Transforming growth factor-β1 (TGF-β1) regulates ATDC5 chondrogenic differentiation and fibronectin isoform expression

Journal of Cellular Biochemistry

Volumn 95, Issue 4, 2005, Pages 750-762

  Han, Fei ^a   Adams, Christopher S ^a   Tao, Zhuliang ^a   Williams, Charlene J ^a,b   Zaka, Raihana ^a   Tuan, Rocky S ^c   Norton, Pamela A ^b   Hickok, Noreen J ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

Alcian blue; Alternative splicing; Collagen type I; Collagen type II; Fibronectin; TGF 1

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 2; FIBRONECTIN; ISOPROTEIN; PROTEOGLYCAN; PROTEOGLYCAN SULFATE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; MESSENGER RNA; SULFATE; TGFB1 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL FATE; CHONDROGENESIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE TIME EFFECT RELATION; EXON; MESENCHYME; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOGLYCAN SYNTHESIS; STAINING; TERATOMA; ALTERNATIVE RNA SPLICING; ANIMAL; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; TIME; TUMOR CELL LINE;

ANIMALIA;

ALTERNATIVE SPLICING; ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CHONDROGENESIS; COLLAGEN TYPE I; COLLAGEN TYPE II; EXONS; FIBRONECTINS; GENE EXPRESSION REGULATION; MICE; PROTEIN ISOFORMS; PROTEOGLYCANS; RNA, MESSENGER; SULFATES; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 24744456615     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.20427     Document Type: Article

References (49)

1. Asahina I, Sampath TK, Hauschka PV. 1996. Human osteogenic protein-1 induces chondroblastic, osteoblastic, and/or adipocytic differentiation of clonal murine target cells. Exp Cell Res 222:38-47.
2. Atsumi T, Miwa Y, Kimata K, Ikawa Y. 1990. A chondrogenic cell line derived from a differentiating culture of AT805 teratocarcinoma cells. Cell Diff Develop 30:109-116.
3. Balza E, Borsi L, Allemanni G, Zardi L. 1988. Transforming growth factor beta regulates the levels of different fibronectin isoforms in normal human cultured fibroblasts. FEBS Lett 228:42-44.
4. Bennett VD, Pallante KM, Adams SL. 1991. The splicing pattern of fibronectin mRNA changes during chondrogenesis resulting in an unusual form of the mRNA in cartilage. J Biol Chem 266:5918-5924.
5. Benya PD, Padilla SR. 1993. Dihydrocytochalasin B enhances transforming growth factor-beta-induced reexpression of the differentiated chondrocyte phenotype without stimulation of collagen synthesis. Exp Cell Res 204:268-277.
6. Borsi L, Balza E, Allemanni G, Zardi L. 1992. Differential expression of the fibronectin isoform containing the ED-B oncofetal domain in normal human fibroblast cell lines originating from different tissues. Exp Cell Res 199: 98-105.
7. Burger A, Wagner C, Viedt C, Reis B, Hug F, Hansch GM. 1998. Fibronectin synthesis by human tubular epithelial cells in culture: Effects of PDGF and TGF-beta on synthesis and splicing. Kidney Int 54:407-415.
8. Burton-Wurster N, Lust G, Macleod JN. 1997. Cartilage fibronectin isoforms: In search of functions for a special population of matrix glycoproteins. Matrix Biol 15:441-454.
9. Cassiede P, Dennis JE, Ma F, Caplan AI. 1996. Osteochondrogenic potential of marrow mesenchymal progenitor cells exposed to TGF-beta 1 or PDGF-BB as assayed in vivo and in vitro. J Bone Min Res 11:1264-1273.
10. Chen W, Culp LA. 1998. Adhesion to fibronectin's EDB domain induces tyrosine phosphorylation of focal adhesion proteins in Balb/c 3T3 cells. Clin Exp Metastasis 16:30-42.
11. Colman-Lerner A, Fischman ML, Lanuza GM, Bissell DM, Kornblihtt AR, Baranao JL. 1999. Evidence for a role of the alternatively spliced ED-I sequence of fibronectin during ovarian follicular development. Endocrinology 140:2541-2548.
12. ffrench-Constant C. 1995. Alternative splicing of fibronectin-many different proteins but few different functions. Exp Cell Res 221:261-271.
13. Fukuda T, Yoshida N, Kataoka H, Manabe R, Mizuno-Horikawa Y, Sato M, Kuriyama K, Yasui N, Sekiguchi K. 2002. Mice lacking the EDB segment of fibronectin develop normally but exhibit reduced cell growth and fibronectin matrix assembly in vitro. Cancer Res 62: 5603-5610.
14. Gehris AL, Brandli DW, Lewis SD, Bennett VD. 1996a. The exon encoding the fibronectin type III-9 repeat is constitutively included in the mRNA from chick limb mesenchyme and cartilage. Biochimica et Biophysica Acta 1311:5-12.
15. Gehris AL, Oberlender SA, Shepley KJ, Tuan RS, Bennett VD. 1996b. Fibronectin mRNA alternative splicing is temporally and spatially regulated during chondrogenesis in vivo and in vitro. Dev Dyn 206:219-230.
16. Guan JL, Trevithick JE, Hynes RO. 1990. Retroviral expression of alternatively spliced forms of rat fibronectin. J Cell Biol 110:833-847.
17. Hashimoto-Uoshima M, Yan YZ, Schneider G, Aukhil I. 1997. The alternatively spliced domains EIIIB and EIIIA of human fibronectin affect cell adhesion and spreading. J Cell Sci 110:2271-2280.
18. Hickok NJ, Haas AR, Tuan RS. 1998. Regulation of chondrocyte differentiation and maturation. Microsc Res Tech 43:174-190.
19. Hocevar BA, Brown TL, Howe PH. 1999. TGF-beta induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. EMBO J 18: 1345-1356.
20. Inoue T, Nabeshima K, Shimao Y, Kataoka H, Koono M. 1998. Cell density-dependent regulation of fibronectin splicing at the EDA region in fibroblasts: Cell density also modulates the responses of fibroblasts to TGF-beta and cancer cell-conditioned medium. Cancer Lett 129: 45-54.
21. Inoue T, Nabeshima K, Shimao Y, Koono M. 1999. Hepatocyte growth Factor/Scatter factor (HGF/SF) is a regulator of fibronectin splicing in MDCK cells: Comparison between the effects of HGF/SF and TGF-beta1 on fibronectin splicing at the EDA region. Biochem Biophys Res Commun 260:225-231.
22. Kawai J, Akiyama H, Shigeno C, Ito H, Konishi J, Nakamura T. 1999. Effects of transforming growth factor-beta signaling on chondrogenesis in mouse chondrogenic EC cells, ATDC5. Eur J Cell Biol 78:707-714.
23. Kornblihtt AR, Umezawa K, Vibe-Pedersen K, Baralle FE. 1985. Primary structure of human fibronectin: Differential splicing may generate at least 10 polypeptides from a single gene. EMBO J 4:1755-1759.
24. Kuo BA, Uporova TM, Liang H, Bennett VD, Tuan RS, Norton PA. 2002. Alternative splicing during chondrogenesis: Modulation of fibronectin exon EIIIA splicing by SR proteins. J Cell Biochem 86:45-55.
25. Loty S, Forest N, Boulekbache H, Sautier J-M. 1995. Cytochalasin D induces changes in cell shape and promotes in vitro chondrogenesis: A morphological study. Biol Cell 83:149-161.
26. Lust G, Burton-Wurster N, Leipold H, Steinmeyer J, Todhunter R. 1991. Modulation of fibronectin and proteoglycan synthesis by chondrocytes. Scand J Rheumatol Suppl 27:58-59.
27. MacLeod JN, Burton-Wurster N, Gu DN, Lust G. 1996. Fibronectin mRNA splice variant in articular cartilage lacks bases encoding the V, III-15, and I-10 protein segments. J Biol Chem 271:18954-18960.
28. Magnuson VL, Young M, Schattenberg DG, Mancini MA, Chen DL, Steffensen B, Klebe RJ. 1991. The alternative splicing of fibronectin pre-mRNA is altered during aging and in response to growth factors. J Biol Chem 266: 14654-14662.
29. Manabe R, Ohe N, Maeda T, Fukuda T, Sekiguchi K. 1997. Modulation of cell-adhesive activity of fibronectin by the alternatively spliced EDA segment. J Cell Biol 139:295-307.
30. Manabe R, Ohe N, Sekiguchi K. 1999. Alternatively spliced EDA segment regulates fibronectin-dependent cell cycle progression and mitogenic signal transduction. J Biol Chem 274:5919-5924.
31. Muro AF, Chauhan AK, Gajovic S, Iaconcig A, Porro F, Stanta G, Baralle FE. 2003. Regulated splicing of the fibronectin EDA exon is essential for proper skin wound healing and normal lifespan. J Cell Biol 162:149-160.
32. Nakayama N, Duryea D, Manoukian R, Chow G, Han CY. 2003. Macroscopic cartilage formation with embryonic stem-cell-derived mesodermal progenitor cells. J Cell Sci 116:2015-2028.
33. Norton PA, Hynes RO. 1987. Alternative splicing of chicken fibronectin in embryos and in normal and transformed cells. Mol Cell Biol 7:4297-4307.
34. Palmer G, Guicheux J, Bonjour JP, Caverzasio J. 2000. Transforming growth factor-beta stimulates inorganic phosphate transport and expression of the type III phosphate transporter Glvr-1 in chondrogenic ATDC5 cells. Endocrinology 141:2236-2243.
35. Paul-JI, Schwarzbauer JE, Tamkun JW, Hynes RO. 1986. Cell-type-specific fibronectin subunits generated by alternative splicing. J Biol Chem 261:12258-12265.
36. Peters JH, Hynes RO. 1996. Fibronectin isoform distribution in the mouse. I. The alternatively spliced EIIIB, EIIIA, and V segments show widespread codistribution in the developing mouse embryo. Cell Adhes Commun 4:103-125.
37. Schwarzbauer JE, Tamkun JW, Lemischka IR, Hynes RO. 1983. Three different fibronectin mRNAs arise by alternative splicing within the coding region. Cell 35:421-431.
38. Schwarzbauer JE, Patel RS, Fonda D, Hynes RO. 1987. Multiple sites of alternative splicing of the rat fibronectin gene transcript. EMBO J 6:2573-2580.
39. Shukunami C, Shigeno C, Atsumi T, Ishizeki K, Suzuki F, Hiraki Y. 1996. Chondrogenic differentiation of clonal mouse embryonic cell line ATDC5 in vitro: Differentiation-dependent gene expression of parathyroid hormone (PTH)/PTH-related peptide receptor. J Cell Biol 133: 457-468.
40. Shukunami C, Ohta Y, Sakuda M, Hiraki Y. 1998. Sequential progression of the differentiation program by bone morphogenetic protein-2 in chondrogenic cell line ATDC5. Exp Cell Res 241:1-11.
41. Siebler T, Robson H, Shalet SM, Williams GR. 2002. Dexamethasone inhibits and thyroid hormone promotes differentiation of mouse chondrogenic ATDC5 cells. Bone 31:457-464.
42. Tan MH, Sun Z, Opitz SL, Schmidt TE, Peters JH, George EL. 2004. Deletion of the alternatively spliced fibronectin EIIIA domain in mice reduces atherosclerosis. Blood 104: 11-18.
43. Tuli R, Tuli S, Nandi S, Huang X, Manner PA, Hozack WJ, Danielson KG, Hall DJ, Tuan RS. 2003. Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves N-cadherin and mitogen-activated protein kinase and Wnt signaling cross-talk. J Biol Chem 278:41227-41236.
44. Viedt C, Burger A, Hansch GM. 1995. Fibronectin synthesis in tubular epithelial cells: Up-regulation of the EDA splice variant by transforming growth factor beta. Kidney Int 48:1810-1817.
45. Wang A, Cohen DS, Palmer E, Sheppard D. 1991. Polarized regulation of fibronectin secretion and alternative splicing by transforming growth factor. J Biol Chem 266: 15598-15601.
46. White DG, Hershey HP, Moss JJ, Daniels H, Tuan RS, Bennett VD. 2003. Functional analysis of fibronectin isoforms in chondrogenesis: Full-length recombinant mesenchymal fibronectin reduces spreading and promotes condensation and chondrogenesis of limb mesenchymal cells. Differentiation 71:251-261.
47. Worster AA, Brower-Toland BD, Fortier LA, Bent SJ, Williams J, Nixon AJ. 2001. Chondrocytic differentiation of mesenchymal stem cells sequentially exposed to transforming growth factor-beta1 in monolayer and insulin-like growth factor-I in a three-dimensional matrix. J Orthop Res 19:738-749.
48. Wu LN, Genge BR, Ishikawa Y, Wuthier RE. 1992. Modulation of cultured chicken growth plate chondrocytes by transforming growth factor-beta 1 and basic fibroblast growth factor. J Cell Biochem 49:181-198.
49. Zhang DW, Burton-Wurster N, Lust G. 1995. Alternative splicing of ED-A and ED-B sequences of fibronectin pre-mRNA differs in chondrocytes from different cartilaginous tissues and can be modulated by biological factors. J Biol Chem 270:1817-1822.