Snorc is a novel cartilage specific small membrane proteoglycan expressed in differentiating and articular chondrocytes

Osteoarthritis and Cartilage

Volumn 19, Issue 8, 2011, Pages 1026-1035

  Heinonen, J ^a   Taipaleenmaki H ^a   Roering, P ^a,b   Takatalo, M ^b   Harkness, L ^c   Sandholm, J ^a   Uusitalo Jarvinen H ^a,d   Kassem, M ^c,e   Kiviranta, I ^b,f   Laitala Leinonen, T ^a   Saamanen A M ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

^d TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^e KING SAUD UNIVERSITY   (Saudi Arabia)

^f JYVÄSKYLÄ CENTRAL HOSPITAL   (Finland)

Author keywords

Articular cartilage; Cartilage specific; Chondrogenesis; Chondroitin sulfate; Novel gene; Transmembrane proteoglycan

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; HYBRID PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; N ACETYLGALACTOSAMINE; N ACETYLGALACTOSAMINE 4 SULFATASE; N ACETYLGLUCOSAMINE; PROTEIN SNORC; PROTEOGLYCAN; SERINE; SIGNAL PEPTIDE; THREONINE; UNCLASSIFIED DRUG;

ACAN GENE; AGED; ANIMAL CELL; ARTICLE; ARTICULAR CARTILAGE; CALLUS; CARBOXY TERMINAL SEQUENCE; CARTILAGE DEGENERATION; CELL DIFFERENTIATION; CELL LYSATE; CELL MATURATION; CHONDROGENESIS; COL2A1 GENE; CONTROLLED STUDY; CYTOPLASM; EMBRYO; GENE; GENE EXPRESSION PROFILING; HOMEOSTASIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIMB BUD; MOUSE; NONHUMAN; PHENOTYPE; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SOX9 GENE; TISSUE SPECIFICITY; UPREGULATION; VERTEBRATE; WESTERN BLOTTING;

AGED; ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CHONDROCYTES; CHONDROGENESIS; CHONDROITIN SULFATE PROTEOGLYCANS; COLLAGEN TYPE II; HINDLIMB; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PROTEOGLYCANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 79960300279     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2011.04.016     Document Type: Article

References (46)

1. Olsen B.R., Reginato A.M., Wang W. Bone development. Annu Rev Cell Dev Biol 2000, 16:191-220.
2. Wuelling M., Vortkamp A. Transcriptional networks controlling chondrocyte proliferation and differentiation during endochondral ossification. Pediatr Nephrol 2010, 25:625-631.
3. Lefebvre V., Smits P. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C Embryo Today 2005, 75:200-212.
4. Goldring M.B., Tsuchimochi K., Ijiri K. The control of chondrogenesis. J Cell Biochem 2006, 97:33-44.
5. Watanabe H., de Caestecker M.P., Yamada Y. Transcriptional cross-talk between Smad, ERK1/2, and p38 mitogen-activated protein kinase pathways regulates transforming growth factor-beta-induced aggrecan gene expression in chondrogenic ATDC5 cells. J Biol Chem 2001, 276:14466-14473.
6. de Crombrugghe B., Lefebvre V., Behringer R.R., Bi W., Murakami S., Huang W. Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol 2000, 19:389-394.
7. Ornitz D.M. FGF signaling in the developing endochondral skeleton. Cytokine Growth Factor Rev 2005, 16:205-213.
8. Minina E., Kreschel C., Naski M.C., Ornitz D.M., Vortkamp A. Interaction of FGF, Ihh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev Cell 2002, 3:439-449.
9. Lefebvre V., Dumitriu B., Penzo-Mendez A., Han Y., Pallavi B. Control of cell fate and differentiation by SRY-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol 2007, 39:2195-2214.
10. Pan Q., Yu Y., Chen Q., Li C., Wu H., Wan Y., et al. Sox9, a key transcription factor of bone morphogenetic protein-2-induced chondrogenesis, is activated through BMP pathway and a CCAAT box in the proximal promoter. J Cell Physiol 2008, 217:228-241.
11. Zhao L., Li G., Zhou G.Q. SOX9 directly binds CREB as a novel synergism with the PKA pathway in BMP-2-induced osteochondrogenic differentiation. J Bone Miner Res 2009, 24:826-836.
12. Liu C.J., Zhang Y., Xu K., Parsons D., Alfonso D., Di Cesare P.E. Transcriptional activation of cartilage oligomeric matrix protein by Sox9, Sox5, and Sox6 transcription factors and CBP/p300 coactivators. Front Biosci 2007, 12:3899-3910.
13. Oh C.D., Maity S.N., Lu J.F., Zhang J., Liang S., Coustry F., et al. Identification of SOX9 interaction sites in the genome of chondrocytes. PLoS One 2010, 5. e10113.
14. Reginato A.M., Olsen B.R. The role of structural genes in the pathogenesis of osteoarthritic disorders. Arthritis Res 2002, 4:337-345.
15. Superti-Furga A., Unger S. Nosology and classification of genetic skeletal disorders: 2006 revision. Am J Med Genet A 2007, 143:1-18.
16. Rimoin D.L., Cohn D., Krakow D., Wilcox W., Lachman R.S., Alanay Y. The skeletal dysplasias: clinical-molecular correlations. Ann NY Acad Sci 2007, 1117:302-309.
17. Johannessen M.K., Skretting G., Ytrehus B., Roed K.H. Neonatal growth cartilage: equine tissue specific gene expression. Biochem Biophys Res Commun 2007, 354:975-980.
18. Funari V.A., Day A., Krakow D., Cohn Z.A., Chen Z., Nelson S.F., et al. Cartilage-selective genes identified in genome-scale analysis of non-cartilage and cartilage gene expression. BMC Genomics 2007, 8:165.
19. Wallace I.M., O'Sullivan O., Higgins D.G., Notredame C. M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res 2006, 34:1692-1699.
20. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
21. Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2007, 2:953-971.
22. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305:567-580.
23. Julenius K., Molgaard A., Gupta R., Brunak S. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 2005, 15:153-164.
24. Gupta R., Brunak S. Prediction of glycosylation across the human proteome and the correlation to protein function. Pac Symp Biocomput 2002, 310-322.
25. Blom N., Gammeltoft S., Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 1999, 294:1351-1362.
26. Säämänen A.K., Salminen H.J., Dean P.B., De Crombrugghe B., Vuorio E.I., Metsäranta M.P. Osteoarthritis-like lesions in transgenic mice harboring a small deletion mutation in type II collagen gene. Osteoarthritis Cartilage 2000, 8:248-257.
27. Uusitalo H., Hiltunen A., Ahonen M., Gao T.J., Lefebvre V., Harley V., et al. Accelerated up-regulation of L-Sox5, Sox6, and Sox9 by BMP-2 gene transfer during murine fracture healing. J Bone Miner Res 2001, 16:1837-1845.
28. Salminen H., Perälä M., Lorenzo P., Saxne T., Heinegård D., Säämänen A.M., et al. Up-regulation of cartilage oligomeric matrix protein at the onset of articular cartilage degeneration in a transgenic mouse model of osteoarthritis. Arthritis Rheum 2000, 43:1742-1748.
29. Takatalo M., Järvinen E., Laitinen S., Thesleff I., Rönnholm R. Expression of the novel Golgi protein GoPro49 is developmentally regulated during mesenchymal differentiation. Dev Dyn 2008, 237:2243-2255.
30. Sundvall M., Korhonen A., Paatero I., Gaudio E., Melino G., Croce C.M., et al. Isoform-specific monoubiquitination, endocytosis, and degradation of alternatively spliced ErbB4 isoforms. Proc Natl Acad Sci U S A 2008, 105:4162-4167.
31. Säämänen A.M., Tammi M., Kiviranta I., Jurvelin J., Helminen H.J. Levels of chondroitin-6-sulfate and nonaggregating proteoglycans at articular cartilage contact sites in the knees of young dogs subjected to moderate running exercise. Arthritis Rheum 1989, 32:1282-1292.
32. Salminen H., Vuorio E., Säämänen A.M. Expression of Sox9 and type IIA procollagen during attempted repair of articular cartilage damage in a transgenic mouse model of osteoarthritis. Arthritis Rheum 2001, 44:947-955.
33. Taipaleenmäki H., Suomi S., Hentunen T., Laitala-Leinonen T., Säämänen A.M. Impact of stromal cell composition on BMP-induced chondrogenic differentiation of mouse bone marrow derived mesenchymal cells. Exp Cell Res 2008, 314:2400-2410.
34. Mello M.A., Tuan R.S. High density micromass cultures of embryonic limb bud mesenchymal cells: an in vitro model of endochondral skeletal development. In Vitro Cell Dev Biol Anim 1999, 35:262-269.
35. Harkness L., Taipaleenmäki H., Mahmood A., Frandsen U., Säämänen A.M., Kassem M., et al. Isolation and differentiation of chondrocytic cells derived from human embryonic stem cells using dlk1/FA1 as a novel surface marker. Stem Cell Rev 2009, 5:353-368.
36. Rodriguez E., Roland S.K., Plaas A., Roughley P.J. The glycosaminoglycan attachment regions of human aggrecan. J Biol Chem 2006, 281:18444-18450.
37. Couchman J.R. Transmembrane signaling proteoglycans. Annu Rev Cell Dev Biol 2010, 26:89-114.
38. Choi Y., Chung H., Jung H., Couchman J.R., Oh E.S. Syndecans as cell surface receptors: unique structure equates with functional diversity. Matrix Biol 2010, 30:93-99.
39. Kohler J.J. Post-translational modifications: a shift for the O-GlcNAc paradigm. Nat Chem Biol 2010, 6:634-635.
40. Zhou Z., Apte S.S., Soininen R., Cao R., Baaklini G.Y., Rauser R.W., et al. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci USA 2000, 97:4052-4057.
41. Holmbeck K., Bianco P., Chrysovergis K., Yamada S., Birkedal-Hansen H. MT1-MMP-dependent, apoptotic remodeling of unmineralized cartilage: a critical process in skeletal growth. J Cell Biol 2003, 163:661-671.
42. Karaplis A.C., Luz A., Glowacki J., Bronson R.T., Tybulewicz V.L., Kronenberg H.M., et al. Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev 1994, 8:277-289.
43. Huang W., Chung U.I., Kronenberg H.M., de Crombrugghe B. The chondrogenic transcription factor Sox9 is a target of signaling by the parathyroid hormone-related peptide in the growth plate of endochondral bones. Proc Natl Acad Sci USA 2001, 98:160-165.
44. Huang W., Zhou X., Lefebvre V., de Crombrugghe B. Phosphorylation of SOX9 by cyclic AMP-dependent protein kinase A enhances SOX9's ability to transactivate a Col2a1 chondrocyte-specific enhancer. Mol Cell Biol 2000, 20:4149-4158.
45. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., de Crombrugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 2002, 16:2813-2828.
46. Mertin S., McDowall S.G., Harley V.R. The DNA-binding specificity of SOX9 and other SOX proteins. Nucleic Acids Res 1999, 27:1359-1364.