Differential regulation of GDF-5 and FGF-2/4 by immobilisation in ovo exposes distinct roles in joint formation

Developmental Dynamics

Volumn 235, Issue 3, 2006, Pages 826-834

  Kavanagh, E ^a   Church, V L ^b   Osborne, A C ^c   Lamb, K J ^a   Archer, C W ^d   Francis West, P H ^b   Pitsillides, A A ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c ASTRAZENECA   (United Kingdom)

^d CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Cavitation; FGF; GDF 5; Joint; Movement

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 4; GROWTH DIFFERENTIATION FACTOR 5;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE CELL; CELL NUCLEUS; CHICK EMBRYO; CHONDROGENESIS; CONTROLLED STUDY; DYNAMICS; EMBRYO; GENE OVEREXPRESSION; IMMOBILIZATION; IMMUNOHISTOCHEMISTRY; JOINT; JOINT CAVITY; LIMB MOVEMENT; MECHANICAL STIMULATION; MECHANICAL STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CHICK EMBRYO; CHONDROCYTES; CHONDROGENESIS; DOWN-REGULATION; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 4; IMMOBILIZATION; JOINTS; OVUM; RNA, MESSENGER; STRESS, MECHANICAL;

ANIMALIA;

EID: 33644923194     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20679     Document Type: Article

References (72)

1. Abu-Hijleh G, Reid O, Scothorne RJ. 1997. Cell death in the developing chick knee joint: I. Spatial and temporal patterns. Clin Anat 10:183-200.
2. Aikawa T, Segre GV, Lee K. 2001. Fibroblast growth factor inhibits chondrocytic growth through induction of p21 and subsequent inactivation of cyclin E-Cdk2. J Biol Chem 276:29347-29352.
3. Anderson R, Landry M, Muneoka K. 1993. In vitro maintenance of posterior (ZPA) signaling in mouse limb bud cells. Prog Clin Biol Res 383A:371-380.
4. Archer CW, Dowthwaite GP, Francis-West P. 2003. Development of synovial joints. Birth Defects Res C Embryo Today 69: 144-155.
5. Balazs EA, Watson D, Duff IF, Roseman S. 1967. Hyaluronic acid: I Molecular parameters of HA in normal and arthritic fluids. Arthrit Rheum 10:357-376.
6. Bastow ER, Lamb KJ, Osborne A, Kavanagh E, Lewthwaite JC, Wheeler-Jones CPD, Pitsillides AA. 2005. Selective activation of the MEK-ERK pathway is regulated by mechanical stimuli in forming joints and promotes pericellular matrix formation. J Biol Chem 280:11749-11758.
7. Bernays A. 1878. The history of the development of the human knee joint with remarks about joints in general. Morphol Jahrb 4:403-446.
8. Brecht M, Mayer U, Schlosser E, Prehm P. 1986. Increased hyaluronate synthesis is required for fibroblast detachment and mitosis. Biochem J 239:445-450.
9. Chayen J, Bitensky L. 1991. Practical histochemistry. London: John Wiley & Sons
10. Cheng GC, Briggs WH, Gerson DS, Libby P, Grodzinsky AJ, Gray ML, Lee RT. 1997 Mechanical strain tightly controls fibroblast growth factor-2 release from cultured human vascular smooth muscle cells. Circ Res 80:28-36.
11. Cho TJ, Gerstenfeld LC, Einhorn TA. 2002. Differential temporal expression of members of the transforming growth factor beta superfamily during murine fracture healing. J Bone Miner Res 17:513-520.
12. Cohn MJ, Izpisua-Belmonte JC, Abud H, Heath JK, Tickle C. 1995. Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 80:739-746
13. Craig FM, Bayliss MT, Bentley G, Archer CW. 1990. A role for hyaluronan in joint development. J Anat 171:17-23.
14. Dowthwaite GP, Edwards JCW, Pitsillides AA. 1998. An essential role for the interaction between hyaluronan and hyaluronan binding proteins during joint development. J Histochem Cytochem 46:641-651.
15. Dowthwaite GP, Ward AC, Flannely J, Suswillo RF, Flannery CR, Archer CW, Pitsillides AA. 1999. Effect of mechanical strain on hyaluronan metabolism in embryonic fibrocartilage cells. Matrix Biol 18:523-532.
16. Drachman DB, Sokoloff L. 1966. The role of movement in embryonic joint development. Dev Biol 14:401-420.
17. Edwards CJ, Francis-West PH. 2001. Bone morphogenetic proteins in the development and healing of synovial joints. Semin Arthritis Rheum 31:33-42.
18. Edwards JC, Wilkinson LS, Jones HM, Soothill P, Henderson KJ, Worrall JG, Pitsillides AA. 1994. The formation of human synovial joint cavities: a possible role for hyaluronan and CD44 in altered interzone cohesion. J Anat 185:355-367.
19. Fallon JF, Lopez A, Ros MA, Savage MP, Olwin BB, Simandl BK. 1994. FGF-2: apical ectodermal ridge growth signal for chick limb development. Science 264:104-107.
20. Fell HB, Canti RG. 1934. Experiments on the development in vitro of the avian knee joint. Proc R Soc B1176:316-351.
21. Fosang AJ, Hex NJ, Carney SL, Hardingham TE. 1990. An ELISA plate-based assay for hyaluronan using biotinylated GI domain (HA-binding region). Matrix 10:306-313.
22. Francis-West PH, Abdelfattah A, Chen P, Allen C, Parish J, Ladher R, Allen S, MacPherson S, Luyten FP, Archer CW. 1999a. Mechanisms of Gdf-5 action during skeletal development. Development 126:1305-1315
23. Francis-West PH, Parish J, Lee K, Archer CW. 1999b. BMP/GDF-signalling interactions during synovial joint development. Cell Tissue Res 296:111-119.
24. Guo X, Day TF, Jiang X, Garrett-Beal L, Topol L, Yang Y. 2004. Wnt/beta-catenin signaling is sufficient and necessary for synovial joint formation. Genes Dev 18: 2404-2417.
25. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
26. Hamburger V, Waugh M. 1940. The primary development of the skeleton in nerveless and poorly innervated limb transplants of chick embryos. Physiol Zool 13:367-380.
27. Hartmann C, Tabin CJ. 2001. Wnt-14 plays a pivotal role in inducing synovial joint formation in the developing appendicular skeleton. Cell 104:341-351.
28. Houliston RA, Pearson JD, Wheeler-Jones CP. 2001. Agonist-specific cross talk between ERKs and p38(mapk) regulates PGI(2) synthesis in endothelium. Am J Physiol Cell Physiol 281:01266-1276.
29. Ito MM, Kida MY. 2000. Morphological and biochemical re-evaluation of the process of cavitation in the rat knee joint: cellular and cell strata alterations in the interzone. J Anat 197:659-679.
30. Kavanagh E, Osborne AC, Ashhurst DE, Pitsillides AA. 2002a. Keratan sulfate epitopes exhibit a conserved distribution during joint development that remains undisclosed on the basis of glycosaminoglycan charge density. J Histochem Cytochem 50:1039-1047.
31. Kavanagh E, Abiri M, Bland YS, Ashhurst DE. 2002b. Division and death of cells in developing synovial joints and long bones. Cell Biol Int 26:679-688.
32. Knudson CB, Munaim SI, Toole BP. 1995. Ectodermal stimulation of the production of hyaluronan-dependent pericellular matrix by embryonic limb mesodermal cells. Dev Dyn 204:186-191.
33. Kuroda K, Utani A, Hamasaki Y, Shinkai H. 2001. Up-regulation of putative hyaluronan synthase mRNA by basic fibroblast growth factor and insulin-like growth factor-1 in human skin fibroblasts. J Dermatol Sci 26:156-160.
34. Lamb KJ, Lewthwaite JC, Bastow ER, Pitsillides AA. 2003. Defining boundaries during joint cavity formation: going out on a limb. Int J Exp Pathol 84:55-67.
35. Laufer E, Nelson CE, Johnson RL, Morgan BA, Tabin C. 1994. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79:993-1003.
36. Lelkes G. 1958. Experiments in vitro on the role of movement in the development of joints. J Embryol Exp Morphol 6:183-186.
37. Lightfoot PS, Swisher R, Coffin JD, Doetschman TC, German RZ. 1997. Ontogenetic limb bone scaling in basic fibroblast growth factor (FGF-2) transgenic mice. Growth Dev Aging 61:127-139.
38. Logan C, Francis-West P. 1999. Gene transfer in avian embryos using replication-competent retroviruses. Methods Mol Biol 97:539-551.
39. Macias D, Ganan Y, Ros MA, Hurle JM. 1996. In vivo inhibition of programmed cell death by local administration of FGF-2 and FGF-4 in the interdigital areas of the embryonic chick leg bud. Anat Embryol 193:533-541.
40. Mehdizadeh S, Bitensky L, Chayen J. 1991. The assay of uridine diphosphoglucose dehydrogenase activity: discrimination from xanthine dehydrogenase activity. Cell Biochem Funct 9:103-110
41. Merino R, Macias D, Ganan Y, Economides AN, Wang X, Wu Q, Stahl N, Samath KT, Varona P, Hurle JM. 1999. Expression and function of Gdf-S during digit skeletogenesis in the embryonic chick leg bud. Dev Biol 206:33-45.
42. Mitrovic D. 1971. Effect of pharmacological paralysis on the formation and evolution of articular fissures of the digital joints in chick embryo feet. Acad Sci Hebd Seances Acad Sci 273:1748-1751.
43. Mitrovic D. 1974. Blood vessels and arthrogenesis. A possible relationship with the cavitation process (author's translation). Z Anat Entwicklung 144:39-60.
44. Mitrovic D. 1978. Development of the diarthrodial joints in the rat embryo. Am J Anat 151:475-485.
45. Mitrovic D. 1982. Development of the articular cavity in paralysed chick embryos and in chick embryo limb buds cultured on chorioallabtoic membranes. Acta Anat 113:313-324.
46. Moone AM, Boulet AM, Capecchi MR. 2000. Normal limb development in conditional mutants of FGF4. Development 127:989-996.
47. Munaim SI, Klagsbrun M, Toole BP. 1991. Hyaluronan-dependent pericellular coats of chick embryo limb mesodermal cells: induction by basic fibroblast growth factor. Dev Biol 143:297-302.
48. Murray PDF, Drachman DB. 1969. The role of movement in the development of joints and related structures: the head and neck in the chick embryo. J Embryol Exp Morphol 22:349-371.
49. Niswander L, Martin GR. 1993. FGF-4 and BMP-2 have opposite effects on limb growth. Nature 361:68-71.
50. Niswander L, Tickle C, Vogel A, Booth I, Martin GR. 1993. FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75:579-587.
51. Ochiya T, Sakamoto H, Tsukamoto M, Sugimura T, Terada M. 1995. Hst-1 (FGF-4) antisense oligonucleotides block murine limb development. J Cell Biol 130:997-1003.
52. Osborne AC, Lamb KJ, Lewthwaite JC, Dowthwaite GP, Pitsillides AA. 2002. Short-term rigid and flaccid paralysis diminish growth of embryonic chick limbs and abrogate joint cavity formation but differentially preserve pre-cavitated joints. J Musculoskel Neuron Interact 2: 448-456.
53. Pitsillides AA. 1999. The role of hyaluronan in joint cavitation. Biology of the synovial joint. In: Archer CW, Caterson B, Ralphs J, Benjamin M, editors. London: Harwood Academics, p 41-61.
54. Pitsillides AA, Blake SM. 1992. Uridine Diphosphosglucose dehydrogenase activity in synovial lining cells in the experimental antigen induced model of rheumatoid arthritis: an indication of synovial lining cell function. Ann Rheumat Dis 51:992-995.
55. Pitsillides AA, Archer CW, Prehm P, Bayliss MT, Edwards JC. 1995a. Alterations in hyaluronan synthesis during developing joint cavitation. J Histochem Cytochem 43:263-273.
56. Pitsillides AA, Rawlinson SCF, Suswillo RF, Bourrin S, Zaman G, Lanyon LE. 1995b. Mechanical strain-induced NO production by bone cells: a possible role in adaptive bone (re)modelling? FASEB 9:1614-1622.
57. Quinn TP, Schlueter M, Soifer SJ, Gutierrez JA. 2002. Cyclic mechanical stretch induces VEGF and FGF-2 expression in pulmonary vascular smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 282: L897-903
58. Riley BB, Savage MP, Simandl BK, Olwin BB, Fallon JF. 1993. Retroviral expression of FGF-2 (bFGF) affects patterning in chick limb bud. Development 118:95-104.
59. Ruano-Gil D, Nardi-Vilardaga J, Teixidor-Johe A. 1980. Embryonic mobility and joint development. Folia Morphol (Praha) 28:221-223.
60. Skutek M, van Griensven M, Zeichen J, Brauer N, Bosch U. 2001. Cyclic mechanical stretching modulates secretion pattern of growth factors in human tendon fibroblasts. Eur J Appl Physiol 86:48-52.
61. Storm EE, Kingsley DM. 1996. Joint patterning defects caused by single and double mutations in members of the bone morphogenic protein family Development 122:3969-3979.
62. Storm EE, Kingsley DM. 1999. Gdf-5 coordinates bone and joint formation during digit development. Dev Biol 209:11-27.
63. Sun X, Lewandoski M, Meyers EN, Liu Y-H, Maxson RE, Martin GR. 2000. Conditional inactivation of FGF4 reveals complexity of signalling during lib bud development. Nature Genet 25:83-86.
64. Sun X, Mariani FV, Martin GR. 2002. Functions of FGF signalling from the apical dermal ridge in limb development. Nature 418:501-508.
65. Sundbland L. 1953. Studies on hyaluronate in synovial fluids. Acta Soc Meds Ups 58:113-119.
66. Taylor GP, Anderson R, Reginelli AD, Muneoka K. 1994. FGF-2 induces regeneration of the chick limb bud. Dev Biol 163: 282-284.
67. Tickle C. 2000. Limb development: an international model for vertebrate pattern formation. Int J Dev Biol 44:101-108.
68. Tsumaki N, Nakase T, Miyaji T, Kakiuchi M, Kimura T, Ochi T, Yoshikawa H. 2002. Bone morphogenicprotein signals are required for cartilage formation and differently regulate joint development during skeletogenesis. J Bone Miner Res 17:898-906
69. Vogel A, Tickle C. 1993. FGF-4 maintains polarizing activity of posterior limb bud cells in vivo and in vitro. Development 119:199-206.
70. Ward AC, Dowthwaite GP, Edwards JCW, Pitsillides AA. 1997. The effect of embryonic limb immobilisation on cavitation-associated changes in hyaluronan synthesis and FGF-2 and 4 expression during development. Conn Tissue Res 36: 104-105.
71. Waris V, Xu JW, Nordsletten L, Sorsa T, Santavirta S, Konttinen YT. 1996. Basic fibroblast growth factor (bFGF) in the synovial-like membrane around loose total hip prostheses. Scand J Rheumatol 25:257-262.
72. Yasuda Y. 1973 Differentiation of human limb buds in vitro. Anat Rec 175:561-579.