Alteration of proteoglycan sulfation affects bone growth and remodeling

Bone

Volumn 54, Issue 1, 2013, Pages 83-91

  Gualeni, Benedetta ^a   de Vernejoul, Marie Christine ^b,c   Marty Morieux, Caroline ^b,c   De Leonardis, Fabio ^a   Franchi, Marco ^d   Monti, Luca ^a   Forlino, Antonella ^a   Houillier, Pascal ^e   Rossi, Antonio ^a   Geoffroy, Valerie ^b,c  

^a UNIVERSITY OF PAVIA   (Italy)

^b HÔPITAL LARIBOISIÈRE   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITY OF BOLOGNA   (Italy)

^e HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

Animal models; Bone histomorphometry; Diastrophic dysplasia; Osteoblasts; Osteoclasts; Proteoglycan

Indexed keywords

CALCIUM; CARBOXY TERMINAL TELOPEPTIDE; CARRIER PROTEIN; COLLAGEN FIBRIL; DEOXYPYRIDINOLINE; HYALIN; PARATHYROID HORMONE; PROTEOGLYCAN; SOLUTE CARRIER FAMILY 26 MEMBER 2; SULFATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE GROWTH; BONE MASS; BONE MATRIX; BONE REMODELING; CELL COUNT; CHONDRODYSPLASIA; CONTROLLED STUDY; DIASTROPHIC DYSPLASIA; DISEASE MODEL; ELECTRON MICROSCOPY; GENE; GENE MUTATION; HYALINE CARTILAGE; IN VIVO STUDY; MALE; MORPHOMETRICS; MOUSE; MOUSE MUTANT; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PATHOGENESIS; PERIOSTEUM; SLC26A2 GENE; SULFATION; TRABECULAR BONE; URINALYSIS; WILD TYPE;

AGING; ANIMALS; BONE AND BONES; BONE DENSITY; BONE DEVELOPMENT; BONE REMODELING; BONE RESORPTION; CALCIUM; CELL DIFFERENTIATION; COLLAGEN; DWARFISM; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; ORGAN SIZE; OSTEOCLASTS; PARATHYROID HORMONE; PROTEOGLYCANS; SULFUR;

EID: 84874383426     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.01.036     Document Type: Article

References (29)

1. Hästbacka J., de la Chapelle A., Mahtani M.M., Clines G., Reeve Daly M.P., Daly M., et al. The diastrophic dysplasia gene encodes a novel sulfate transporter: positional cloning by fine-structure linkage disequilibrium mapping. Cell 1994, 78:1073-1087.
2. Rossi A., Kaitila I., Wilcox W.R., Rimoin D.L., Steinmann B., Cetta G., et al. Proteoglycan sulfation in cartilage and cell cultures from patients with sulfate transporter chondrodysplasias: relationship to clinical severity and indications on the role of intracellular sulfate production. Matrix Biol 1998, 17:361-369.
3. Kvist A.J., Johnson A.E., Morgelin M., Gustafsson E., Bengtsson E., Lindblom K., et al. Chondroitin sulfate perlecan enhances collagen fibril formation. Implications for perlecan chondrodysplasias. J Biol Chem 2006, 281:33127-33139.
4. Superti-Furga A. Skeletal dysplasias related to defects in sulfate metabolism. Connective tissue and its heritable disorders 2002, 939-960. Wiley-Liss, New-York. B. Steinmann, P. Royce (Eds.).
5. Forlino A., Piazza R., Tiveron C., Della Torre S., Tatangelo L., Bonafe L., et al. A diastrophic dysplasia sulfate transporter (SLC26A2) mutant mouse: morphological and biochemical characterization of the resulting chondrodysplasia phenotype. Hum Mol Genet 2005, 14:859-871.
6. Gualeni B., Facchini M., De Leonardis F., Tenni R., Cetta G., Viola M., et al. Defective proteoglycan sulfation of the growth plate zones causes reduced chondrocyte proliferation via an altered Indian hedgehog signalling. Matrix Biol 2010, 29:453-460.
7. Zelzer E., Olsen B.R. The genetic basis for skeletal diseases. Nature 2003, 423:343-348.
8. Van Der Weyden L., Wei L., Luo J., Yang X., Birk D.E., Adams D.J., et al. Functional knockout of the matrilin-3 gene causes premature chondrocyte maturation to hypertrophy and increases bone mineral density and osteoarthritis. Am J Pathol 2006, 169:515-527.
9. Ho M.S., Tsang K.Y., Lo R.L., Susic M., Makitie O., Chan T.W., et al. COL10A1 nonsense and frame-shift mutations have a gain-of-function effect on the growth plate in human and mouse metaphyseal chondrodysplasia type Schmid. Hum Mol Genet 2007, 16:1201-1215.
10. Leighton M.P., Nundlall S., Starborg T., Meadows R.S., Suleman F., Knowles L., et al. Decreased chondrocyte proliferation and dysregulated apoptosis in the cartilage growth plate are key features of a murine model of epiphyseal dysplasia caused by a matn3 mutation. Hum Mol Genet 2007, 16:1728-1741.
11. Pirog-Garcia K.A., Meadows R.S., Knowles L., Heinegard D., Thornton D.J., Kadler K.E., et al. Reduced cell proliferation and increased apoptosis are significant pathological mechanisms in a murine model of mild pseudoachondroplasia resulting from a mutation in the C-terminal domain of COMP. Hum Mol Genet 2007, 16:2072-2088.
12. Rodgers K.D., Sasaki T., Aszodi A., Jacenko O. Reduced perlecan in mice results in chondrodysplasia resembling Schwartz-Jampel syndrome. Hum Mol Genet 2007, 16:515-528.
13. Blumbach K., Niehoff A., Paulsson M., Zaucke F. Ablation of collagen IX and COMP disrupts epiphyseal cartilage architecture. Matrix Biol 2008, 27:306-318.
14. Posey K.L., Hankenson K., Veerisetty A.C., Bornstein P., Lawler J., Hecht J.T. Skeletal abnormalities in mice lacking extracellular matrix proteins, thrombospondin-1, thrombospondin-3, thrombospondin-5, and type IX collagen. Am J Pathol 2008, 172:1664-1674.
15. Cortes M., Baria A.T., Schwartz N.B. Sulfation of chondroitin sulfate proteoglycans is necessary for proper Indian hedgehog signaling in the developing growth plate. Development 2009, 136:1697-1706.
16. Nieminen J., Sahlman J., Hirvonen T., Lapvetelainen T., Miettinen M., Arnala I., et al. Disturbed synthesis of type II collagen interferes with rate of bone formation and growth and increases bone resorption in transgenic mice. Calcif Tissue Int 2008, 82:229-237.
17. Su N., Du X., Chen L. FGF signaling: its role in bone development and human skeleton diseases. Front Biosci 2008, 13:2842-2865.
18. Valverde-Franco G., Liu H., Davidson D., Chai S., Valderrama-Carvajal H., Goltzman D., et al. Defective bone mineralization and osteopenia in young adult FGFR3-/- mice. Hum Mol Genet 2004, 13:271-284.
19. Mugniery E., Dacquin R., Marty C., Benoist-Lasselin C., de Vernejoul M.C., Jurdic P., et al. An activating Fgfr3 mutation affects trabecular bone formation via a paracrine mechanism during growth. Hum Mol Genet 2012, 21:2503-2513.
20. Esapa C.T., Hough T.A., Testori S., Head R.A., Crane E.A., Chan C.P., et al. A mouse model for spondyloepiphyseal dysplasia congenita with secondary osteoarthritis due to a Col2a1 mutation. J Bone Miner Res 2012, 27:413-428.
21. Su N., Sun Q., Li C., Lu X., Qi H., Chen S., et al. Gain-of-function mutation in FGFR3 in mice leads to decreased bone mass by affecting both osteoblastogenesis and osteoclastogenesis. Hum Mol Genet 2010, 19:1199-1210.
22. Glatt V., Canalis E., Stadmeyer L., Bouxsein M.L. Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. J Bone Miner Res 2007, 22:1197-1207.
23. Geoffroy V., Marty-Morieux C., Le Goupil N., Clement-Lacroix P., Terraz C., Frain M., et al. In vivo inhibition of osteoblastic metalloproteinases leads to increased trabecular bone mass. J Bone Miner Res 2004, 19:811-822.
24. Parfitt A.M., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., Meunier P.J., et al. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 1987, 2:595-610.
25. Sheehan D., Hrapchak B. Theory and practice of histotechnology 1980, St Louis, Mosby. 2nd ed.
26. Dobson K.R., Reading L., Haberey M., Marine X., Scutt A. Centrifugal isolation of bone marrow from bone: an improved method for the recovery and quantitation of bone marrow osteoprogenitor cells from rat tibiae and femurae. Calcif Tissue Int 1999, 65:411-413.
27. Hu J.C., Athanasiou K.A. Handbook of histology methods for bone and cartilage 2003, Humana Press Inc.
28. Xu T., Bianco P., Fisher L.W., Longenecker G., Smith E., Goldstein S., et al. Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat Genet 1998, 20:78-82.
29. Corsi A., Xu T., Chen X.D., Boyde A., Liang J., Mankani M., et al. Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J Bone Miner Res 2002, 17:1180-1189.