Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: II. Stimulation by bone morphogenetic protein-2 requires modulation of N-cadherin expression and function

Differentiation

Volumn 64, Issue 2, 1999, Pages 77-89

  Haas, Andrew R ^a   Tuan, Rocky S ^b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCIAN BLUE; BONE MORPHOGENETIC PROTEIN 2; CELL ADHESION MOLECULE; COLLAGEN TYPE 2; NERVE CELL ADHESION MOLECULE; PROTEOGLYCAN; SULFATE; SULFUR 35; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DENSITY; CELL DIFFERENTIATION; CHONDROGENESIS; MESENCHYME CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 0033024513     PISSN: 03014681     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-0436.1999.6420077.x     Document Type: Article

References (65)

1. Ahrens M, Ankenbauer T, Schroder D, Hollnagel A, Mayer H, Gross G (1993) Expression of human bone morphogenetic protein-2 or -4 in murine mesenchymal progenitor cells induces differentiation into distinct mesenchymal cell lineages. DNA Cell Biol 12:871-880
2. Ahrens PB, Solursh M, Reiters R (1977) Stage-related capacity for limb chondrogenesis in cell culture. Dev Biol 60:69-82
3. Aikawa T, Shirasuna K, Iwamoto M, Watatani K, Nakamura T, Okura M, Yoshioka H, Matsuya T (1996) Establishment of bone morphogenetic protein 2 responsive chondrogenic cell line. J Bone Min Res 11:544-552
4. Atkinson BL, Fantle KS, Benedict JJ, Huffer WE, Gutierrez-Hartman A (1997) Combination of osteoinductive bone proteins differentiates mesenchymal C3H10T1/2 cells specifically to the cartilage lineage. J Cell Biochem 65:325-329
5. Bassols A, Massague J (1988) Transforming growth factor-β regulates the expression and structure of extracellular matrix chondroitin/dermatan sulfate proteoglycans. J Biol Chem 263: 3039-3045
6. Blaschuk OW, Sullivan R, David S, Pouliot Y (1990) Identification of a cadherin cell recognition sequence. Dev Biol 139: 227-229
7. Brand-Saberi B, Gamel AJ, Krenn V, Muller TS, Wilting J, Christ B (1996) N-cadherin is involved in myoblast migration and muscle differentiation in the avian limb bud. Dev Biol 178:160-173
8. Carrington JL, Chen P, Yanagishita M, Reddi AH (1991) Osteogenin (bone morphogenetic protein-3) stimulates cartilage formation by chick limb bud cells in vitro. Dev Biol 146:406-415
9. Caterson B, Christner JE, Baker JR, Couchman JR (1985) Production and characterization of monoclonal antibodies directed against connective tissue proteoglycans. Fed Proc Am Soc Exp Biol 44:386-393
10. Centrella, M, Horowitz MC, Wozney JM, McCarthy TL (1994) Transforming growth factor-β gene family members and bone. Endocrine Rev 15:27-39
11. Chen P, Carrington JL, Hammonds RG, Reddi AH (1991) Stimulation of chondrogenesis in limb bud mesoderm cells by recombinant human bone morphogenetic protein 2B (BMP-26) and modulation by transforming growth factor β1 and β2. Exp Cell Res 195:509-515
12. D'Alessandro JS, Yetzaldape J, Wang EA (1994) Bone morphogenetic proteins induce differentiation in astrocyte lineage cells. Growth Factors 11:53-69
13. Danielson PE, Forss-Petter S, Brow MA, Calavetta L, Douglass J, Milner RJ, Sutcliffe JG (1988) p1B15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA 7:261-267
14. Denker AE, Nicoll SB, Tuan RS (1995) Formation of cartilage-like spheroids by micromass cultures of murine C3H10T1/2 cells upon treatment with transforming growth factor-β1. Differentiation 59:25-34
15. Dessau W, von der Mark K, Fischer S (1980) Changes in the patterns of collagens and fibronectin during limb bud chondrogenesis. J Embryol Exp Morphol 57:51-60
16. Duprez DM, Coltey M, Amthor H, Brickell PM, Tickle C (1996) Bone morphogenetic protein-2 (BMP-2) inhibits muscle development and promotes cartilage formation in chick limb bud cultures. Dev Biol 174:448-452
17. Einheber S, Hannocks M-J, Metz CN, Rifkin DB, Salzer JL (1995) Transforming growth factor-β1 regulates axon/Schwann cell interactions. J Cell Biol 129:443-458
18. Elima K, Vuorio T, Vuorio E (1987) Determination of the single polyadenylation site of the human proα1(II) collagen gene. Nucleic Acids Res 15:9499-9504
19. Fagotto F, Funayama N, Gluck U, Gumbiner BM (1996) Binding to cadherins antagonizes the signaling activity of β-catenin during axis formation in Xenopus. J Cell Biol 132:1105-1114
20. Frenzel EM, Johnson RG (1996) Gap junction formation between cultured embryonic lens cells is inhibited by antibody to N-cadherin. Dev Biol 179:1-16
21. Fujimori T, Takeichi M (1993) Disruption of epithelial cell-cell adhesion by exogenous expression of a mutated nonfunctional N-cadherin. Mol Biol Cell 4:37-47
22. Gawande SR Tuan RS (1990) Characterization of bone-derived chondrogenesis-stimulating activity on embryonic limb mesenchymal cells in vitro. Cell Tissue Kinet 23:375-390
23. Gehris AL, Oberlender SA, Shepley KJ, Tuan RS, Bennett VD (1996) Fibronectin mRNA alternative splicing is temporally and spatially regulated during chondrogenesis in vivo and in vitro. Dev Dyn 206:219-230
24. Gumbiner BM (1996) Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 84:345-357
25. Heasman J, Crawford A, Goldstone K, Garner-Hamrick P, Gumbiner B, McCrea P, Kintner C, Noro CY, Wylie C (1994) Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79:791-803
26. Hogan BLM (1996) Bone morphogenetic proteins in development. Current Biol. 6:432-438
27. Holmdahl R, Rubin K, Klareskog L, Larsson E, Wigzell H (1986) Characterization of the antibody response in mice with type II collagen-induced arthritis using monoclonal anti-type II collagen antibodies. Arthr Rheum 29:400-410
28. Jiang TX, Yi JR, Ying SY, Chuong CM (1993) Activin enhances chondrogenesis of limb bud cells: stimulation of precartilaginous mesenchymal condensations and expression of N-CAM. Dev Biol 155:545-557
29. Katagiri T, Yamaguchi A, Ikeda T, Yoshiki S, Wozney JM, Rosen V, Wang EA, Tanaka H, Omura S, Suda T (1990) The non-osteogenic mouse pluripotent cell line, C3H10T1/2, is induced to differentiate into osteoblastic cells by recombinant human bone morphogenetic protein-2. Biochem Biophys Res Commun 172:295-299
30. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Ikeda T, Rosen V, Wozney JM, Fujisawa-Sehara A, Suda T (1994) Bone morphogenetic protein-2 converts the differentiation pathway of C212 myoblasts into the osteoblast lineage. J Cell Sci 127:1755-1766
31. Kintner C (1992) Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain. Cell 69:225-236
32. Knudsen CB, Toole BP (1985) Changes in the pericellular matrix during differentiation of limb bud mesoderm. Dev Biol 112:308-318
33. Kulyk WM, Rodgers BJ, Greer K, Kosher RA (1989) Promotion of embryonic chick limb cartilage differentiation by transforming growth factor-β. Dev Biol 135:424-430
34. Larue L, Antos C, Butz S, Huber O, Delmas V, Dominis M, Kemler R (1996) A role for cadherins in tissue formation. Development 122:3185-3194
35. Leonard CM, Fuld HM, Frenz DA, Downie SA, Massague J, Newman SA (1991) Role of transforming growth factor-β in chondrogenic pattern formation in the embryonic limb: stimulation of mesenchymal condensation and fibronectin gene expression by exogenous TGF-β and evidence for endogenous TGF-β-like activity. Dev Biol 145:99-109
36. Lyons KM, Pelton RW, Hogan BLM (1990) Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for bone morphogenetic protein-2A (BMP-2A). Development 109:833-844
37. Mackie EJ, Thesleff I, Chiquet-Ehrismann R (1987) Tenascin is associated with chondrogenic and osteogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol 105:2569-2579
38. Miyatani S, Shimamura K, Hatta M, Nagafuchi A, Nose A, Matsunaga M, Hatta K, Takeichi M. (1989) Neural cadherin: Role in selective cell-cell adhesion. Science 245:631-635
39. Nagafuchi A, Tsukita S, Takeichi M (1993) Transmembrane control of cadherin-mediated cell-cell adhesion. Sem Cell Biol 4:175-181
40. Nakase T, Nomura S, Yoshikawa H, Hashimoto J, Hirota S, Kitamura Y, Oikawa S, Ono K, Takaoka K (1994) Transient and localized expression of bone morphogenetic protein 4 messenger RNA during fracture healing. J Bone Min Res 9:651-659
41. Oberlender SA, Tuan RS (1994a) Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis. Development 120:177-187
42. Oberlender SA, Tuan RS (1994b) Spatiotemporal profile of N-cadherin in the developing limb mesenchyme. Cell Adhes and Commun 2:521-537
43. Peralta Soler A, Knudsen KA, Jaurand MC, Johnson KR, Wheelock MJ, Klein-Szanto AJ, Salazar H (1995) The differential expression of N-cadherin and E-cadherin distinguishes pleural mesotheliomas from lung adenocarcinomas. Hum Path 26:1363-1369
44. Rickard DJ, Sullivan TA, Shenker BJ, Leboy PS, Kazhdan I (1994) Induction of rapid osteoblast differentiation in rat bone marrow stromal cell cultures by dexamethasone and BMP-2. Dev Biol 161:218-228
45. Roark EF, Greer K (1994) Transforming growth factor-β and bone morphogenetic protein-2 act by distinct mechanisms to promote chick limb cartilage differentiation in vitro. Dev Dyn 200:103-116
46. Rosen V, Noue J, Song JJ, Thies RS, Cox K, Wozney JM (1994) Responsiveness of clonal limb bud cell lines to bone morphogenetic protein 2 reveals a sequential relationship between cartilage and bone cell phenotypes. J Bone Min Res 9: 1759-1768
47. Roubin R, Hermine DB, Hirsch MR, Christo G (1990) Modulation of N-CAM expression by transforming growth factor-β, serum, and autocrine factors. J Cell Biol 111:673-683
48. San Antonio JD, Tuan RS (1986) Chondrogenesis of limb bud mesenchyme in vitro: stimulation by cations. Dev Biol 115: 313-324
49. Shapiro L, Fannon AM, Kwong PD, A. Thompson A, Lehmann MS, Grubel G, Legrand J-F, Als-Nielsen J, Colman DR, Hendrickson WA (1995) Structural basis of cell-cell adhesion by cadherins. Nature 374:327-337
50. Steinberg MS, Takeichi M (1994) Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc Natl Acad Sci USA 91:206-209
51. Stringa E, Tuan RS (1996) Chondrogenic cell subpopulation of chick embryonic calvarium: isolation by peanut agglutinin affinity chromatography and in vitro characterization. Anat Embryol 194:427-437
52. Swalla BJ, Upholt WB, Solursh M (1988) Analysis of type II collagen RNA localization in chick wing buds by in situ hybridization. Dev Biol 125:51-58
53. Takeichi M (1995) Morphogenetic role of classic cadherins. Curr Opin Cell Biol 7:619-627
54. Tavella S, P. Raffo P, Tacchetti C, Ranieri C, Castagnola P (1994) N-CAM and N-cadherin expression during in vitro chondrogenesis. Exp Cell Res 215:354-362
55. Taylor SM, Jones PA (1979) Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 17: 771-779
56. Thies RS, Bauduy M, Ashton BA, Kurtzberg L, Wozney JM, Rosen V (1992) Recombinant human bone morphogenetic protein-2 induces osteoblastic differentation in W-20-17 stromal cells. Endocrinology 130:1318-1324
57. Toole B (1972) Hyaluronate turnover during chondrogenesis in the developing chick limb and axial skeleton. Dev Biol 29: 321-329
58. Torres MA, Yang-Snyder, JA, Purcell SM, DeMarais AA, McGrew LL, Moon RT (1996) Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5a class and by a dominant negative cadherin in early Xenopus development. J Cell Biol 133:1123-1137
59. 3 or TGF-β1. Exp Cell Res 213:433-437
60. Tyndall WA, Tuan RS (1995) Involvement of N-cadherin mediated cell adhesion in TGF-β1/BMP-2 stimulation of limb mesenchymal chondrogenesis. Trans Orthop Res 20:75
61. Wang EA, Israel DI, Kelly S, Luxenberg DP (1993) Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells. Growth Factors 9:57-71
62. Widelitz RB, Jiang T-X, Murray BA, Chuong C-M (1993) Adhesion molecules in skeletogenesis II: Neural cell adhesion molecules mediate precartilaginous mesenchyme condensations and enhance chondrogenesis. J Cell Physiol 156:399-411
63. Wong M, Tuan RS (1995) Interactive cellular modulation of chondrogenic differentiation in vitro by subpopulations of chick embryonic calvarial cells. Dev Biol 167:130-147
64. Yamaguchi A, Katagiri T, Ikeda T, Wozney JM, Rosen V, Wang EA, Kahn AJ, Suda T, Yoshiki S (1991) Recombinant human BMP-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J Cell Biol 113:681-687
65. Zanetti NC, Solursh M (1984) Induction of chondrogenesis in limb mesenchymal cultures by disruption of the actin cytoskeleton. J Cell Biol 99:115-123