Successive formative stages of precartilaginous mesenchymal condensations in vitro: Modulation of cell adhesion by Wnt-7a and BMP-2

Journal of Cellular Physiology

Volumn 180, Issue 3, 1999, Pages 314-324

  Stott, N Susan ^a,b   Jiang, T X ^a   Chuong, Cheng Ming ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; DESMIN; FIBRONECTIN; INTEGRIN; NERVE CELL ADHESION MOLECULE; TENASCIN;

ARTICLE; CARTILAGE CELL; CELL ADHESION; CELL AGGREGATION; CELL DIFFERENTIATION; CHONDROGENESIS; CONTROLLED STUDY; DNA CONTENT; EMBRYO; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; LIMB BUD; MESENCHYME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; AVIAN PROTEINS; BONE MORPHOGENETIC PROTEINS; CARTILAGE; CELL ADHESION; CELL ADHESION MOLECULES; CHICK EMBRYO; CHONDROGENESIS; CULTURE TECHNIQUES; EXTREMITIES; MESODERM; PROTO-ONCOGENE PROTEINS; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEINS;

EID: 0032805495     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199909)180:3<314::AID-JCP2>3.0.CO;2-Y     Document Type: Article

References (66)

1. Ahrens PB, Solursh M, Reiter RS. 1977. Stage related capacity for limb chondrogenesis in cell culture. Dev Biol 60:69-82.
2. Akita K, Francis-West P, Vargesson N. 1996. The ectodermal control in chicken limb development: Wnt-7a, Shh, Bmp-2 and Bmp-4 expression and the effect of FGF-4 on gene expression. Mech Dev 60:127-137.
3. Caplan AI. 1991. Mesenchymal stem cells. J Orthop Res 9:641-650.
4. Carrington JL, Chen P, Yanagashita M, Reddi AH. 1991. Osteogenin (bone morphogenetic protein-3) stimulates cartilage formation by chick limb bud cells in vitro. Dev Biol 146:406-415.
5. Chen P, Carrington JL, Hammonds G, Reddi AH. 1991. Stimulation of chondrogenesis in limb bud mesoderm cells by recombinant human bone morphogenetic protein 2B (BMP-2B) and modulation by transforming growth factor beta 1 and beta 2. Exp Cell Res 195:509-515.
6. Chen Q, Johnson DM, Haudenschild DR, Goetinck PF. 1995. Progression and recapitulation of the chondrocyte differentiation program: cartilage matrix protein is a marker for chondrocyte maturation. Dev Biol 172:293-306.
7. Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakakura T. 1986. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47:131-139.
8. Chiquet-Ehrismann R, Hagios C, Schenk S. 1995. The complexity in regulating the expression of tenascins. Bioessays 17:873-878.
9. Christ B, Jacob HJ, Jacob M, Brand B. 1986. Principles of hand ontogenesis in man. Acta Morphol Nerl Scand 24:249-268.
10. Chuong CM, Edelman GM. 1985. Expression of cell-adhesion molecules in embryonic induction. I. Morphogenesis of nestling feathers. J Cell Biol 101:1009-1026.
11. Chuong CM, Widelitz RB, Jiang TX, Abbott UK, Lee YS, Chen HM. 1993. Roles of Adhesion molecules NCAM and tenascin in limb skeletogenesis: analysis with antibody perturbation, exogenous gene expression, talpid mutants and activin stimulation. Prog Clin Biol Res 383:465-474.
12. Chuong CM, Widelitz RB, Ting-Berreth S, Jiang TX. 1996. Early events during skin apednage regenerations: dependence on epithelial-mesenchymal interaction and order of molecular reappearance. J Invest Dermatol 107:639-646.
13. Danto SI, Fischman DA. 1984. Immunocytochemical analysis of intermediate filaments in embryonic heart cells with monoclonal antibodies to desmin. J Cell Biol 98:2179-2191.
14. Dealy CN, Roth A, Ferrari D, Brown AM, Kosher RA. 1993. Wnt-5a and Wnt-7a are expressed in the developing chick limb bud in a manner suggesting roles in pattern formation along the proximodistal and dorsoventral axes. Mech Dev 43:175-186.
15. DeLuca S, Heinegard D, Hascall VC, Kimura JH, Caplan AI. 1977. Chemical and physical changes in proteoglycans during development of chick limb bud chondrocytes grown in vivo. J Biol Chem 252:6600-6608.
16. Dessau W, von der Mark H, 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.
17. Downie SA, Newman SA. 1994. Morphogenetic differences between fore and hind limb precartilaginous mesenchyme: relationship to mechanisms of skeletal pattern formation. Dev Biol 162:195-208.
18. Duprez D, Bell EJ de H, Richardson MK, Archer CW, Wolpert L, Brickell PM, Francis-West PH. 1996a. Overexpression of BMP-2 and BMP-4 alters the size and shape of developing skeletal elements in the chick limb. Mech Dev 57:145-147.
19. Duprez DM, Coltey M, Amthor H, Brickell PM, Tickle C. 1996b. Bone morphogenetic protein-2 (BMP-2) inhibits muscle development and promotes cartilage formation in chick limb bud cultures. Dev Biol 174:448-452.
20. Frenz DA, Jaikaria NS, Newman SA. 1989. The mechanism of precartilaginous mesenchymal condensation: a major role for interaction of the cell surface with the amino-terminal heparin-binding domain of fibronectin. Dev Biol 136:97-103.
21. Gardner JM, Fambrough DM. 1983. Fibronectin expression during myogenesis. J Cell Biol 96:474-485.
22. Gehris AL, Stringa E, Spina J, Desmond ME, Tuan RS, Bennett VD. 1997. The region encoded by the alternatively spliced exon IIIA in mesenchymal fibronectin appears essential for chondrogenesis at the level of cellular condensation. Dev Biol 190:191-205.
23. Hall BK, Miyake T. 1995. Divide, accumulate, differentiate: cell condensation in skeletal development revisited. Int J Dev Biol 39:881-893.
24. Hamburger V, Hamilton HL. 1951. A series of normal stages in development of the chick embryo. J Morphol 88:49-91.
25. Hassell JR, Horrigan EA. 1982. Chondrogenesis: a model developmental system for measuring teratogenic potential of compounds. Teratogen Carcinogen Mutagen 2:325-331.
26. Hoang B, Moos M Jr, Vukicevic S, Luyten FP. 1996. Primary structure and tissue distribution of FRZB, a novel protein related to Drosophila frizzled, suggest a role in skeletal morphogenesis. J Biol Chem 271:26131-26137.
27. Jiang TX, Jian-Ru Y, Shao-Yao Y, Chuong CM. 1993. Activin enhances chondrogenesis of limb bud cells: stimulation of precartilaginous mesenchymal condensations and expression of NCAM. Dev Biol 155:545-557.
28. Johnson RL, Tabin CJ. 1997. Molecular models for vertebrate limb development. Cell 90:979-990.
29. Jung HS, Francis-West PH, Widelitz RB, Jiang TX, Ting-Berreth S, Tickle S, Wolpert L, Chuong CM. 1998. Local inhibitory action of BMPs and their relationships with activators in feather formation: implications for periodic patterning. Dev Biol 196:11-23.
30. Knudson CB, Toole BP. 1985. Changes in the pericellular matrix during differentiation of the limb bud mesoderm. Dev Biol 112:308-318.
31. Kulyk WM, Rodgers BJ, Greer K, Kosher RA. 1989. Promotion of embryonic chick limb cartilage differentiation by transforming growth factor-beta. Dev Biol 135:424-430.
32. Labarca C, Paigen K. 1980. A simple, rapid, and sensitive DNA assay procedure. Anal Biochem 102:344-352.
33. Lee YS. 1996. The role of cell adhesion in precartilage condensation and its modulation by BMP-2, FGF-4 and protein kinase pathway. Ph.D. thesis. University of Southern California.
34. Lee YS, Chuong CM. 1997. Activation of protein kinase A is a pivotal step in both BMP-2 and cyclic-AMP induced chondrogenesis. J Cell Physiol 170:153-165.
35. Lee YS, Stott NS, Jiang TX, Widelitz RB, Chuong CM. (In press). Early events during precartilage condensation in limb bud micromass cultures.
36. Leonard C, Fuld HM, Frenz DA, Downie SA, Massague J, Newman SA. 1991. Role of transforming growth factor beta in chondrogenic pattern formation in the embryonic limb. Dev Biol 145:99-109.
37. Lev R, Spicer SS. 1964. Specific staining of sulfate groups with Alcian blue at low pH. J Histochem Cytochem 12:38-41.
38. Macias D, Ganan Y, Sampath TK, Piedra ME, Ros MA, Hurle JM. 1997. Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development 124:1109-1117.
39. Mackie EJ, Thesleff I, Chiquet-Ehrismann R. 1987. Tenascin-C is associated with chondrogenic and oateogenic differentiation in vivo and promotes chondrogenesis in vitro. J Cell Biol 105:2569-2579.
40. Moon RT, Brown JD, Torres M. 1997a. WNTs modulate cell fate and behavior during vertebrate development. Trends Genet 13:157-162.
41. Moon RT, Brown JD, Yang-Synder JA, Miller JR. 1997b. Structurally related receptors and antagonists compete for secreted Wnt ligands. Cell 88:725-728.
42. Morgan BA, Fekete DM. 1996. Manipulating gene expression with replication competent viruses. Method Cell Biol 51:185-218.
43. Newman SA. 1996. Sticky fingers: Hox genes and cell adhesion in vertebrate limb development. Bioessays 18:171-174.
44. Oberlender SA, Tuan R. 1994. Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis. Development 120: 177-187.
45. O'Keefe RJ, Puzas JE, Loveys L, Hicks DG, Rosier RN. 1994. Analysis of type II and type X collagen synthesis in cultured growth plate chondrocytes by in-situ hybridization: rapid induction of type X collagen in culture. J Bone Miner Res 9:1713-1722.
46. Pacifici M. 1995. Tenascin-C and the development of articular cartilage. Matrix Biol 14:689-698.
47. Pacifici M, Golden EB, Iwamoto M, Adams SL. 1991. Retinoic acid induces type X collagen expression in cultured chick chondrocytes. Exp Cell Res 195:38-46.
48. Parr BA, Shea MJ, Vassileva G, McMahon AP. 1993. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119:247-261.
49. Parr BA, Avery EJ, Cygan JA, McMahon AP. 1998. The classical mouse mutant postaxial hemimelia results from a mutation in the Wnt-7a gene. Dev Biol 202:228-234.
50. Paulsen DF, Chen WD, Pang L, Johnson B, Okello D. 1994, Stage-and region-dependent chondrogenesis and growth of chick wing-bud mesenchyme in serum-containing and defined tissue culture media. Dev Dyn 200:39-52.
51. Reddi AH. 1998. Role of morphogenetic proteins in skeletal tissue engineering and regeneration. Nat Biotechnol 16:247-252.
52. Riley EH, Lane JM, Urist MR, Lyons KM, Lieberman JR. 1996. Bone morphogenetic protein-2: biology and applications. Clin Orthop 324: 39-46.
53. Roark EF, Greer K. 1994. Transforming growth factor-beta and bone morphogenetic protein-2 act by distinct mechanisms to promote chick limb cartilage differentiation in vitro. Dev Dyn 200:103-116.
54. Rudnicki JA, Brown AMC. 1997. Inhibition of chondrogenesis by Wnt gene expression in vivo and in vitro. Dev Biol 185:104-118.
55. Siegfried E, Perrimon N. 1994. Drosophila wingless: a paradigm for the function and mechanism of Wnt signaling. Bioessays 16:395-404.
56. Stott NS, Chuong CM. 1997. Dual action of sonic hedgehog on chondrocyte hypertrophy: retrovirus mediated ectopic sonic hedgehog expression in limb bud micromass culture induces novel cartilage nodules that are positive for alkaline phosphatase and type X collagen. J Cell Sci 110:2691-2701.
57. Stott NS, Lee YS, Chuong CM. 1998. Retroviral gene transfer in chondrogenic limb bud micromass culture. Biotechniques 24:660-666.
58. Tickle C. 1995. Vertebrate limb development. Curr Biol 5:478-484.
59. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, Tabin CJ. 1996. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273:613-622.
60. Widelitz RB, Jiang TX, Murray BA, Chuong CM. 1993. Adhesion molecules in skeletogenesis: II. Neural cell adhesion molecules mediate precartilaginous condensations and enhance chondrogenesis. J Cell Physiol 156:399-411.
61. Wozney JM, Rosen V. 1998. Bone morphogenetic protein and bone morphogenetic protein gene family in bone formation and repair Clin Orthop 346:26-37.
62. Yamashita H, Ten Dijke P, Heldin CH, Miyazono K. 1996. Bone morphogenetic protein receptors. Bone 19:569-574.
63. Yang Y, Niswander L. 1995. Interaction between the signaling molecules WNT7A and SHH during vertebrate limb development: dorsal signals regulate anteroposterior patterning. Cell 80:939-947.
64. Zakany J, Duboule D. 1993. Correlation of expression of Wnt-1 in developing limbs with abnormalities in growth skeletal patterning. Nature 362:546-549.
65. Zanetti NC, Solursh M. 1986. Epithelial effects on limb chondrogenesis involve extracellular matrix and cell shape. Dev Biol 113:110-118.
66. Zou H, Weiser R, Massague J, Niswander L. 1997. Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev 11:2191-2203.