Retinoids regulate the anterior expression boundaries of 5′ Hoxb genes in posterior hindbrain

EMBO Journal

Volumn 22, Issue 2, 2003, Pages 262-269

  Oosterveen, Tony ^c   Niederreither, Karen ^a,b   Dollé, Pascal ^a   Chambon, Pierre ^a   Meijlink, Frits ^c   Deschamps, Jacqueline ^c  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c NONE

Author keywords

Mouse Hox genes; Posterior hindbrain patterning; Retinoic acid response; Transcriptional regulation

Indexed keywords

GENE PRODUCT; OXIDOREDUCTASE; RETINAL; RETINAL DEHYDROGENASE; RETINOIC ACID DERIVATIVE; RETINOID DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENE HOXB5; GENE HOXB6; GENE HOXB8; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REPORTER GENE; RHOMBENCEPHALON; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SPINAL CORD; TRANSCRIPTION REGULATION; TRANSGENE;

5' FLANKING REGION; ALDEHYDE OXIDOREDUCTASES; ANIMALS; CENTRAL NERVOUS SYSTEM; EMBRYO; EMBRYONIC STRUCTURES; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; GENES, REPORTER; HOMEODOMAIN PROTEINS; HUMANS; IN SITU HYBRIDIZATION; MICE; MORPHOGENESIS; MULTIGENE FAMILY; RESPONSE ELEMENTS; RETINAL DEHYDROGENASE; RETINOIDS; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; TRANSGENES; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO; MAMMALIA;

EID: 0037439084     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg029     Document Type: Article

References (45)

1. Berggren, K., McCaffery, K., Drager, U. and Forehand, C.J. (1999) Differential distribution of retinoic acid synthesis in the chicken embryo as determined by immunolocalization of the retinoic acid synthetic enzyme RALDH2. Dev. Biol., 210, 288-304.
2. Charité, J., de Graaff, W., Vogels, R., Meijlink, F. and Deschamps, J. (1995) Regulation of the Hoxb-8 gene: synergism between multimerized cis-acting elements increases responsiveness to positional information. Dev. Biol., 171, 294-305.
3. Charité, J., de Graaff, W., Consten, D., Reijnen, M.J., Korving, J. and Deschamps, J. (1998) Transducing positional information to the Hox genes: critical interaction of cdx gene products with position-sensitive regulatory elements. Development, 125, 4349-4358.
4. Conlon, R.A. and Rossant, J. (1992) Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development, 116, 357-368.
5. Deschamps, J., van den Akker, E., Forlani, S., de Graaff, W., Oosterveen, T., Roelen, B. and Roelfsema, J. (1999) Initiation, establishment and maintenance of Hox gene expression patterns in the mouse. Int. J. Dev. Biol., 43, 635-650.
6. Dupé, V. and Lumsden, A. (2001) Hindbrain patterning involves graded responses to retinoic acid signalling. Development, 128, 2199-2208.
7. Eid, R., Koseki, H. and Schughart, K. (1993) Analysis of lacZ reporter genes in transgenic embryos suggests the presence of several cisacting regulatory elements in the murine Hoxb-6 gene. Dev. Dyn., 196, 205-216.
8. Folkers, G.E., van der Burg, B. and van der Saag, P.T. (1998) Promoter architecture, cofactors and orphan receptors contribute to cell-specific activation of the retinoic acid receptor β2 promoter. J. Biol. Chem., 273, 32200-32212.
9. Gavalas, A., Studer, M., Lumsden, A., Rijli, F.M., Krumlauf, R. and Chambon, P. (1998) Hoxal and Hoxbl synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development, 125, 1123-1136.
10. Gavalas, A. and Krumlauf, R. (2000) Retinoid signalling and hindbrain patterning. Curr. Opin. Genet. Dev., 10, 380-386.
11. Gould, A., Itasaki, N. and Krumlauf, R. (1998) Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron, 21, 39-51.
12. Greer, J.M., Puetz, J., Thomas, K.R. and Capecchi, M.R. (2000) Maintenance of functional equivalence during paralogous Hox gene evolution. Nature, 403, 661-665.
13. Haramis, A.G., Brown, J.M. and Zeller, R. (1995) The limb deformity mutation disrupts the SHH/FGF-4 feedback loop and regulation of 5′ HoxD genes during limb pattern formation. Development, 121, 4237-4245.
14. Hogan, B., Beddington R., Constantini, F. and Lacy, E. (1994) Manipulating the Mouse Embryo. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
15. Huang, D., Chen, S.W., Langston, A.W. and Gudas, L.J. (1998) A conserved retinoic acid responsive element in the murine Hoxb-1 gene is required for expression in the developing gut. Development, 125, 3235-3246.
16. Kmita, M., van der Hoeven, F., Zákány, J., Krumlauf, R. and Duboule, D. (2000) Mechanisms of Hox gene colinearity: transposition of the anterior Hoxb1 gene into the posterior HoxD complex. Genes Dev., 14, 198-211.
17. Kondo, T. and Duboule, D. (1999) Breaking colinearity in the mouse HoxD complex. Cell, 97, 407-417.
18. Krumlauf, R. (1994) Hox genes in vertebrate development. Cell, 78, 191-201.
19. Krumlauf, R., Holland, P.W., McVey, J.H. and Hogan, B.L. (1987) Developmental and spatial patterns of expression of the mouse homeobox gene, Hox2.1. Development, 99, 603-617.
20. Lu, H.C., Revelli, J.P., Goering, L., Thaller, C. and Eichele, G. (1997) Retinoid signaling is required for the establishment of a ZPA and for the expression of Hoxb-8, a mediator of ZPA formation. Development, 124, 1643-1651.
21. Maden, M., Sonneveld, E., van der Saag, P.T. and Gale, E. (1998) The distribution of endogenous retinoic acid in the chick embryo: implications for developmental mechanisms. Development, 125, 4133-4144.
22. Mader, S., Leroy, P., Chen, J.Y. and Chambon, P. (1993) Multiple parameters control the selectivity of nuclear receptors for their response elements. Selectivity and promiscuity in response element recognition by retinoic acid receptors and retinoid X receptors. J. Biol. Chem., 268, 591-600.
23. Manzanares, M., Bel-Vialar, S., Ariza-McNaughton, L., Ferretti, E., Marshall, H., Maconochie, M.M., Blasi, F. and Krumlauf, R (2001) Independent regulation of initiation and maintenance phases of Hoxa3 expression in the vertebrate hindbrain involve auto- and cross-regulatory mechanisms. Development, 128, 3595-3607.
24. Marshall, H., Studer, M., Popperi, H., Aparicio, S., Kuroiwa, A., Brenner, S. and Krumlauf, R. (1994) A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1, Nature, 370, 567-571.
25. Nierderreither, K., McCaffery, P., Drager, U.C., Chambon, P. and Dolle, P. (1997) Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech. Dev., 62, 67-78.
26. Niederreither, K., Subbarayan, V., Dolle, P. and Chambon, P. (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet., 21, 444-448.
27. Niederreither, K., Vermot, J., Schuhbaur, B., Chambon, P. and Dolle, P. (2000) Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development, 127, 75-85.
28. Niederreither, K., Vermot, J., Messaddeq, N., Schuhbaur, B., Chambon, P. and Dolle, P. (2001) Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development, 128, 1019-1031.
29. Ogura, T. and Evans, R.M. (1995) A retinoic acid-triggered cascade of HOXB1 gene activation. Proc. Natl Acad. Sci. USA, 92, 387-391.
30. Pöpperl, H., Bienz, M., Studer, M., Chan, S.-K., Aparicio, S., Brenner, S., Mann, R.S. and Krumlauf, R. (1995) Segmental expression of Hoxb1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell, 81, 1031-1042.
31. Schughart, K., Utset, M.F., Awgulewitsch, A. and Ruddle, F.H. (1988) Structure and expression of Hox-2.2, a murine homeobox-containing gene. Proc. Natl Acad. Sci. USA, 85, 5582-5586.
32. Seitanidou, T., Schneider-Maunoury, S., Desmarquet, C., Wilkinson, D.G. and Charnay, P. (1997) Krox-20 is a key regulator of rhombomere-specific gene expression in the developing hindbrain. Mech. Dev., 65, 31-42.
33. Sharpe, J., Nonchev, S., Gould, A., Whiting, J. and Krumlauf, R. (1998) Selectivity, sharing and competitive interactions in the regulation of Hoxb genes. EMBO J., 17, 1788-1798.
34. Shen, S., van den Brink, C., Kruijer, W. and van der Saag, P.T. (1992) Embryonic stem cells stably transfected with mRARβ2-lacZ exhibit specific expression in chimeric embryos. Int. J. Dev. Biol., 36, 465-476.
35. Simeone, A., Acampora, D., Arcioni, L., Andrews, P.W., Boncinelli, E. and Mavilio, F. (1990) Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Nature, 346, 763-766.
36. Studer, M., Popperl, H., Marshall, H., Kuroiwa, A. and Krumlauf, R. (1994) Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1. Science, 265, 1728-1732.
37. Swindell, E., Thaller, C., Sockanathan, S., Petkovitch, M., Jessel, T. and Eichele, G. (1999) Complementary domains of retinoic acid production and degradation in the early chick embryo. Dev. Biol., 216, 282-296.
38. Valarché, I., de Graaff, W. and Deschamps, J. (1997) A 3′ remote control region is a candidate to modulate Hoxb-8 expression boundaries. Int. J. Dev, Biol., 41, 705-714.
39. van den Akker, E., Reijnen, M., Korving, J., Brouwer, A., Meijlink, F. and Deschamps, J. (1999) Targeted inactivation of Hoxb8 affects survival of a spinal ganglion and causes aberrant limb reflexes. Mech. Dev., 89, 103-114.
40. van den Akker, E., Forlani, S., Chawengsaksophak, K., de Graaff, W., Beck, F., Meyer, B.I. and Deschamps, J. (2002) Cdx1 and Cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development, 129, 2181-2193.
41. van der Hoeven, F., Zákány, J. and Duboule, D. (1996) Gene transpositions in the HoxD complex reveal a hierarchy of regulatory controls. Cell, 85, 1025-1035.
42. Vogels, R., Charité, J., de Graaff, W. and Deschamps, J. (1993) Proximal cis-acting elements cooperate to set Hoxb-7 (Hox-2.3) expression boundaries in transgenic mice. Development, 118, 71-82.
43. Wilkinson, D.G., Bhatt, S., Chavrier, P., Bravo, R. and Charnay, P. (1989) Segment-specific expression of a zinc-finger gene in the developing nervous system of the mouse. Nature, 337, 461-464.
44. Wilkinson, D.G. (1992) Whole mount in situ hybridization of vertebrate embryos. In Wilkinson, D.G. (ed.), In Situ Hybridization. IRL Press at Oxford University Press, pp. 75-83.
45. Zákány, J., Gerard, M., Favier, B. and Duboule, D. (1997) Deletion of a HoxD enhancer induces transcriptional heterochrony leading to transposition of the sacrum. EMBO J., 16, 4393-4402.