Deletion of a HoxD enhancer induces transcriptional heterochrony leading to transposition of the sacrum

EMBO Journal

Volumn 16, Issue 14, 1997, Pages 4393-4402

  Zákány, József ^a   Gérard, Matthieu ^a,b   Favier, Bertrand ^c,d   Duboule, Denis ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b NATIONAL CANCER INSTITUTE   (United States)

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

^d INSTITUT ALBERT BONNIOT   (France)

Author keywords

Cre; Gene targeting; HoxD complex; LoxP; Mouse development; Regulatory mutation

Indexed keywords

DNA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA TRANSPOSITION; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; FETUS; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; LIMB DEVELOPMENT; MOUSE; MUTAGENESIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SACRUM; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VERTEBRA;

ANIMALS; CELL LINE; ENHANCER ELEMENTS (GENETICS); FORELIMB; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; MICE, TRANSGENIC; MUTAGENESIS, INSERTIONAL; SACRUM; SEQUENCE DELETION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 0342872062     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.14.4393     Document Type: Article

References (49)

1. Alkema, M.J., van der Lugt, N.M., Bobeldijk, R.C., Berns, A. and van Lohuizen, M. (1995) Transformation of axial skeleton due to overexpression of bmi-1 in transgenic mice. Nature, 374, 724-727.
2. Alkema, M.J., Bronk, M., Verhoeven, E. Otte, A., van't Veer, L.J., Berns, A. and van Lohuizen, M. (1997) Identification of Bmi-1 interacting proteins as constituents of a multimeric mammalian Polycomb complex. Genes Dev., 11, 226-240.
3. Burke, A.C., Nelson, C.E., Morgan, B.A. and Tabin, C. (1995) Hox genes and the evolution of vertebrate axial morphology. Development, 121, 333-346.
4. Carroll, S.B. (1995) Homeotic genes and the evolution of arthropods and chordates. Nature, 376, 479-485.
5. Castelli-Gair, J. and Akam, M. (1995) How the Hox gene Ubx specifies two different segments: the significance of spatial and temporal regulation within metamers. Development, 121, 2973-2982.
6. Coates, M. (1994) The origin of vertebrate limbs. Development (Suppl.), 169-180.
7. Davis, A.P. and Capecchi, M.R. (1994) Axial homeosis and appendicular skeleton defects in mice with a targeted disruption of Hoxd-11. Development, 120, 2187-2198.
8. Davis, A.P. and Capecchi, M.R. (1996) A mutational analysis of the 5′ HoxD genes: dissection of genetic interactions during limb development in the mouse. Development, 122, 1175-1185.
9. Davis, A.P., Witte, D.P., Hsieh-Li, H.M., Potter, S.S. and Capecchi, M.R. (1995) Absence of radius and ulna in mice lacking Hoxa-11 and Hoxd-11. Nature, 375, 791-795.
10. Deschamps, J. and Wijgerde, M. (1993) Two phases in the establishment of HOX expression domains. Dev. Biol., 156, 473-480.
11. Doetschman, T.C., Eistetter, H., Katz, M. Schmidt, W. and Kemler, R. (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol., 87, 27-45.
12. Dollé, P. and Duboule, D. (1989) Two genes members of the Hox-5 complex show regional and cell type specific expression in limbs and gonads. EMBO J., 8, 1507-1515.
13. Dollé, P., Izpisúa-Belmonte, J.-C., Falkenstein, H., Renucci, A. and Duboule, D. (1989) Coordinate expression of murine Hox-5 complex homeobox-containing genes during limb pattern formation. Nature, 342, 767-772.
14. Dollé, P., Izpisúa-Belmonte, J.-C., Boncinelli, E. and Duboule, D. (1991) The Hox-4.8 gene is localised at the 5′ extremity of the HOX-4 complex and is expressed in the most posterior parts of the body during development. Mech. Dev., 36, 3-14.
15. Duboule, D. (1992) The vertebrate limb; a model system to study the Hox/HOM gene network during development and evolution. BioEssays, 14, 375-389.
16. 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. Development (Suppl.), 135-142.
17. Dupé, V., Davenne, M., Brocard, J., Dollé, P., Mark, M. Dierich, A., Chambon, P. and Rijli, F. (1997) In vivo functional analysis of the Hoxa-1 3′ retinoic acid response element (3′ RARE). Development, 124, 399-410.
18. Favier, B., Le Meur, M., Chambon, P. and Dollé, P. (1995) Axial skeleton homeosis and forelimb malformations in Hoxd-11 mutant mice. Proc. Natl Acad. Sci. USA, 92, 310-314.
19. Favier, B., Rijli, F.M., Fromental-Ramain, C., Fraulob, V., Chambon, P. and Dollé, P. (1996) Functional cooperation between the non-paralogous genes Hoxa-10 and Hoxd-11 in the developing forelimb and axial skeleton. Development, 122, 449-460.
20. Fromental-Ramain, C., Warot, X., Lakkaraju, S., Favier, B., Haack, H., Birling, C., Dierich, A., Dollé, P. and Chambon, P. (1996) Specific and redundant functions of the paralogous Hoxa-9 and Hoxd-9 genes in forelimb and axial skeleton patterning. Development, 122, 461-472.
21. Gaunt, S.J. (1994) Conservation in the Hox code during morphological evolution. Int. J. Dev. Biol., 38, 549-552.
22. Gaunt, S.J. and Strachan, L. (1994) Forward spreading in the establishment of a vertebrate Hox expression boundary: the expression domain separates into anterior and posterior zones, and the spread occurs across implanted glass barriers. Dev. Dynam., 199, 229-240.
23. Gaunt, S.J. and Strachan, L. (1996) Temporal colinearity in expression of anterior Hox genes in developing chick embryos. Dev. Dynam., 207, 270-280.
24. Gaunt, S.J., Miller, J.R., Powell, D.J. and Duboule, D. (1986) Homeobox gene expression in mouse embryos varies with position by the primitive streak stage. Nature, 324, 662-664.
25. Gérard, M., Duboule, D. and Zákány, J. (1993) Structure and activity of regulatory elements involved in the activation of the Hoxd-11 gene during late gastrulation. EMBO J., 12, 3539-3550.
26. Gérard, M., Chen, J.-Y., Gronemeyer, H., Chambon, P., Duboule, D. and Zákány, J. (1996) In vivo targeted mutagenesis of a regulatory element required for positioning the Hoxd-11 and Hoxd-10 expression boundaries. Genes Dev., 10, 2326-2334.
27. Gould, A., Morrison, A., Sproat, G., White, R.A.H. and Krumlauf, R. (1997) Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev., 11, 900-913.
28. Hérault, Y., Hraba-Renevey, S., van der Hoeven, F. and Duboule, D. (1996) Function of the Evx-2 gene in the morphogenesis of vertebrate limbs. EMBO J., 15, 6727-6738.
29. Izpisúa-Belmonte, J.-C., Falkenstein, H., Dollé, P., Renucci, A. and Duboule, D. (1991) Murine genes related to the Drosophila AbdB homeotic gene are sequentially expressed during development of the posterior part of the body. EMBO J., 10, 2279-2289.
30. Knittel, T., Kessel, M. and Gruss, P. (1995) A conserved enhancer of the human and murine Hoxa-7 gene specifies the anterior boundary of expression during embryonal development. Development, 121, 1077-1088.
31. Kondo, T., Dollé, P., Zákány, J. and Duboule, D (1996) Function of posterior HoxD genes in the morphogenesis of the anal sphincter. Development, 122, 2651-2659.
32. Krumlauf, R. (1994) Hox genes in vertebrate development. Cell, 78, 191-201.
33. Lessertisseur, J. and Saban, R. (1967) Squelette Axial. In Grassé, P.-P. (ed.), Traite de Zoologie. Masson et Cie, Paris, Vol. XVI, Fascicule I, pp. 584-1109.
34. Olson, E.N., Arnold, H.H., Rigby, P.W.J. and Wold, B.J. (1996) Know your neighbours: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell, 85, 1-4.
35. Rijli, F.M., Dollé, P. Fraulob, V., LeMeur, M. and Chambon, P. (1994) Insertion of a targeting construct in a Hoxd-10 allele can influence the control of Hoxd-9 expression. Dev. Dynam., 201, 366-377.
36. Shashikant, C.S. and Ruddle, F.H. (1996) Combinations of closely situated cis-acting elements determine tissue-specific patterns and anterior extent of early Hoxc-8 expression. Proc. Natl Acad. Sci. USA, 93, 12364-12369.
37. Small, K. and Potter, S.S. (1993) Homeotic transformations and limb defects in HoxA11 mutant mice. Genes Dev., 7, 2318-2328.
38. Studer, M., Lumsden, A., Arivza-Mc Naughton, L., Bradley, A. and Krumlauf, R. (1996) Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature, 384, 630-634.
39. Subramanian, V., Meyer, B.I. and Gruss, P. (1995) Disruption of the murine homeobox gene Cdx1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell, 83, 641-653.
40. Todd, W. (1922) Numerical significance in the thoracicolumbar vertebrae of the mammalia. Anat. Rec., 24, 261-286.
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. van der Lugt, N.M.T. et al. (1994) Posterior transformation, neurological abnormalities, and severe haematopoietic defects in mice with targeted deletion of the bmi-1 proto-oncogene. Genes Dev., 8, 757-769.
43. Vogels, R., Charite, 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.
44. Walters, M.C, Magis, W., Fiering, S., Eidemiller, J., Scalzo, D., Groudine, M. and Martin, D.I.K. (1996) Transcriptional enhancers act in cis to suppress position-effect variegation. Genes Dev., 10, 185-195.
45. Whiting, J., Marshall, H., Cook, M., Krumlauf, R., Rigby, P.W.J., Scott, D. and Allemann, R.K. (1991) Multiple spatially specific enhancers are required to reconstruct the pattern of Hox-2.6 gene expression. Genes Dev., 5, 2048-2059.
46. Yu, B.D., Hess, J.L., Horning, S.E., Brown, G.A. and Korsmeyer, S.J. (1995) Altered Hox expression and segmental identity in Mll-mutant mice. Nature, 378, 505-508.
47. Zákány, J. and Duboule, D. (1996) Synpolydactyly in mice with a targeted deficiency in the HoxD complex. Nature, 384, 69-71.
48. Zákány, J., Gérard, M., Favier, B., Potter, S.S. and Duboule, D. (1996) Functional equivalence and rescue among group 11 Hox gene products in vertebral patterning. Dev. Biol., 176, 325-328.
49. Zappavigna, V., Renucci, A., Izpisúa-Belmonte, J.-C., Urier, G., Peschle, C. and Duboule, D. (1991) Hox4 genes encode transcription factors with potential auto- and cross-regulatory capacities. EMBO J., 10, 4177-4187.