DOI: 10.1083/jcb.136.2.459. Abnormal Compartmentalization of Cartilage Matrix Components in Mice Lacking Collagen X: Implications for Function

Abnormal Compartmentalization of Cartilage Matrix Components in Mice Lacking Collagen X: Implications for Function

10.1083/jcb.136.2.459

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

There are conflicting views on whether collagen X is a purely structural molecule, or regulates bone mineralization during endochondral ossification. Mutations in the human collagen α1(X) gene (COL10A1) in Schmid metaphyseal chondrodysplasia (SMCD) suggest a supportive role. But mouse collagen α1(X) gene (Col10a1) null mutants were previously reported to show no obvious phenotypic change. We have generated collagen X deficient mice, which shows that deficiency does have phenotypic consequences which partly resemble SMCD, such as abnormal trabecular bone architecture. In particular, the mutant mice develop coxa vara, a phenotypic change common in human SMCD. Other consequences of the mutation are reduction in thickness of growth plate resting zone and articular cartilage, altered bone content, and atypical distribution of matrix components within growth plate cartilage. We propose that collagen X plays a role in the normal distribution of matrix vesicles and proteoglycans within the growth plate matrix. Collagen X deficiency impacts on the supporting properties of the growth plate and the mineralization process, resulting in abnormal trabecular bone. This hypothesis would accommodate the previously conflicting views of the function of collagen X and of the molecular pathogenesis of SMCD.

Bibliography

Kwan, K. M., Pang, M. K. M., Zhou, S., Cowan, S. K., Kong, R. Y. C., Pfordte, T., Olsen, B. R., Sillence, D. O., Tam, P. P. L., & Cheah, K. S. E. (1997). Abnormal Compartmentalization of Cartilage Matrix Components in Mice Lacking Collagen X: Implications for Function. The Journal of Cell Biology, 136(2), 459â471.

Authors 10

Kin Ming Kwan (first)
Michael K.M. Pang (additional)
Sheila Zhou (additional)
Soot Keng Cowan (additional)
Richard Y.C. Kong (additional)
Tim Pfordte (additional)
Bjorn R. Olsen (additional)
David O. Sillence (additional)
Patrick P.L. Tam (additional)
Kathryn S.E. Cheah (additional)

References 48 Referenced 156

10.1007/BF02899263 / Virchows Arch B Cell Pathol / Type X collagen expression in osteoarthritic and rheumatoid articular cartilage by Aigner (1993)
{'key': '2023072823015227900_B2', 'first-page': '320', 'article-title': 'Biology of disease. Mechanism of mineral formation in bone', 'volume': '60', 'author': 'Anderson', 'year': '1989', 'journal-title': 'Lab Invest'} / Lab Invest / Biology of disease. Mechanism of mineral formation in bone by Anderson (1989)
{'key': '2023072823015227900_B3', 'first-page': '266', 'article-title': 'Molecular biology of matrix vesicles', 'volume': '314', 'author': 'Anderson', 'year': '1995', 'journal-title': 'Clin Orthop Rel Res'} / Clin Orthop Rel Res / Molecular biology of matrix vesicles by Anderson (1995)
10.1083/jcb.115.4.1171 / J Cell Biol / Elevated extracellular calcium concentrations induce type X collagen synthesis in chondrocyte cultures by Bonen (1991)
10.1097/00003086-199208000-00041 / Clin Orthop Rel Res / Mineral-matrix interactions in bone and cartilage by Boskey (1992)
10.1074/jbc.270.9.4558 / J Biol Chem / Type x collagen multimer assembly in vitro is prevented by a gly618to val mutation in the α1(X) NC1 domain resulting in Schmid metaphyseal chondrodysplasia by Chan (1995)
{'key': '2023072823015227900_B7'}
10.1242/dev.111.4.945 / Development / Expression of the mouse α1(II) collagen gene is not restricted to cartilage during development by Cheah (1991)
{'key': '2023072823015227900_B9'}
10.1083/jcb.117.3.687 / J Cell Biol / Domains of type X collagen: alteration of cartilage matrix by fibril association and proteoglycan accumulation by Chen (1992)
10.1002/ar.1092300402 / Anat Rec / A contribution with review to the description of mineralization of bone and other calcified tissues in vivo by Christofferson (1991)
10.1016/0092-8674(95)90487-5 / Cell / Toward a molecular understanding of skeletal development by Erlebacher (1995)
10.1016/S0174-173X(86)80023-1 / Coll Rel Res / The immunoperoxidase localization of type X collagen in chick cartilage and lung by Gibson (1986)
10.1016/S0021-9258(18)48010-6 / J Biol Chem / Type X collagen synthesis during endochondral ossification in fracture repair by Grant (1987)
{'key': '2023072823015227900_B15'}
10.1016/0169-6009(91)90005-K / Bone Miner / Distribution of type X collagen mRNA in normal and osteoarthritic human cartilage by Hoyland (1991)
10.1097/00003086-199101000-00035 / Clin Orthop Rel Res / Role of proteoglycan in the provisional calcification of cartilage by Hunter (1991)
10.1016/S0022-5320(82)90036-3 / J Ultrastruct Res / Improved cartilage fixation by ruthenium hexammine trichloride (RHT). A prerequisite for morphometry in growth cartilage by Hunziker (1982)
10.1016/S0030-5898(20)31561-3 / Orthop Clin North Am / Growth plate physiology and pathology by Iannotti (1990)
{'key': '2023072823015227900_B20', 'first-page': '427', 'article-title': 'A dominant negative mutation in the α1(X) collagen gene produces spondylometaphyseal defects in mice', 'volume': '383B', 'author': 'Jacenko', 'year': '1993', 'journal-title': 'Prog Clin Biol Res'} / Prog Clin Biol Res / A dominant negative mutation in the α1(X) collagen gene produces spondylometaphyseal defects in mice by Jacenko (1993)
10.1038/365056a0 / Nature (Lond) / Spondylometaphyseal dysplasia in mice carrying a dominant negative mutation in a matrix protein specific for cartilage-to-bone transition by Jacenko (1993)
10.1016/0014-5793(92)81316-E / FEBS Lett / Selective binding of anchorin CII (annexin V) to type II and X collagen and to chondrocalcin (C-propeptide of type II collagen): implications for anchoring function between matrix vesicles and matrix proteins by Kirsch (1992)
10.1016/S0021-9258(19)78146-0 / J Biol Chem / Stimulation of calcification of growth plate cartilage matrix vesicles by binding to type II and X collagens by Kirsch (1994)
10.1111/j.1432-0436.1992.tb00503.x / Differentiation / Ascorbate independent differentiation of human chondrocytes in vitro: simultaneous expression of types I and X collagen and matrix mineralization by Kirsch (1992)
10.1016/S0021-9258(17)32133-6 / J Biol Chem / Roles of the nucleational core complex and collagens (types II and X) in calcification of growth plate cartilage matrix vesicles by Kirsch (1994)
10.1111/j.1432-1033.1993.tb17739.x / Eur J Biochem / Intron-exon structure, alternative use of promoter and expression of the mouse collagen X gene, Col10a-1. by Kong (1993)
10.1083/jcb.114.3.597 / J Cell Biol / Macromolecular organization of chicken type X collagen in vitro by Kwan (1991)
10.1007/BF02387549 / Pediatr Radiol / Metaphyseal chondrodysplasia, Schmid type clinical and radiographic deliniation with a review of literature by Lachman (1988)
{'key': '2023072823015227900_B29', 'first-page': '59', 'article-title': 'Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r)', 'volume': '75', 'author': 'Liu', 'year': '1993', 'journal-title': 'Cell'} / Cell / Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r) by Liu (1993)
{'key': '2023072823015227900_B30'}
{'key': '2023072823015227900_B31'}
10.1002/humu.1380050204 / Hum Mutat / Concentration of mutations causing Schmid metaphyseal chondrodysplasia in the C-terminal noncollagenous domain of type X collagen by McIntosh (1995)
10.1111/j.1432-1033.1991.tb15951.x / Eur J Biochem / The complete primary structure of the human alpha 1(VIII) chain and assignment of its gene (COL8A1) to chromosome 3 by Muragaki (1991)
10.1016/S0021-9258(20)89508-8 / J Biol Chem / The alpha 2(VIII) collagen gene. A novel member of the short chain collagen family located on the human chromosome 1 by Muragaki (1991)
10.1083/jcb.109.5.2547 / J Cell Biol / Immunoelectron microscopic studies of type X collagen in endochondral ossification by Poole (1989)
10.1016/0092-8674(93)90229-J / Cell / Hoxb-4 (Hox-2.6)mutant mice show homeotic transformation of a cervical vertebra and defects in the closure of the sternal rudiments by Ramírez-Solis (1993)
10.1038/ng1094-129 / Nature Genet / Normal long bone growth and development in type x collagen-null mice by Rosati (1994)
10.1083/jcb.100.2.598 / J Cell Biol / Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues by Schmid (1985)
{'key': '2023072823015227900_B39'}
10.1016/0012-1606(90)90176-J / Dev Biol / Immunoelectron microscopy of type X collagen: supramolecular forms within embryonic chick cartilage by Schmid (1990)
10.1111/j.1749-6632.1990.tb17918.x / Ann NY Acad Sci / Hypertrophic cartilage matrix: Type X collagen, supramolecular assembly, and calcification by Schmid (1990)
{'key': '2023072823015227900_B42', 'first-page': '533', 'article-title': 'Late events in chondrocyte differentiation: hypertrophy, type X collagen synthesis and matrix calcification', 'volume': '5', 'author': 'Schmid', 'year': '1991', 'journal-title': 'In Vivo'} / In Vivo / Late events in chondrocyte differentiation: hypertrophy, type X collagen synthesis and matrix calcification by Schmid (1991)
10.1097/00003086-199411000-00032 / Clin Orthop / Type X collagen in fracture callus and the effects of experimental diabetes by Topping (1994)
10.1002/art.1780350715 / Arthritis Rheum / Type X collagen synthesis in human osteoarthritic cartilage: indication of chondrocyte hypertrophy by Von der Mark (1992)
10.1016/0960-9822(93)90069-Z / Curr Biol / Here today, bone tomorrow by Wallis (1993)
{'key': '2023072823015227900_B46', 'first-page': '169', 'article-title': 'Amino acid substitutions of conserved residues in the carboxyl-terminal domain of the α1(X) chain of type X collagen occur in two unrelated families with metaphyseal chondrodysplasia type Schmid', 'volume': '54', 'author': 'Wallis', 'year': '1994', 'journal-title': 'Am J Hum Genet'} / Am J Hum Genet / Amino acid substitutions of conserved residues in the carboxyl-terminal domain of the α1(X) chain of type X collagen occur in two unrelated families with metaphyseal chondrodysplasia type Schmid by Wallis (1994)
10.1038/ng0993-79 / Nature Genet / A type X collagen mutation causes Schmid metaphyseal chondrodysplasia by Warman (1993)
10.1016/S0021-9258(17)35300-0 / J Biol Chem / Association between proteoglycans and matrix vesicles in the extracellular matrix of growth plate cartilage by Wu (1991)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:46 p.m.)
Deposited	2 years, 1 month ago (July 28, 2023, 7:03 p.m.)
Indexed	1 month, 1 week ago (July 22, 2025, 6:45 a.m.)
Issued	28 years, 7 months ago (Jan. 27, 1997)
Published	28 years, 7 months ago (Jan. 27, 1997)
Published Online	28 years, 7 months ago (Jan. 27, 1997)
Published Print	28 years, 7 months ago (Jan. 27, 1997)

Funders 0

None

BibTeX

@article{Kwan_1997, title={Abnormal Compartmentalization of Cartilage Matrix Components in Mice Lacking Collagen X: Implications for Function}, volume={136}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.136.2.459}, DOI={10.1083/jcb.136.2.459}, number={2}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Kwan, Kin Ming and Pang, Michael K.M. and Zhou, Sheila and Cowan, Soot Keng and Kong, Richard Y.C. and Pfordte, Tim and Olsen, Bjorn R. and Sillence, David O. and Tam, Patrick P.L. and Cheah, Kathryn S.E.}, year={1997}, month=jan, pages={459–471} }

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      "author": "Kong",
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      "author": "McIntosh",
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