Retinoic acid receptor α function in vertebrate limb skeletogenesis: A modulator of chondrogenesis

Journal of Cell Biology

Volumn 136, Issue 2, 1997, Pages 445-457

  Cash, David E ^a   Bock, Cheryl B ^a   Schughart, Klaus ^b   Linney, Elwood ^a   Michael Underhill, T ^c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CHONDROGENESIS; GENE EXPRESSION REGULATION; GENE TARGETING; GROWTH REGULATION; LIMB DEVELOPMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TRANSGENE; VERTEBRATE;

ANIMALS; BONE AND BONES; CARTILAGE; CELL DIFFERENTIATION; CULTURE TECHNIQUES; EXTREMITIES; FEMALE; GENE EXPRESSION; LIMB BUD; LIMB DEFORMITIES, CONGENITAL; MALE; MESODERM; MICE; MICE, TRANSGENIC; OSTEOGENESIS; RECEPTORS, RETINOIC ACID;

ANIMALIA; MAMMALIA; MUS MUSCULUS; VERTEBRATA;

EID: 0031046482     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.136.2.445     Document Type: Article

References (64)

1. Ahrens, P.B., M. Solursh, and R.S. Reiter. 1977. Stage related capacity for limb chondrogenesis in cell culture. Dev. Biol. 60:69-82.
2. Balkan, W., M. Colbert, C. Bock, and E. Linney. 1992a. Transgenic indicator mice for studying activated retinoic acid receptors during development. Proc. Natl Acad. Sci. USA. 89:3347-3351.
3. Balkan, W., G.K. Klintworth, C.B. Bock, and E. Linney. 1992b. Transgenic mice expressing a constitutively active retinoic acid receptor in the lens exhibit ocular defects. Dev. Biol. 151:622-625.
4. Barth, J., and R. Ivarie. 1994. Enhanced detection of low abundance transcripts in early stage quail embryos by a modified nonradioactive whole mount in situ hybridization technique. Biotechniques. 17:326-327.
5. Boylan, J.F., D. Lohnes, R. Taneja, P. Chambon, and L. Gudas. 1993. Loss of retinoic acid receptor γ function in F9 cells by gene disruption results in aberrant Hoxa-1 expression and differentiation upon retinoic acid treatment. Proc. Natl. Acad. Sci. USA. 90:9601-9605.
6. Boylan, J.F., T. Lufkin, C.C. Achkar, R. Taneja, P. Chambon, and L.J. Gudas. 1995. Targeted disruption of retinoic acid receptor α (RARα) and retinoic acid receptor γ (RARγ) results in receptor-specific alterations in retinoic acid-mediated differentiation and retinoic acid metabolism. Mol. Cell. Biol. 15:843-851.
7. Chambon, P. 1994. The retinoid signaling pathway: molecular and genetic analyses. Semin. Cell Biol. 5:115-125.
8. Conlon, R.A., and J. Rossant. 1992. Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development (Camb.). 116:357-368.
9. Dollé, P., J.-C. Izpisua-Belmonte, H. Falkenstein, A. Renucci, and D. Duboule. 1989a. Coordinate expression of the murine Hox-5 complex homeobox-containing genes during limb pattern formation. Nature (Lond.). 342:767-772,
10. Dollé, P., E. Ruberte, P. Kastner, M. Petkovich, C.M. Stoner, L.J. Gudas, and P. Chambon. 1989b. Differential expression of genes encoding α, β, and γ retinoic acid receptors and CRABP in the developing limbs of the mouse. Nature (Lond.). 342:702-705.
11. Dollé, P., E. Ruberte, P. Leroy, G. Morriss-Kay, and P. Chambon. 1990. Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development (Camb.). 110:1133-1151.
12. Dollé, P., V. Fraulob, P. Kastner, and P. Chambon. 1994. Developmental expression of murine retinoid X receptor (RXR) genes. Mech. Dev. 45:91-104.
13. Eckhardt, K., and G. Schmitt. 1994. A retinoic receptor α antagonist counter-acts retinoid teratogenicity in vitro and reduced incidence and/or severity of malformations in vivo. Toxicol. Lett. (Amst.). 70:299-308.
14. Elmazar, M.M.A., U. Reichert, B. Shroot, and H. Nau. 1996. Pattern of retinoid-induced teratogenic effects: possible relationship with relative selectivity for nuclear retinoid receptors RARα. RARβ, and RAR-γ. Teratology. 53: 158-167.
15. Giguère, V. 1994. Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endo. Rev. 15:61-79.
16. Jiang, H., M. Gyda III, D.C. Harnish, R.A. Chandraratna, K.J. Soprano, D.M. Kochhar, and D.R. Soprano. 1994. Teratogenesis by retinoic acid analogs positively correlates with elevation of retinoic acid receptor-β2 mRNA levels in treated embyros. Teratology. 50:38-43.
17. Kastner, P., J.M. Grondona, M. Mark, A. Gansmuller, M. LeMeur, D. Decimo, J.-L. Vonesch, P. Dollé, and P. Chambon. 1994. Genetic analysis of RXRα developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell. 78:987-1003.
18. Kochhar, D.M. 1973. Limb development in mouse embyros. I. Analysis of teratogenic effects of retinoic acid. Teratology. 7:289-295.
19. Kochhar, D.M., and M.B. Aydelotte. 1974. Susceptible stages and abnormal morphogenesis in the developing mouse limb, analysed in organ culture after transplacental exposure to vitamin A (retinoic acid). J. Embryol. Exp. Morph. 31:721-734.
20. Krust, A., P. Kastner, M. Petkovich, A. Zelent, and P. Chambon. 1989. A third human retinoic acid receptor, hRAR-γ. Proc. Natl. Acad. Sci. USA. 86:5310-5314.
21. Kwasigroch, T.E., and D.M. Kochhar. 1980. Production of congenital limb defects with retinoic acid: phenomenological evidence of progressive differentiation during limb morphogenesis. Anal. Embryol. 161:105-113.
22. Kwasigroch, T.E., J.F. Vannoy, J.K. Church, and R.G. Skalko. 1986. Retinoic acid enhances and depresses in vitro development of cartilaginous bone anlagen in embryonic mouse limbs. In Vitro Cell. Dev. Biol. 22:150-156.
23. Langsten, A.W., and L.J. Gudas. 1992. Identification of a retinoic acid responsive element 3′ of the murine homeobox gene Hox-1.6. Mech. Dev. 38:217-228.
24. Leid, M., P. Kastner, and P. Chambon. 1992a. Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem. Sci. 17:427-433.
25. Leid, M., P. Kastner, R. Lyons, H. Nakshatri, M. Saunders, T. Zacharewski, J.-Y. Chen, A. Staub, J.-M. Garnier, S. Mader, and P. Chambon. 1992b. Purification, cloning, and RXR identity of the HeLa Cell factor with which RAR or TR heterodimerizes to bind target sequences efficiently. Cell 68: 377-395.
26. Lev, R., and S.S. Spicer. 1964. Specific staining of sulphate groups with alcian blue at low pH. J. Histochem. Cytochem. 12:309.
27. Lewis, C.A., R.M. Pratt, J.P. Pennypacker, and J.R. Hassell. 1978. Inhibition of limb chondrogenesis in vitro by vitamin A. Dev. Biol. 64:31-47.
28. Li, E., H.M. Sucov, K.-F. Lee, R.M. Evans, and R. Jaenisch. 1993. Normal development and growth of mice carrying a targeted disruption of the α1 retinoic acid receptor gene. Proc. Natl. Acad. Sci. USA. 90:1590-1594.
29. Linney, E. 1992. Retinoic acid receptors: transcription factors modulating gene regulation, development and differentiation. In Current Topics in Developmental Biology. R.A. Pedersen, editor. Academic Press, San Diego. 309-350.
30. Lohnes, D., P. Kastner, A. Dierich, M. Mark, M. LeMeur, and P. Chambon. 1993. Function of retinoic acid receptor γ in the mouse. Cell. 73:643-658.
31. Lohnes, D., M. Mark, C. Mendelsohn, P. Dollé, A. Dierich, P. Gorry, A. Gansmuller, and P. Chambon. 1994. Function of the retinoic acid receptors (RARs) during development. (I) Craniofacial and skeletal abnormalities in RAR double mutants. Development (Camb.). 120:2723-2748.
32. Lufkin, T., D. Lohnes, M. Mark, A. Dierich, P. Gorry, M.-P. Gaub, M. LeMeur, and P. Chambon. 1993. High postnatal lethality and testis degeneration in retinoic acid receptor α mutant mice. Proc. Natl. Acad. Sci. USA. 90:7225-7229.
33. Luo, J., P. Pasceri, R.A. Conlon, J. Rossant, and V. Giguère. 1995. Mice lacking all isoforms of retinoic acid receptor β develop normally and are susceptible to the teratogenic effects of retinoic acid. Mech. Dev. 53:61-71.
34. Marshall, H., M. Studer, H. Popperl, S. Aparicio, A. Kuroiwa, S. Brenner, and R. Krumlauf. 1994. A conserved retinoic acid reponse element required for early expression of the homeobox gene Hoxb-1. Nature (Lond.). 370:567-571.
35. McLeod, M.J. 1980. Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red s. Teratology. 22:299-301.
36. Mendelsohn, C., E. Ruberte, M. LeMeur, G. Morriss-Kay, and P. Chambon. 1991. Developmental analysis of the retinoic acid-inducible RAR-β2 promoter in transgenic animals. Development (Camb.). 113:723-734.
37. Mendelsohn, C., E. Ruberte, and P. Chambon. 1992. Retinoid receptors in vertebrate limb development. Dev. Biol. 152:50-61.
38. Mendelsohn, C., D. Lohnes, D. Decimo, T. Lufkin, M. LeMeur, P. Chambon, and M. Mark. 1994a. Function of the retinoic acid receptors (RARs) during development. (II) Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development (Camb.). 120:2749-2771.
39. Mendelsohn, C., M. Mark, P. Dollé, A. Dierich, M.P. Gaub, A. Krust, C. Lampron, and P. Chambon. 1994b. Retinoic acid receptor β2 (RARβ2) null mutant mice appear normal. Dev. Biol. 166:246-258.
40. Niswander, L., C. Tickle, A. Vogel, I. Booth, and G.R. Martin. 1993. FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell. 75:579-587.
41. Niswander, L., S. Jeffery, G.R. Martin, and C. Tickle. 1994. A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature (Lond.). 371:609-612.
42. Popperl, H., and M.S. Featherstone. 1993. Identification of a retinoic acid response element upstream of the murine HOX-4.2 gene. Mol Cell. Biol. 13: 257-265.
43. Riddle, R.D., R.L. Johnson, E. Laufer, and C. Tabin. 1993. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 75:1401-1416.
44. Ruberte, E., P. Dollé, A. Krust, A. Zelent, G. Morriss-Kay, and P. Chambon. 1990. Specific spatial and temporal distribution of retinoic acid receptor γ transcripts during mouse embryogenesis. Development (Camb.). 108:213-222.
45. Ruberte, E., P. Dollé, P. Chambon, and G. Morriss-Kay. 1991. Retinoic acid receptors and cellular retinoid binding proteins. II. Their differential pattern of transcription during early morphogenesis in mouse embryos. Development (Camb.). 111:45-60.
46. Ruberte, E., V. Friederich, P. Chambon, and G. Morriss-Kay. 1993. Retinoic acid receptors and cellular retinoid binding proteins. III. Their differential transcript distribution during mouse nervous system development. Development (Camb.). 118:267-282.
47. Schughart, K., C.J. Bieberich, R. Eid, and F.H. Ruddle. 1991. A regulatory region from the mouse Hox-2.2 promoter directs gene expression into developing limbs. Development (Camb.). 112:807-811.
48. Shenefelt, R.E: 1972. Morphogenesis of malformations in hamsters caused by retinoic acid: relation to dose and stage at treatment. Teratology. 5:103-118.
49. Smith, S.M., I.J. Kirstein, Z.-S. Wang, J.F. Fallon, J. Kelley, and J. Bradshaw-Rouse. 1995. Differential expression of retinoic acid receptor-β isoforms during chick limb ontogeny. Dev. Dyn. 202:54-66.
50. Solursh, M., and S. Meier. 1973. The selective inhibition of mucopolysaccharide synthesis by vitamin A treatment of cultured chick embryo chondrocytes. Calcif. Tissue Res. 13:131-142.
51. Sucov, H.M., E. Dyson, C.L. Gumeringer, J. Price, K.R. Chien, and R.M. Evans. 1994. RXR α mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev. 8:1007-1018.
52. Sucov, H.M., J.C. Izpisua Belamonte, Y. Ganan, and R.M. Evans. 1995. Mouse embyros lacking RXR-α are resistant to retinoic-acid-induced limb defects. Development (Camb.). 121:3997-4003.
53. Sulik, K.K., and D.B. Dehart. 1988. Retinoic-acid-induced limb malformations resulting from apical ectodermal ridge cell death. Teratology. 37:527-537.
54. Summerbell, D. 1983. The effect of local application of retinoic acid to the anterior margin of the developing chick limb. J. Embryol. Exp. Morph. 78:269-289.
55. Tabin, C.J. 1991. Retinoids, homeoboxes, and growth factors: toward molecular models for limb development. Cell. 66:199-217.
56. Tickle, C., B.M. Alberts, L. Wolpert, and J. Lee. 1982. Local application of retinoic acid to the limb bud mimics the pattern of chick wing development. Nature (Lond.). 296:564-565.
57. Tickle, C., J. Lee, and G. Eichele. 1985. A quantitative analysis of the effect of all-trans-retinoic acid on the pattern of chick wing development. Dev. Biol. 109:82-95.
58. Tickle, C., A. Crawley, and J. Farrar. 1989. Retinoic acid application to chick wing buds leads to a dose-dependent reorganization of the apical ectodermal ridge that is mediated by the mesenchyme. Development (Camb.). 106:691-705.
59. Underhill, T.M., L.E. Kotch, and E. Linney. 1995. Retinoids and mouse embryonic development. Vitam. Horm. 51:403-457.
60. Von Schroeder, H.P., Y. Hasimoto, and J.N.M. Heersche. 1994. The effects of natural and synthetic retinoids on the differentiation of RCJ C5.18 chondrogenic cells. Teratology. 50:54-62.
61. White, J.A., M.B. Boffa, B. Jones, and M. Petkovich. 1994. A zebrafish retinoic acid receptor expressed in the regenerating caudal fin. Development (Camb.). 120:1861-1872.
62. Yu, V.C., C. Delsert, B. Andersen, J.M. Holloway, O.V. Devary, A.M. Naar, S.Y. Kim, J.-M. Boutin, C.K. Glass, and M.G. Rosenfeld. 1991. RXRβ: a coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell. 67:1251-1266.
63. Zelent, A., M. Krust, M. Petkovich, P. Kastner, and P. Chambon. 1989. Cloning of murine α and β retinoic acid receptors and a novel receptor γ predominantly expressed in skin. Nature (Lond.). 339:714-717.
64. Zimmerman, B., and D. Tsambos. 1985. Evaluation of the sensitive step of inhibition of chondrogenesis by retinoids in limb mesenchymal cells in vitro. Cell Diff. 17:95-103.