A critical evaluation of specific aspects of joint development

Developmental Dynamics

Volumn 237, Issue 9, 2008, Pages 2284-2294

  Pitsillides, Andrew ^a   Ashhurst, Doreen E ^b  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Cartilage; Joint cavitation; Joint specification

Indexed keywords

COLLAGEN TYPE 2;

ARTICULAR CARTILAGE; CHONDROGENESIS; EMBRYO DEVELOPMENT; JOINT; JOINT CAVITY; LIMB DEVELOPMENT; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; CHICK EMBRYO; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; JOINTS; MICE; MODELS, BIOLOGICAL;

EID: 51549094758     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21654     Document Type: Review

References (107)

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. Aigner T, Gebhard PM, Schmid E, Bau B, Harley V, Poschl E. 2003. SOX9 expression does not correlate with type II collagen expression in adult articular chondrocytes. Matrix Biol 22:363-372.
3. Akiyama H, Chaboissier MC, Martin JF, Schedl A, de Crombrugghe B. 2002. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 16:2813-2828.
4. Akiyama H, Kim JE, Nakashima K, Balmes G, Iwai N, Deng JM, Zhang Z, Martin JF, Behringer RR, Nakamura T, de Crombrugghe B. 2005. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci USA 102:14665-14670.
5. Andersen H. 1961. Histochemical studies on the histogenesis of the knee joint and superior tibio-fibular joint in human foetuses. Acta Anat 46:279-303.
6. Archer CW, Buxton P, Hall BK, Francis-West P. 2006. Mechanical regulation of secondary chondrogenesis. Biorheology 43:355-370.
7. Barlow AJ, Bogardi JP, Ladher R, Francis-West PH. 1999. Expression of chick Barx-1 and its differential regulation by FGF-8 and BMP signaling in the maxillary primordia. Dev Dyn 214:291-302.
8. Bastow ER, Lamb KJ, Lewthwaite JC, Osborne AC, Kavanagh E, Wheeler-Jones CP, 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.
9. Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. 1999. Sox9 is required for cartilage formation. Nat Genet 22: 85-89.
10. Bland YS, Ashhurst DE. 1996. Development and ageing of the articular cartilage of the rabbit knee joint: distribution of the fibrillar collagens. Anat Embryol 194:607-619.
11. Bland YS, Ashhurst DE. 2001. The hip joint: the fibrillar collagens associated with development and ageing in the rabbit. J Anat 198:17-27.
12. Brunet LJ, McMahon JA, McMahon AP, Harland RM. 1998. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 280: 1455-1457.
13. Capdevila J, Johnson RL. 1998. Endogenous and ectopic expression of noggin suggests a conserved mechanism for regulation of BMP function during limb and somite patterning. Dev Biol 197:205-217.
14. Cheah KSE, Lau ET, Au PKC, Tam PPL. 1991. Expression of the mouse α1 (II) collagen gene is not restricted to cartilage during development. Development 111:945-953.
15. Craig FM, Bentley G, Archer CW. 1987. The spatial and temporal pattern of collagens I and II and keratan sulphate in the developing chick metatarsophalangeal joint. Development 99:383-391.
16. de la Fuente L and Helms JA. 2005. The fickle finger of fate. J Clin Invest 115: 833-836.
17. 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. JEEM 57:51-60.
18. Dowthwaite GP, Edwards JC, Pitsillides AA. 1998. An essential role for the interaction between hyaluronan and hyaluronan binding proteins during joint development. J Histochem Cytochem 46:641-651.
19. Dowthwaite GP, Flannery CR, Flannelly J, Lewthwaite JC, Archer CW, Pitsillides AA. 2003. A mechanism underlying the movement requirement for synovial joint cavitation. Matrix Biol 22:311-322.
20. Dowthwaite GP, Bishop JC, Redman SN, Khan IM, Rooney P, Evans DJR, Haughton L, Bayram Z, Boyer S, Thomson B, Wolfe MS, Archer CW. 2004. The surface of articular cartilage contains a progenitor cell population. J Cell Sci 117:889-897.
21. Duboule D. 2002. Making progress with limb models. Nature 418:492-493.
22. Dudley AT, Ros MA, Tabin CJ. 2002. A re-examination of proximodistal patterning during vertebrate limb development. Nature 418:539-544.
23. Edwards JC, Wilkinson LS, Jones HM, Soothill P, Henderson KJ. 1994. The formation of human synovial joint cavities: a possible role for hyaluronan and CD44 in altered interzone cohesion. J Anat 185:355-367.
24. Edwards JC, Wilkinson LS, Soothill P, Hembry RM, Murphy G, Reynolds JJ. 1996. Matrix metalloproteinases in the formation of human synovial joint cavities. J Anat 188:355-360.
25. Farge, E. 2003. Mechanical induction of twist in the Drosophila foregut/stomodeal primordium. Current Biol 13:1365-1377.
26. Fell, HB, Canti, RG. 1934. Experiments on the development in vitro of the avian knee joint. Proc R Soc B1176:316-351.
27. Fernandez-Teran MA, Hinchliffe JR, Ros MA. 2006. Birth and death of cells in limb development: a mapping study. Dev Dyn 235:2521-2537
28. Francis-West PH, Abdelfattah A, Chen P, Allen C, Parish J, Ladher R, Allen S, MacPherson S, Luvten FP, Archer CW. 1999a. Mechanisms of GDF-5 action during skeletal development. Development 126:1305-1315.
29. Francis-West PH, Parish J, Lee K, Archer CW. 1999b. BMP/GDF-signalling interactions during synovial joint development. Cell Tissue Res 296:111-119.
30. Furusawa T, Lim JH, Catez F, Birger Y, Mackem S, Bustin M. 2006. Down-regulation of nucleosomal binding protein HMGN1 expression during embryogenesis modulates Sox9 expression in chondrocytes. Mol Cell Biol 26:592-604.
31. Garciadiego-Cazares D, Rosales C, Katoh M, Chimal-Monroy J. 2004. Coordination of chondrocyte differentiation and joint formation by alpha5beta1 integrin in the developing appendicular skeleton. Development 131:4735-42.
32. Guo X, Day TF, Jiang X, Garrett-Beal L, Topol L, Yang, Y. 2004. Wnt/β-catenin signaling is sufficient and necessary for synovial joint formation. Genes Dev 18: 2404-2417.
33. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
34. Hartmann C, Tabin CJ. 2000. Dual roles of Wnt signalling during chondrogenesis in the chicken limb. Development 127:3141-3159.
35. 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.
36. Hyde G, Dover S, Aszodi A, Wallis GA, Boot-Handford RP. 2007. Lineage tracing using matrilin-1 gene expression reveals that articular chondrocytes exist as the joint interzone forms. Dev Biol 304: 825-833.
37. Ikeda T, Kamekura S, Mabuchi A, Kou I, Seki S, Takato T, Nakamura K, Kawaguchi H, Ikegawa S, Chung UI. 2004. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum 50:3561-3573.
38. 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.
39. Kavanagh E, Ashhurst DE. 1999. Development and ageing of the articular cartilage of the rabbit knee joint: distribution of biglycan, decorin, and matrilin-1. J Histochem Cytochem 47:1603-1615.
40. Kavanagh E, Abiri M, Bland YS, Ashhurst DE. 2002a. Division and death of cells in developing synovial joints and long bones. Cell Biol Int 26:679-688.
41. Kavanagh E, Osborne AC, Ashhurst DE, Pitsillides AA. 2002b. Keratan sulphate epitopes exhibit a conserved distribution during joint development that remains undisclosed on the basis of GAG charge density. J Histochem Cytochem 50:1039-47.
42. Kavanagh E, Osborne AC, Church VL, Lamb KJ, Francis-West PH, Archer CW, Pitsillides AA. 2006. Differential regulation of GDF-5 and FGF-2/4 by immobilisation in ovo exposes distinct roles in joint formation. Dev Dyn 235:826-834
43. Kawakami Y, Wadda N, Nishimatsu S-I, Ishikawa T, Noji S, Nohno T. 1999. Involvement of Wnt-5a in chondrogenic pattern formation in the chick limb bud. Develop Growth Differ 41:29-40.
44. Kawakami Y, Rodriguez-Leon J, Belmonte JC. 2006. The role of TGFbetas and Sox9 during limb chondrogenesis. Curr Opin Cell Biol 18:723-729.
45. Kim JH, Do HJ, Yang HM, Oh JH, Choi SJ, Kim DK, Cha KY, Chung HM. 2005. Overexpression of SOX9 in mouse embryonic stem cells directs the immediate chondrogenic commitment. Exp Mol Med 37:261-268.
46. Kimura S, Shiota K. 1996. Sequential changes of programmed cell death in developing fetal mouse limbs and its possible roles in limb morphogenesis. J Morph 229:337-346.
47. Kosher RA, Solursh M. 1989. Widespread distribution of type II collagen during embryonic chick development. Dev Biol 131:558-566.
48. Koyama E, Leatherman JL, Shimazu A, Nah H-D, Pacifici M. 1995. Syndecan-3, tenascin-C, and the development of cartilaginous skeletal elements and joints in chick limbs. Dev Dyn 203:152-162.
49. Koyama E, Shibukawa Y, Nagayama M, Sugito H, Young B, Yuasa T, Okabe T, Ochiai T, Kamiya N, Rountree RB, Kingsley DM, Iwamoto M, Enomoto-Iwamoto M, Pacifici M. 2008. A distinct cohort of progenitor cells participates in synovial joint and articular cartilage formation during mouse limb skeletogenesis. Dev Biol 316:62-73.
50. Kravis D, Upholt WB. 1985. Quantitation of type II procollagen mRNA levels during chick limb cartilage differentiation. Dev Biol 108:164-172.
51. 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.
52. Li Y, Tew SR, Russell AM, Gonzalez KR, Hardingham TE, Hawkins RE. 2004. Transduction of passaged human articular chondrocytes with adenoviral, retroviral, and lentiviral vectors and the effects of enhanced expression of SOX9. Tissue Eng 10:575-584.
53. Lizarraga G, Lichtler A, Upholt WB, Kosher RA. 2002. Studies on the role of Cux1 in regulation of the onset of joint formation in the developing limb. Dev Biol 243:44-54.
54. Lovinescu I, Koyama E, Pacifici M. 2003. Roles of FGF-10 on the development of diathrodial limb joints. Penn Dent J 103: 5-9.
55. Lui VCH, Ng LJ, Nicholls J, Tam PPL, Cheah KSE. 1995. Tissue-specific and differential expression of alternatively spliced α1(II) collagen mRNAs in early human embryos. Dev Dyn 203:198-211.
56. Mariani FV, Martin GR. 2003. Deciphering skeletal patterning: clues from the limb. Nature 423:319-325.
57. Merino R, Macias D, Ganan Y, Economides AN, Wang X, Wu Q, Stahl N, Sampath KT, Varona P, Hurle JM. 1999. Expression and function of Gdf-5 during digit skeletogenesis in the embryonic chick leg bud. Dev Biol 206:33-45.
58. Mitrovic DR. 1977. Development of the metatarsophalangeal joint of the chick embryo: morphological, ultrastructural and histochemical studies. Am J Anat 150:333-348.
59. Mitrovic DR. 1978. Development of the diarthrodial joints in the rat embryo. Am J Anat 151:475-486.
60. Mori C, Nakamura N, Kimura S, Irie H, Takigawa T, Shiota K. 1995. Programmed cell death in the interdigital tissue of the fetal mouse limb is apoptosis with DNA fragmentation. Anat Rec 242:103-110.
61. Murphy JM, Heinegård D, McIntosh A, Sterchi D, Barry FP. 1999. Distribution of cartilage molecules in the developing mouse joint. Matrix Biol 18:487-497.
62. Nah H-D, Upholt WB. 1991. Type II collagen mRNA containing an alternatively spliced exon predominates in chick limb prior to chondrogenesis. J Biol Chem 266:23446-23452.
63. Nah H-D, Rodgers BJ, Kulyk WM, Kream BE, Kosher RA, Upholt WB. 1988. In situ hybridization analysis of the expression of the type II collagen gene in the developing chicken limb bud. Collagen Rel Res 8:277-294.
64. Nalin AM, Greenlee TK, Sandell LJ. 1995. Collagen gene expression during development of avian synovial joints: transient expression of types II and XI collagen genes in the joint capsule. Dev Dyn 203:352-362.
65. Niedermaier M, Schwabe GC, Fees S, Helmrich A, Brieske N, Seemann P, Hecht J, Seitz V, Strieker S, Leschik G, Schrock E, Selby PB, Mundlos S. 2005. An inversion involving the mouse Shh locus results in brachydactyly through dysregulation of Shh expression. J Clin Invest 115:900-909.
66. Ng LJ, Tam PPL, Cheah KSE. 1993. Preferential expression of alternatively spliced mRNAs encoding type II procollagen with a cysteine-rich amino-propeptide in differentiating cartilage and non-chondrogenic tissues during early mouse development. Dev Biol 159:403-417.
67. Ng L-J, Wheatley S, Muscat GEO, Conway-Campbell J, Bowles J, Wright E, Bell DM, Tam PPL, Cheah KSE, Koopman P. 1997. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol 183:108-121.
68. Oganesian A, Zhu Y, Sandell LJ. 1997. Type IIA procollagen amino propeptide is localized in human embryonic tissues. J Histochem Cytochem 45:1469-1480.
69. Osborne AC, Lamb KJ, Lewthwaite JC, Dowthwaite GP, Wheeler-Jones CPD, 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. Journal of Musculoskeletal and Neuronal Interactions 2:448-456.
70. Pacifici M, Koyama E, Iwamoto M, Gentili C. 2000. Development of articular cartilage: what do we know about it and how may it occur? Connect Tissue Res 41: 175-184.
71. Pacifici M, Koyama E, Iwamoto M. 2005. Mechanisms of synovial joint and articular cartilage formation: recent advances, but many lingering mysteries. Birth Defects Res C Embryo Today 75: 237-248.
72. Pacifici M, Koyama E, Shibukawa Y, Wu C, Tamammura Y, Enomoto-Iwamoto M, Iwamoto M. 2006. Cellular and molecular mechanisms of synovial joint and articular cartilage formation. Ann NY Acad Sci 1068:74-86.
73. Pitsillides AA. 1999. The role of hyaluronan in joint cavitation. In: Archer CW, Caterson B, Benjamin M, Ralphs JR, editors. Singapore: Harwood Academic Publishers. p 41-62.
74. Pitsillides AA, Archer CW, Prehm P, Baylies MT, Edwards JC. 1995. Alterations in hyaluronan synthesis during developing joint cavitation. J Histochem Cytochem 43:263-273.
75. Ryan MC, Sandell LJ. 1990. Differential expression of a cysteine-rich domain in the amino-terminal propeptide of type II (cartilage) procollagen by alternative splicing of mRNA. J Biol Chem 265:10334-10339.
76. Ryan MC, Sieraski M, Sandell LJ. 1990. The human type II procollagen gene: identification of an additional protein-coding domain and location of potential regulatory sequences in the promoter and first intron. Genomics 8:41-48.
77. Salminen H, Vuorio E, Saamanen AM. 2001. Expression of Sox9 and type IIA procollagen during attempted repair of articular cartilage damage in a transgenic mouse model of osteoarthritis. Arthritis Rheum 44:947-955.
78. Sandell LJ, Nalin AM, Reife RA. 1994. Alternative splice form of type II procollagen mRNA (IIA) is predominant in skeletal precursors and non-cartilaginous tissues during early mouse development. Dev Dyn 199:129-140.
79. Sandell LJ, Zhu Y, Oganesian A. 1997. Collagen gene expression as markers for skeletal development, disease, and repair. In: Buckwalter JA, Ehrlich MG, Sandell LJ, Tripel SB, editors. Skeletal growth and development; clinical issues and basic science advances. Chapter 3. Rosemont, IL: American Academy of Orthopaedic Surgeons. pp 37-52.
80. Sanz-Ezquerro JJ, Tickle C. 2003. Fgf signaling controls the number of phalanges and tip formation in developing joints. Curr Biol 13:1830-1836.
81. Satoh A, Suzuki M, Amano T, Tamura K, Ide H. 2005. Joint development in Xenopus laevis and induction of segmentations in regenerating froglet limb (spike). Dev Dyn 233:1444-1453.
82. Segat D, Frie C, Nitsche PD, Klatt AR, Piecha D, Korpos E, Deák F, Wagener R, Paulsson M, Smyth N. 2000. Expression of matrilin-1, -2 and -3 in developing mouse limbs and heart. Matrix Biol 19: 649-655.
83. Settle SH Jr, Rountree RB, Sinha A, Thacker A, Higgins K, Kingsley DM. 2003. Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse Gdf6 and Gdf5 genes. Dev Biol 254:116-130.
84. Singley CT, Solursh M. 1981. The spatial distribution of hyaluronic acid and mesenchymal condensation in the embryonic chick wing. Dev Biol 84:102-120.
85. Snow HE, Riccio LM, Mjaatvedt CH, Hoffman S, Capehart AA. 2005. Versican expression during skeletal/joint morphogenesis and patterning of muscle and nerve in the embryonic mouse limb. Anat Rec A Discov Mol Cell Evol Biol 282:95-105.
86. Soderstrom M, Bohling T, Ekfors T, Nelimarkka L, Aro HT, Vuorio E. 2002. Molecular profiling of human chondrosarcomas for matrix production and cancer markers. Int J Cancer 100:144-151.
87. Spitz F, Duboule D. 2001. The art of making a joint. Science 291:1713-1714.
88. Storm EE, Huynh TV, Copeland NG, Jenkins NA, Kingsley DM, Lee SJ. 1994. Limb alterations in brachypodism mice due to mutations in a new member of the TGF beta-superfamily. Nature 368:639-643.
89. Storm EE, Kingsley DM. 1996. Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 122:3969-3979.
90. Storm EE, Kingsley DM. 1999. GDF5 coordinates bone and joint formation during digit development. Dev Biol 209:11-27.
91. Suzuki T, Hasso SM, Fallon JF. 2008. Unique SMAD1/5/8 activity at the phalanx-forming region determines digit identity. Proc Natl Acad Sci USA 105: 4185-4190.
92. Sun X, Mariani FV, Martin GR. 2002. Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418:501-508.
93. 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.
94. Tanaka H, Murphy CL, Murphy C, Kimura M, Kawai S, Polak JM. 2004. Chondrogenic differentiation of murine embryonic stem cells: effects of culture conditions and dexamethasone. J Cell Biochem 93:454-462.
95. Tew SR, Li Y, Pothacharoen P, Tweats LM, Hawkins RE, Hardingham TE. 2005. Retroviral transduction with SOX9 enhances re-expression of the chondrocyte phenotype in passaged osteoarthritic human articular chondrocytes. Osteoarthritis Cartilage 13:80-89.
96. Thorogood PV, Hinchliffe JR. 1975. An analysis of the condensation process during chondrogenesis in the embryonic chick hind limb. J Embryol Exp Morph 33:581-606.
97. Toole BP. 1972. Hyaluronate turnover during chondrogenesis in the developing chick limb and axial skeleton. Dev Biol 29:321-329.
98. Von der Mark K, Von der Mark H, Gay S. 1976. Study of differential collagen synthesis during development of the chick embryo by immunofluoresence. II. Localization of type I and type II collagen during long bone development. Dev Biol 53: 153-170.
99. Ward AC, Dowthwaite GP, Pitsillides AA. 1999. Hyaluronan in joint cavitation. Biochem Soc Trans 27:128-135.
100. Wilson DJ. 1986. Development of avascularity during cartilage differentiation in the embryonic limb: an exclusion model. Differentiation 30:183-187.
101. Wood A, Ashhurst DE, Corbett A, Thorogood P. 1991. The transient expression of type II collagen at tissue interfaces during mammalian craniofacial development. Development 111:955-968.
102. Wright E, Hargrave MR, Christiansen J, Cooper L, Kun J, Evans T, Gangadharan U, Greenfield A, Koopman P. 1995. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nat Genet 9:15-20.
103. Yano F, Kugimiya F, Ohba S, Ikeda T, Chikuda H, Ogasawara T, Ogata N, Takato T, Nakamura K, Kawaguchi H, Chung UI. 2005. The canonical Wnt signaling pathway promotes chondrocyte differentiation in a Sox9-dependent manner. Biochem Biophys Res Commun 333:1300-1308.
104. Yin M, Pacifici M. 2001. Vascular regression is required for mesenchymal condensation and chondrogenesis in the developing limb. Dev Dyn 222:522-533.
105. Zhao Q, Eberspaecher H, Lefebvre V, De Crombrugghe B. 1997. Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev Dyn 209:377-386.
106. Zhu Y, Oganesian A, Keene DR, Sandell LJ. 1999. Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondrogenic tissue and binds to TGF-β1 and BMP-2. J Cell Biol 144:1069-1080.
107. zur Nieden NI, Kempka G, Rancourt DE, Ahr HJ. 2005. Induction of Chondro-, osteo- and adipogenesis in embryonic stem cells by bone morphogenetic protein-2: effect of cofactors on differentiating lineages. BMC Dev Biol 5:1-15.