bone Miner Res 19:2000–2004PubMed
151.
Zurück zum Zitat Garnero P, Cloos P, Sornay-Rendu E, Qvist P, Delmas PD (2002) Type I collagen racemization and isomerisation and the risk of fracture in postmenopausal women: the OFELY prospective study. J Bone Miner Res 17:826–833PubMed Garnero P, Cloos P, Sornay-Rendu E, Qvist P, Delmas PD (2002) Type I collagen racemization and isomerisation and the risk of fracture in postmenopausal women: the OFELY prospective study. J Bone Miner Res 17:826–833PubMed
Metadaten
Titel
The role of collagen in bone strength
verfasst von
S. Viguet-Carrin
P. Garnero
P. D. Delmas
Publikationsdatum
01.03.2006
Verlag
Springer-Verlag
Erschienen in
Osteoporosis International / Ausgabe 3/2006
Print ISSN: 0937-941X
Elektronische ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-005-2035-9

Weitere Artikel der Ausgabe 3/2006

Osteoporosis International 3/2006 Zur Ausgabe

Letter

Letter

Arthropedia

Grundlagenwissen der Arthroskopie und Gelenkchirurgie. Erweitert durch Fallbeispiele, Videos und Abbildungen. 
» Jetzt entdecken

Update Orthopädie und Unfallchirurgie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.