Collagen of fibrocartilage: a distinctive molecular phenotype in bovine meniscus

Eyre, David R.; Wu, Jiann Jiu

doi:10.1016/0014-5793(83)80592-4

Cited by 161 publications

(80 citation statements)

References 13 publications

(5 reference statements)

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“…2) was seen in any of the collagen preparations from articular cartilage. The appearance of the ␣1(V) chain in the adult tissue therefore was not due simply to a switch in basic collagen phenotype from collagen II to collagen I with accompanying collagen V, a molecular phenotype that occurs for example in fibrocartilages (21).…”

Section: Resultsmentioning

confidence: 99%

Differences in Chain Usage and Cross-linking Specificities of Cartilage Type V/XI Collagen Isoforms with Age and Tissue

Weis

Kim

et al. 2009

Journal of Biological Chemistry

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Collagen type V/XI is a minor but essential component of collagen fibrils in vertebrates. We here report on age-and tissuerelated variations in isoform usage in cartilages. With maturation of articular cartilage, the ␣1(V) chain progressively replaced the ␣2(XI) chain. A mix of the molecular isoforms, ␣1(XI)␣1(V)␣3(XI) and ␣1(XI)␣2(XI)␣3(XI), best explained this finding. A prominence of ␣1(V) chains is therefore characteristic and a potential biomarker of mature mammalian articular cartilage. Analysis of cross-linked peptides showed that the ␣1(V) chains were primarily cross-linked to ␣1(XI) chains in the tissue and hence an integral component of the V/XI polymer. From nucleus pulposus of the intervertebral disc (in which the bulk collagen monomer is type II as in articular cartilage), type V/XI collagen consisted of a mix of five genetically distinct chains, ␣1(XI), ␣2(XI), ␣3(XI), ␣1(V), and ␣2(V). These presumably were derived from several different molecular isoforms, including ␣1(XI)␣2(XI)␣3(XI), (␣1(XI)) 2 ␣2(V), and others. Meniscal fibrocartilage shows yet another V/XI phenotype. The findings support and extend the concept that the clade B subfamily of COL5 and COL11 gene products should be considered members of the same collagen subfamily, from which, in combination with clade A gene products (COL2A1 or COL5A2), a range of molecular isoforms has evolved into tissue-dependent usage. We propose an evolving role for collagen V/XI isoforms as an adaptable polymeric template of fibril macro-architecture.The collagen framework of hyaline cartilages is based on a covalently cross-linked heteropolymeric network of types II, IX, and XI collagens. During development, collagen type IX molecules are covalently linked to the surface of thin, new fibrils of type II collagen polymerized on a template of type XI collagen (1-5). In fetal cartilage, type XI collagen is a heterotrimer of three genetically distinct chains, ␣1(XI), ␣2(XI), and ␣3(XI) in a 1:1:1 ratio (6 -9). The ␣3(XI) chain has the same primary sequence as ␣1(II), but the chains differ in their posttranslational processing and cross-linking properties (7-9). All three collagen subunits, II, IX, and XI, are heavily cross-linked in the same fibril through a lysyl oxidase-mediated mechanism (2, 5, 9). The location of the cross-links determined by sequence analysis of peptides prepared from proteolytically degraded fibrils reveals a high degree of chain specificity (9). Collagen XI molecules are linked to each other in a head-to-tail fashion by N-telopeptide 2 to helix cross-links and laterally to type II collagen molecules through ␣1(II) C-telopeptides (9). Isolated from mature articular cartilage, type XI collagen includes a significant pool of ␣1(V) chains (6), implying the presence of V/XI hybrid molecules. The ratio of type XI collagen to type II collagen is about 1 to 10 in fetal bovine and human epiphyseal cartilage when compared with 1 to 30 in adult articular cartilage. Similarly, the ratio of collagen IX to collagen II falls from about 1 to 10 to 1 t...

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Section: Resultsmentioning

confidence: 99%

Differences in Chain Usage and Cross-linking Specificities of Cartilage Type V/XI Collagen Isoforms with Age and Tissue

Weis

Kim

et al. 2009

Journal of Biological Chemistry

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“…Meniscus collagens were serially precipitated with 0.7, 0.9, and 1.2 M NaCl to separate types I/III, type II, and types V/XI, respectively. Collagen type II is a minor component of the meniscus and is highly modified post-translationally, causing it to precipitate at 0.9 M NaCl, separated from the bulk type I collagen (12). Portions of demineralized bone and guanidine HCl-extracted cartilage residue were digested with CNBr in 70% formic acid at room temperature for 24 h (13), and the resulting CB peptides were freeze-dried.…”

Section: Methodsmentioning

confidence: 99%

Location of 3-Hydroxyproline Residues in Collagen Types I, II, III, and V/XI Implies a Role in Fibril Supramolecular Assembly

Weis

Hudson

Kim

et al. 2010

Journal of Biological Chemistry

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Collagen triple helices are stabilized by 4-hydroxyproline residues. No function is known for the much less common 3-hydroxyproline (3Hyp), although genetic defects inhibiting its formation cause recessive osteogenesis imperfecta. To help understand the pathogenesis, we used mass spectrometry to identify the sites and local sequence motifs of 3Hyp residues in fibril-forming collagens from normal human and bovine tissues. The results confirm a single, essentially fully occupied 3Hyp site (A1) at Pro 986 in A-clade chains ␣1(I), ␣1(II), and ␣2(V). Two partially modified sites (A2 and A3) were found at Pro 944 in ␣1(II) and ␣2(V) and Pro 707 in ␣2(I) and ␣2(V), which differed from A1 in sequence motif. Significantly, the distance between sites 2 and 3, 237 residues, is close to the collagen D-period (234 residues). A search for additional D-periodic 3Hyp sites revealed a fourth site (A4) at Pro 470 in ␣2(V), 237 residues N-terminal to site 3. In contrast, human and bovine type III collagen contained no 3Hyp at any site, despite a candidate proline residue and recognizable A1 sequence motif. A conserved histidine in mammalian ␣1(III) at A1 may have prevented 3-hydroxylation because this site in chicken type III was fully hydroxylated, and tyrosine replaced histidine. All three B-clade type V/XI collagen chains revealed the same three sites of 3Hyp but at different loci and sequence contexts from those in A-clade collagen chains. Two of these B-clade sites were spaced apart by 231 residues. From these and other observations we propose a fundamental role for 3Hyp residues in the ordered self-assembly of collagen supramolecular structures.Collagens are the most abundant and ubiquitous proteins in multi-cellular animals. It is well established that 4-hydroxyproline (4Hyp) 2 residues stabilize the collagen triple helix through water-bridged intramolecular hydrogen bonding (1). However, the function of the much less abundant 3-hydroxyproline (3Hyp), although discovered 50 years ago, is unknown (2). Only 1-2 residues of 3Hyp occur per chain in collagen types I and II and 3-6 residues occur per chain in collagen types V and XI. The content is highest in type IV collagens of basement membranes in which 10% of the total hydroxyproline can be 3Hyp (3).Specific prolyl 3-hydroxylases (P3Hs) are responsible for 3Hyp synthesis. Three different genes encoding P3H1, P3H2, and P3H3 are present in the human genome, which show tissue specificity in their expression (4, 5). Substrate proline residues occur in a prerequisite sequence -Pro-4Hyp-Gly. The ␣1(I) chain has only one established 3Hyp site at Pro 986 in a motif conserved across vertebrate species (human GLPGPIGPPGPR) a close variant of which also occurs in type II collagen (human GIPGPIGPPGPR).Renewed interest in 3Hyp was recently sparked by the discovery that a recessive form of osteogenesis imperfecta (OI) is caused by mutations in CRTAP. This gene encodes a protein (cartilage-associated protein) that is bound to P3H1 and cyclophilin B in the endoplasmic reticulum and is requi...

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“…In the first family the type I procollagen was cleaved with pepsin, the cysteine residues in the a chains were modified with 4-vinyl pyridine (22), and the chains were separated by reverse-phase HPLC (23,24 In the second family the cysteines in the isolated proa chains of type I procollagen were reduced and carboxymethylated with iodoacetate after reduction for 4 h in 8 M urea with DTT. Sodium iodoacetate was added to a final concentration of 20 mM and after 15 min a fresh aliquot of DTT was added and the sample was dialyzed into 0.1 M acetic acid before lyophylization.…”

Section: Determination Ofthermal Stabilitymentioning

confidence: 99%

Osteogenesis imperfecta. The position of substitution for glycine by cysteine in the triple helical domain of the pro alpha 1(I) chains of type I collagen determines the clinical phenotype.

Starman¹,

Eyre²,

Charbonneau³

et al. 1989

J. Clin. Invest.

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Collagen of fibrocartilage: a distinctive molecular phenotype in bovine meniscus

Cited by 161 publications

References 13 publications

Differences in Chain Usage and Cross-linking Specificities of Cartilage Type V/XI Collagen Isoforms with Age and Tissue

Differences in Chain Usage and Cross-linking Specificities of Cartilage Type V/XI Collagen Isoforms with Age and Tissue

Location of 3-Hydroxyproline Residues in Collagen Types I, II, III, and V/XI Implies a Role in Fibril Supramolecular Assembly

Osteogenesis imperfecta. The position of substitution for glycine by cysteine in the triple helical domain of the pro alpha 1(I) chains of type I collagen determines the clinical phenotype.

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