Altered signaling in the G1 phase deregulates chondrocyte growth in a mouse model with proteoglycan undersulfation

Journal of Cellular Biochemistry

Volumn 115, Issue 10, 2014, Pages 1779-1786

  De Leonardis, Fabio ^a   Monti, Luca ^a   Gualeni, Benedetta ^a   Tenni, Ruggero ^a   Forlino, Antonella ^a   Rossi, Antonio ^a  

^a UNIVERSITY OF PAVIA   (Italy)

Author keywords

CELL CYCLE; GROWTH PLATE; PROTEOGLYCAN SULFATION; SKELETAL DYSPLASIA; WNT PATHWAY

Indexed keywords

BETA CATENIN; CYCLIN D1; PROTEIN P130; PROTEOCHONDROITIN SULFATE; PROTEOGLYCAN; SMAD3 PROTEIN; TRANSCRIPTION FACTOR; IHH PROTEIN, MOUSE; RBL2 PROTEIN, MOUSE; SMAD3 PROTEIN, MOUSE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DYSPLASIA; BONE GROWTH; CARTILAGE; CARTILAGE CELL; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DNA REPLICATION; GROWTH PLATE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SULFATION; UPREGULATION; WESTERN BLOTTING; WNT SIGNALING PATHWAY; ANIMAL; ANTAGONISTS AND INHIBITORS; ARTICULAR CARTILAGE; BIOSYNTHESIS; BONE; BONE DEVELOPMENT; BONE DISEASE; C57BL MOUSE; CELL DIFFERENTIATION; CELL PROLIFERATION; EXTRACELLULAR MATRIX; GENE TARGETING; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; BONE AND BONES; BONE DEVELOPMENT; BONE DISEASES; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROCYTES; CHONDROITIN SULFATE PROTEOGLYCANS; CYCLIN D1; E2F TRANSCRIPTION FACTORS; EXTRACELLULAR MATRIX; G1 PHASE; GENE KNOCK-IN TECHNIQUES; GROWTH PLATE; HEDGEHOG PROTEINS; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; RETINOBLASTOMA-LIKE PROTEIN P130; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; WNT SIGNALING PATHWAY;

EID: 84906098667     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24844     Document Type: Article

References (33)

1. Beier F,. 2005. Cell-cycle control and the cartilage growth plate. J Cell Physiol 202: 1-8.
2. Brochhausen C, Lehmann M, Halstenberg S, Meurer A, Klaus G, Kirkpatrick CJ,. 2009. Signalling molecules and growth factors for tissue engineering of cartilage-what can we learn from the growth plate? J Tissue Eng Regen Med 3: 416-429.
3. Burdan F, Szumilo J, Korobowicz A, Farooquee R, Patel S, Patel A, Dave A, Szumilo M, Solecki M, Klepacz R, Dudka J,. 2009. Morphology and physiology of the epiphyseal growth plate. Folia Histochem Cytobiol 47: 5-16.
4. Chun JS, Oh H, Yang S, Park M,. 2008. Wnt signaling in cartilage development and degeneration. BMB Rep 41: 485-494.
5. Cobrinik D,. 2005. Pocket proteins and cell cycle control. Oncogene 24: 2796-2809.
6. Cobrinik D, Lee MH, Hannon G, Mulligan G, Bronson RT, Dyson N, Harlow E, Beach D, Weinberg RA, Jacks T,. 1996. Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev 10: 1633-1644.
7. Cortes M, Baria AT, Schwartz NB,. 2009. Sulfation of chondroitin sulfate proteoglycans is necessary for proper Indian hedgehog signaling in the developing growth plate. Development 136: 1697-1706.
8. Dailey L, Laplantine E, Priore R, Basilico C,. 2003. A network of transcriptional and signaling events is activated by FGF to induce chondrocyte growth arrest and differentiation. J Cell Biol 161: 1053-1066.
9. Forlino A, Piazza R, Tiveron C, Della Torre S, Tatangelo L, Bonafe L, Gualeni B, Romano A, Pecora F, Superti-Furga A, Cetta G, Rossi A,. 2005. A diastrophic dysplasia sulfate transporter (SLC26A2) mutant mouse: Morphological and biochemical characterization of the resulting chondrodysplasia phenotype. Hum Mol Genet 14: 859-871.
10. Fu M, Wang C, Li Z, Sakamaki T, Pestell RG,. 2004. Minireview: Cyclin D1: Normal and abnormal functions. Endocrinology 145: 5439-5447.
11. Goentoro L, Kirschner MW,. 2009. Evidence that fold-change, and not absolute level, of beta-catenin dictates Wnt signaling. Mol Cell 36: 872-884.
12. Gu W, Wells AL, Pan F, Singer RH,. 2008. Feedback regulation between zipcode binding protein 1 and beta-catenin mRNAs in breast cancer cells. Mol Cell Biol 28: 4963-4974.
13. Gualeni B, Facchini M, De Leonardis F, Tenni R, Cetta G, Viola M, Passi A, Superti-Furga A, Forlino A, Rossi A,. 2010. Defective proteoglycan sulfation of the growth plate zones causes reduced chondrocyte proliferation via an altered Indian hedgehog signalling. Matrix Biol 29: 453-460.
14. Guo X, Wang XF,. 2009. Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res 19: 71-88.
15. Ito K, Maruyama Z, Sakai A, Izumi S, Moriishi T, Yoshida CA, Miyazaki T, Komori H, Takada K, Kawaguchi H, Komori T,. 2014. Overexpression of Cdk6 and Ccnd1 in chondrocytes inhibited chondrocyte maturation and caused p53-dependent apoptosis without enhancing proliferation. Oncogene 33: 1862-1871.
16. Karsenty G, Wagner EF,. 2002. Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2: 389-406.
17. Kronenberg HM,. 2006. PTHrP and skeletal development. Ann N Y Acad Sci 1068: 1-13.
18. Laplantine E, Rossi F, Sahni M, Basilico C, Cobrinik D,. 2002. FGF signaling targets the pRb-related p107 and p130 proteins to induce chondrocyte growth arrest. J Cell Biol 158: 741-750.
19. Li TF, Chen D, Wu Q, Chen M, Sheu TJ, Schwarz EM, Drissi H, Zuscik M, O'Keefe RJ,. 2006. Transforming growth factor-beta stimulates cyclin D1 expression through activation of beta-catenin signaling in chondrocytes. J Biol Chem 281: 21296-21304.
20. Long F, Zhang XM, Karp S, Yang Y, McMahon AP,. 2001. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 128: 5099-5108.
21. MacDonald BT, Tamai K, He X,. 2009. Wnt/beta-catenin signaling: Components, mechanisms, and diseases. Dev Cell 17: 9-26.
22. Mertz EL, Facchini M, Pham AT, Gualeni B, De Leonardis F, Rossi A, Forlino A,. 2012. Matrix disruptions, growth, and degradation of cartilage with impaired sulfation. J Biol Chem 287: 22030-22042.
23. Ornitz DM, Marie PJ,. 2002. FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev 16: 1446-1465.
24. Rossi A, Kaitila I, Wilcox WR, Rimoin DL, Steinmann B, Cetta G, Superti-Furga A,. 1998. 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 17: 361-369.
25. Schibler L, Gibbs L, Benoist-Lasselin C, Decraene C, Martinovic J, Loget P, Delezoide AL, Gonzales M, Munnich A, Jais JP, Legeai-Mallet L,. 2009. New insight on FGFR3-related chondrodysplasias molecular physiopathology revealed by human chondrocyte gene expression profiling. PLoS ONE 4: e7633.
26. Schwartz NB, Domowicz M,. 2002. Chondrodysplasias due to proteoglycan defects. Glycobiology: 12: 57R-68R.
27. van der Eerden BC, Karperien M, Wit JM,. 2003. Systemic and local regulation of the growth plate. Endocr Rev 24: 782-801.
28. Vigo E, Muller H, Prosperini E, Hateboer G, Cartwright P, Moroni MC, Helin K,. 1999. CDC25A phosphatase is a target of E2F and is required for efficient E2F-induced S phase. Mol Cell Biol 19: 6379-6395.
29. Warman ML, Cormier-Daire V, Hall C, Krakow D, Lachman R, LeMerrer M, Mortier G, Mundlos S, Nishimura G, Rimoin DL, Robertson S, Savarirayan R, Sillence D, Spranger J, Unger S, Zabel B, Superti-Furga A,. 2010. Nosology and classification of genetic skeletal disorders: Revision. Am J Med Genet A 155A: 943-968.
30. Wells J, Boyd KE, Fry CJ, Bartley SM, Farnham PJ,. 2000. Target gene specificity of E2F and pocket protein family members in living cells. Mol Cell Biol 20: 5797-5807.
31. Yang Y, Topol L, Lee H, Wu J,. 2003. Wnt5a and Wnt5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation. Development 130: 1003-1015.
32. Yoon BS, Lyons KM,. 2004. Multiple functions of BMPs in chondrogenesis. J Cell Biochem 93: 93-103.
33. Zhang M, Wang M, Tan X, Li TF, Zhang YE, Chen D,. 2010. Smad3 prevents beta-catenin degradation and facilitates beta-catenin nuclear translocation in chondrocytes. J Biol Chem 285: 8703-8710.