Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb

Developmental Cell

Volumn 6, Issue 3, 2004, Pages 411-422

  Yashiro, Kenta ^a,b   Zhao, Xianling ^a,b   Uehara, Masayuki ^a,b   Yamashita, Kimiyo ^a,b   Nishijima, Misae ^a,b   Nishino, Jinsuke ^a,b   Saijoh, Yukio ^a,b   Sakai, Yasuo ^a,b,c   Hamada, Hiroshi ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; RETINOIC ACID;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL FATE; CELL MATURATION; CELL TYPE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; IN SITU HYBRIDIZATION; LIMB DEFORMITY; LIMB DEVELOPMENT; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

ABNORMALITIES, DRUG-INDUCED; AGING; ALDEHYDE OXIDOREDUCTASES; ANIMALS; ANIMALS, NEWBORN; BODY PATTERNING; BROMODEOXYURIDINE; CARCINOMA; CELL DEATH; CELL DIFFERENTIATION; CELL LINE, TUMOR; CYTOCHROME P-450 ENZYME SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO; EMBRYONIC INDUCTION; EXTREMITIES; FEMALE; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTORS; GALACTOSIDES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIGH MOBILITY GROUP PROTEINS; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; INDOLES; LIMB BUD; MALE; MESODERM; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PREGNANCY; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFECTION; TRETINOIN;

EID: 1642287727     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(04)00062-0     Document Type: Article

References (60)

1. Abu-Abed S. Dolle P. Metzger D. Beckett B. Chambon P. Petkovich M. The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures Genes Dev. 15 2001 226-240
2. Abu-Abed S. MacLean G. Fraulob V. Chambon P. Petkovich M. Dolle P. Differential expression of the retinoic acid-metabolizing enzymes CYP26A1 and CYP26B1 during murine organogenesis Mech. Dev. 110 2002 173-177
3. Adams C.S. Horton W.E. Jr. Chondrocyte apoptosis increases with age in the articular cartilage of adult animals Anat. Rec. 250 1998 418-425
4. Binkley N. Krueger D. Hypervitaminosis A and bone Nutr. Rev. 58 2000 138-144
5. Bober E. Franz T. Arnold H.H. Gruss P. Tremblay P. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells Development 120 1994 603-612
6. Brockes J.P. Amphibian limb regeneration: rebuilding a complex structure Science 276 1997 81-87
7. Capdevila J. Tsukui T. Rodriquez Esteban C. Zappavigna V. Izpisua Belmonte J.C. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin Mol. Cell 4 1999 839-849
8. Compagni A. Logan M. Klein R. Adams R.H. Control of skeletal patterning by ephrinB1-EphB interactions Dev. Cell 5 2003 217-230
9. Conlon R.A. Retinoic acid and pattern formation in vertebrates Trends Genet. 11 1995 314-319
10. Corson L.B. Yamanaka Y. Lai K.M. Rossant J. Spatial and temporal patterns of ERK signaling during mouse embryogenesis Development 130 2003 4527-4537
11. Crawford K. Stocum D.L. Retinoic acid proximalizes level-specific properties responsible for intercalary regeneration in axolotl limbs Development 104 1988 703-712
12. Duboule, D. (1994). Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev. Suppl., 135-142.
13. Dudley A.T. Ros M.A. Tabin C.J. A re-examination of proximodistal patterning during vertebrate limb development Nature 418 2002 539-544
14. Fujii H. Sato T. Kaneko S. Gotoh O. Fujii-Kuriyama Y. Osawa K. Kato S. Hamada H. Metabolic inactivation of retinoic acid by a novel P450 differentially expressed in developing mouse embryos EMBO J. 16 1997 4163-4173
15. Gardiner D.M. Blumberg B. Komine Y. Bryant S.V. Regulation of HoxA expression in developing and regenerating axolotl limbs Development 121 1995 1731-1741
16. Hardy A. Richardson M.K. Francis-West P.H. Rodriguez C. Izpisua-Belmonte J.C. Duprez D. Wolpert L. Gene expression, polarising activity and skeletal patterning in reaggregated hind limb mesenchyme Development 121 1995 4329-4337
17. Hayamizu T.F. Bryant S.V. Reciprocal changes in Hox D13 and RAR-beta 2 expression in response to retinoic acid in chick limb buds Dev. Biol. 166 1994 123-132
18. Helms J. Thaller C. Eichele G. Relationship between retinoic acid and sonic hedgehog, two polarizing signals in the chick wing bud Development 120 1994 3267-3274
19. Kawakami Y. Rodriguez-Leon J. Koth C.M. Buscher D. Itoh T. Raya A. Ng J.K. Esteban C.R. Takahashi S. Henrique D. et al. MKP3 mediates the cellular response to FGF8 signalling in the vertebrate limb Nat. Cell Biol. 5 2003 513-519
20. Kochhar D.M. Limb development in mouse embryos. I. Analysis of teratogenic effects of retinoic acid Teratology 7 1973 289-298
21. Lammer E.J. Chen D.T. Hoar R.M. Agnish N.D. Benke P.J. Braun J.T. Curry C.J. Fernhoff P.M. Grix A.W. Jr. Lott I.T. et al. Retinoic acid embryopathy N. Engl. J. Med. 313 1985 837-841
22. MacLean G. Abu-Abed S. Dolle P. Tahayato A. Chambon P. Petkovich M. Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development Mech. Dev. 107 2001 195-201
23. Maden M. Vitamin A and pattern formation in the regenerating limb Nature 295 1982 672-675
24. Maden M. Heads or tails? Retinoic acid will decide Bioessays 21 1999 809-812
25. Martin P. Cockroft D. Culture of postimplantation mouse embryos In Sharpe P. Mason I. (Eds.), Methods in Molecular Biology: Molecular Embryology: Methods and Protocols 1999 7-22 Humana Press Inc Totowa, NJ
26. Mercader N. Leonardo E. Azpiazu N. Serrano A. Morata G. Martinez C. Torres M. Conserved regulation of proximodistal limb axis development by Meis1/Hth Nature 402 1999 425-429
27. Mercader N. Leonardo E. Piedra M.E. Martinez A.C. Ros M.A. Torres M. Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes Development 127 2000 3961-3970
28. Nagy, A., Gertsenstein, M., Vintersten, K., and Behringer, R. (2003). Manipulating the Mouse Embryo: A Laboratory Manual, 3rd edn (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
29. Nebert D.W. Russell D.W. Clinical importance of the cytochromes P450 Lancet 360 2002 1155-1162
30. Nelson C.E. Morgan B.A. Burke A.C. Laufer E. DiMambro E. Murtaugh L.C. Gonzales E. Tessarollo L. Parada L.F. Tabin C. Analysis of Hox gene expression in the chick limb bud Development 122 1996 1449-1466
31. Nelson D.R. A second CYP26 P450 in humans and zebrafish: CYP26B1 Arch. Biochem. Biophys. 371 1999 345-347
32. Niederreither K. Subbarayan V. Dolle P. Chambon P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development Nat. Genet. 21 1999 444-448
33. Niederreither K. Abu-Abed S. Schuhbaur B. Petkovich M. Chambon P. Dolle P. Genetic evidence that oxidative derivatives of retinoic acid are not involved in retinoid signaling during mouse development Nat. Genet. 31 2002a 84-88
34. Niederreither K. Vermot J. Schuhbaur B. Chambon P. Dolle P. Embryonic retinoic acid synthesis is required for forelimb growth and anteroposterior patterning in the mouse Development 129 2002b 3563-3574
35. Niswander L. Pattern formation: old models out on a limb Nat. Rev. Genet. 4 2003 133-143
36. Ornitz D.M. Marie P.J. FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease Genes Dev. 16 2002 1446-1465
37. Ray W.J. Bain G. Yao M. Gottlieb D.I. CYP26, a novel mammalian cytochrome P450, is induced by retinoic acid and defines a new family J. Biol. Chem. 272 1997 18702-18708
38. Ros M.A. Lyons G.E. Mackem S. Fallon J.F. Recombinant limbs as a model to study homeobox gene regulation during limb development Dev. Biol. 166 1994 59-72
39. Ross S.A. McCaffery P.J. Drager U.C. De Luca L.M. Retinoids in embryonal development Physiol. Rev. 80 2000 1021-1054
40. Rossant J. Zirngibl R. Cado D. Shago M. Giguere V. Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis Genes Dev. 5 1991 1333-1344
41. Rudnicki M.A. McBurney M.W. Cell culture methods and induction of differentiation of embryonal carcinoma cell lines In Robertson E.J. (Ed.), Teratocarcinomas and Embryonic Stem Cells: a Practical Approach 1987 19-49 IRL Press Limited Oxford
42. Sakai Y. Meno C. Fujii H. Nishino J. Shiratori H. Saijoh Y. Rossant J. Hamada H. The retinoic acid-inactivating enzyme CYP26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo Genes Dev. 15 2001 213-225
43. Sekiya I. Koopman P. Tsuji K. Mertin S. Harley V. Yamada Y. Shinomiya K. Niguji A. Noda M. Transcriptional suppression of Sox9 expression in chondrocytes by retinoic acid J. Cell. Biochem. 81 2001 71-78
44. Stadler H.S. Higgins K.M. Capecchi M.R. Loss of Eph-receptor expression correlates with loss of cell adhesion and chondrogenic capacity in Hoxa13 mutant limbs Development 128 2001 4177-4188
45. Summerbell D. Lewis J.H. Wolpert L. Positional information in chick limb morphogenesis Nature 244 1973 492-496
46. Sun X. Mariani F.V. Martin G.R. Functions of FGF signalling from the apical ectodermal ridge in limb development Nature 418 2002 501-508
47. Tahayato A. Dolle P. Petkovich M. Cyp26C1 encodes a novel retinoic acid-metabolizing enzyme expressed in the hindbrain, inner ear, first branchial arch and tooth buds during murine development Gene Expr. Patterns 3 2003 449-454
48. Tamura K. Yokouchi Y. Kuroiwa A. Ide H. Retinoic acid changes the proximodistal developmental competence and affinity of distal cells in the developing chick limb bud Dev. Biol. 188 1997 224-234
49. Thompson J.N. Howell J.M. Pitt G.A. McLaughlin C.I. The biological activity of retinoic acid in the domestic fowl and the effects of vitamin A deficiency on the chick embryo Br. J. Nutr. 23 1969 471-490
50. Tickle C. Patterning systems-from one end of the limb to the other Dev. Cell 4 2003 449-458
51. Vargesson N. Clarke J.D. Vincent K. Coles C. Wolpert L. Tickle C. Cell fate in the chick limb bud and relationship to gene expression Development 124 1997 1909-1918
52. Weston A.D. Rosen V. Chandraratna R.A. Underhill T.M. Regulation of skeletal progenitor differentiation by the BMP and retinoid signaling pathways J. Cell Biol. 148 2000 679-690
53. Weston A.D. Chandraratna R.A. Torchia J. Underhill T.M. Requirement for RAR-mediated gene repression in skeletal progenitor differentiation J. Cell Biol. 158 2002 39-51
54. White J.A. Guo Y.D. Baetz K. Beckett-Jones B. Bonasoro J. Hsu K.E. Dilworth F.J. Jones G. Petkovich M. Identification of the retinoic acid-inducible all-trans-retinoic acid 4-hydroxylase J. Biol. Chem. 271 1996 29922-29927
55. White J.A. Ramshaw H. Taimi M. Stangle W. Zhang A. Everingham S. Creighton S. Tam S.P. Jones G. Petkovich M. Identification of the human cytochrome P450, P450RAI-2, which is predominantly expressed in the adult cerebellum and is responsible for all-trans-retinoic acid metabolism Proc. Natl. Acad. Sci. USA 97 2000 6403-6408
56. Wilson J. Roth C. Warkany J. An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation Ame. J. Anat. 92 1953 189-217
57. Wolpert L. The French flag problem: a contribution to discussion on pattern formation and regulation In Waddington C.H. (Ed.), Towards a Theoretical Biology 1968 125-133 Edinburgh University Press Edinburgh
58. Wood H.B. Ward S.J. Morriss-Kay G.M. Effects of all-trans-retinoic acid on skeletal pattern, 5′HoxD gene expression, and RAR beta 2/beta 4 promoter activity in embryonic mouse limbs Dev. Genet. 19 1996 74-84
59. Wright E. Hargrave M.R. Christiansen J. Cooper L. Kun J. Evans T. Gangadharan U. Greenfield A. Koopman P. The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos Nat. Genet. 9 1995 15-20
60. Yashiro K. Saijoh Y. Sakuma R. Tada M. Tomita N. Amano K. Matsuda Y. Monden M. Okada S. Hamada H. Distinct transcriptional regulation and phylogenetic divergence of human LEFTY genes Genes Cells 5 2000 343-357