Cdx Protein Interaction with Hoxa5 Regulatory Sequences Contributes to Hoxa5 Regional Expression along the Axial Skeleton

REFERENCES

• Aubin, J., M. Lemieux, M. Tremblay, J. Bérard, and L. Jeannotte. 1997. Early postnatal lethality in Hoxa-5 mutant mice is attributable to respiratory tract defects. Dev. Biol. 192:432–445.
   PubMed Web of Science ®Google Scholar
• Aubin, J., M. Lemieux, M. Tremblay, R. R. Behringer, and L. Jeannotte. 1998. Transcriptional interferences at the Hoxa4/Hoxa5 locus: importance of correct Hoxa5 expression for the proper specification of the axial skeleton. Dev. Dyn. 212:141–156.
   PubMedGoogle Scholar
• Aubin, J., P. Chailler, D. Ménard, and L. Jeannotte. 1999. Loss of Hoxa5 gene function in mice perturbs intestinal maturation. Am. J. Physiol. 277:C965–C973.
   PubMedGoogle Scholar
• Aubin, J., and L. Jeannotte. 2001. Implication des gènes Hox dans les processus d'organogenèse chez les mammifères. Médecine/Science 17:54–62.
   Google Scholar
• Aubin, J., U. Déry, M. Lemieux, P. Chailler, and L. Jeannotte. 2002. Stomach regional specification requires Hoxa5-driven mesenchymal-epithelial signaling. Development 129:4075–4087.
   PubMed Web of Science ®Google Scholar
• Aubin, J., M. Lemieux, J. Moreau, J. Lapointe, and L. Jeannotte. 2002. Cooperation of Hoxa5 and Pax1 genes during formation of the pectoral girdle. Dev. Biol. 244:96–113.
   PubMedGoogle Scholar
• Behringer, R. R., D. A. Crotty, V. M. Tennyson, R. L. Brinster, R. D. Palmiter, and D. J. Wolgemuth. 1993. Sequences 5′ of the homeobox of the Hox-1.4 gene direct tissue-specific expression of lacZ during mouse development. Development 117:823–833.
   PubMedGoogle Scholar
• Béland, M., N. Pilon, M. Houle, K. Oh, J.-R. Sylvestre, P. Prinos, and D. Lohnes. 2004. Cdx1 autoregulation is governed by a novel Cdx1-LEF1 transcription complex. Mol. Cell. Biol. 24:5028–5038.
   PubMed Web of Science ®Google Scholar
• Bel-Vialar, S., N. Itasaki, and R. Krumlauf. 2002. Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 129:5103–5115.
   PubMedGoogle Scholar
• Bradshaw, M. S., C. S. Shashikant, H.-G. Belting, J. A. Bollekens, and F. H. Ruddle. 1996. A long-range regulatory element of Hoxc8 identified by using pClaster vector. Proc. Natl. Acad. Sci. USA. 93:2426–2430.
   PubMedGoogle Scholar
• Brend, T., J. Gilthorpe, D. Summerbell, and P. W. Rigby. 2003. Multiple levels of transcriptional and post-transcriptional regulation are required to define the domain of Hoxb4 expression. Development 130:2717–2728.
   PubMedGoogle Scholar
• Chambeyron, S., and W. A. Bickmore. 2004. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev. 18:1119–1130.
   PubMed Web of Science ®Google Scholar
• Charité, J., W. de Graaff, D. Consten, M. J. Reijnen, J. Korving, and J. Deschamps. 1998. Transducing positional information to the Hox genes: critical interaction of cdx gene products with position-sensitive regulatory elements. Development 125:4349–4358.
   PubMedGoogle Scholar
• Chawengsaksophak, K., R. James, V. E. Hammond, F. Kontgen, and F. Beck. 1997. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 386:84–87.
   PubMedGoogle Scholar
• Dony, C., and P. Gruss. 1987. Specific expression of the Hox1.3 homeobox gene in murine embryonic structures originating from or induced by the mesoderm. EMBO J. 6:2965–2975.
   PubMedGoogle Scholar
• Duboule, D., and G. Morata. 1994. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10:358–364.
   PubMedGoogle Scholar
• Dupé, V., M. Davenne, J. Brocard, P. Dollé, M. Mark, A. Dierich, P. Chambon, and F. M. Rijli. 1997. In vivo functional analysis of the Hoxa-1 3′ retinoic acid response element (3′RARE). Development 124:399–410.
   PubMed Web of Science ®Google Scholar
• Ehran, L. A., and K. E. Yutzey. 2001. Anterior expression of the caudal homologue cCdx-B activates a posterior genetic program in avian embryos. Dev. Dyn. 221:412–421.
   PubMedGoogle Scholar
• Epstein, M., G. Pillemer, R. Yelin, J. K. Yisraeli, and A. Fainsod. 1997. Patterning of the embryo along the anterior-posterior axis: the role of the caudal genes. Development 124:3805–3814.
   PubMedGoogle Scholar
• Gamer, L. W., and C. V. Wright. 1993. Murine Cdx-4 bears striking similarities to the Drosophila caudal gene in its homeodomain sequence and early expression pattern. Mech. Dev. 43:71–81.
   PubMedGoogle Scholar
• Gaunt, S. J., P. L. Coletta, D. Pravtcheva, and P. T. Sharpe. 1990. Mouse Hox-3.4: homeobox sequence and embryonic expression patterns compared with other members of the Hox gene network. Development 109:329–339.
   PubMedGoogle Scholar
• Gérard, M., J. Y. Chen, H. Gronemeyer, P. Chambon, D. Duboule, and J. Zakany. 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.
   PubMed Web of Science ®Google Scholar
• Gould, A., A. Morrison, G. Sproat, R. A. White, and R. Krumlauf. 1997. Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 11:900–913.
   PubMedGoogle Scholar
• Hogan, B., R. S. Beddington, F. Constantini, and E. Lacy. 1994. Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Houle, M., J. R. Sylvestre, and D. Lohnes. 2003. Retinoic acid regulates a subset of Cdx1 function in vivo. Development 130:6555–6567.
   PubMedGoogle Scholar
• Hunter, C. P., J. M. Harris, J. N. Maloof, and C. Kenyon. 1999. Hox gene expression in a single Caenorhabditis elegans cell is regulated by a caudal homolog and intercellular signals that inhibit wnt signaling. Development 126:805–814.
   PubMed Web of Science ®Google Scholar
• Ikeya, M., and S. Takada. 2001. Wnt-3a is required for somite specification along the anteroposterior axis of the mouse embryo and for regulation of cdx-1 expression. Mech. Dev. 193:27–33.
   Google Scholar
• Isaacs, H. V., M. E. Pownall, and J. M. Slack. 1998. Regulation of Hox gene expression and posterior development by the Xenopus caudal homologue Xcad3. EMBO J. 17:3413–3427.
   PubMedGoogle Scholar
• Jeannotte, L., M. Lemieux, J. Charron, F. Poirier, and E. J. Robertson. 1993. Specification of axial identity in the mouse: role of the Hoxa-5 (Hox1.3) gene. Genes Dev. 7:2085–2096.
   PubMed Web of Science ®Google Scholar
• Kmita, M., N. Fraudeau, Y. Hérault, and D. Duboule. 2002. Serial deletions and duplications suggest a mechanism for the collinearity of Hoxd genes in limbs. Nature 420:145–150.
   PubMedGoogle Scholar
• Kmita, M., and D. Duboule. 2003. Organizing axes in time and space; 25 years of colinear tinkering. Science 301:331–333.
   PubMed Web of Science ®Google Scholar
• Knittel, T., M. Kessel, M. H. Kim, and P. Gruss. 1995. A conserved enhancer of the human and murine Hoxa-7 genes specifies the anterior boundary of expression during embryonal development. Development 121:1077–1088.
   PubMedGoogle Scholar
• Kondo, T., and D. Duboule. 1999. Breaking colinearity in the mouse HoxD complex. Cell 97:407–417.
   PubMedGoogle Scholar
• Krumlauf, R., P. W. H. Holland, J. H. McVey, and B. L. M. Hogan. 1987. Developmental and spatial patterns of expression of the mouse homeobox gene Hox2.1. Development 99:603–617.
   PubMedGoogle Scholar
• Krumlauf, R. 1994. Hox genes in vertebrate development. Cell 78:191–201.
   PubMed Web of Science ®Google Scholar
• Larochelle, C., M. Tremblay, D. Bernier, J. Aubin, and L. Jeannotte. 1999. Multiple cis-acting regulatory regions are required for restricted spatio-temporal Hoxa5 gene expression. Dev. Dyn. 214:127–140.
   PubMedGoogle Scholar
• Lickert, H., C. Domon, G. Huls, C. Wehrle, I. Duluc, H. Clevers, B. I. Meyer, J. N. Freund, and R. Kemler. 2000. Wnt/(beta)-catenin signaling regulates the expression of the homeobox gene Cdx1 in embryonic intestine. Development 127:3805–3813.
   PubMed Web of Science ®Google Scholar
• Lohnes, D. 2003. The Cdx1 homeodomain protein: an integrator of posterior signaling in the mouse. Bioessays 25:971–980.
   PubMedGoogle Scholar
• Margalit, Y., S. Yarus, E. Shapira, Y. Gruenbaum, and A. Fainsod. 1993. Isolation and characterization of target sequences of the chicken CdxA homeobox gene. Nucleic Acids Res. 21:4915–4922.
   PubMedGoogle Scholar
• Meunier, D., J. Aubin, and L. Jeannotte. 2003. Perturbed thyroid morphology and transient hypothyroidism symptoms in Hoxa5 mutant mice. Dev. Dyn. 227:367–378.
   PubMedGoogle Scholar
• Mlodzik, M., G. Gibson, and W. J. Gehring. 1990. Effects of ectopic expression of caudal during Drosophila development. Development 109:271–277.
   PubMedGoogle Scholar
• Moreau, J., and L. Jeannotte. 2002. Sequence analysis of a Hoxa4-Hoxa5 intergenic region including shared regulatory elements. DNA Seq. 13:203–209.
   PubMed Web of Science ®Google Scholar
• Moreno, E., and G. Morata. 1999. Caudal is the Hox gene that specifies the most posterior Drosophila segment. Nature 400:873–877.
   PubMedGoogle Scholar
• Morrison, A., L. Ariza-McNaughton, A. Gould, M. Featherstone, and R. Krumlauf. 1997. HOXD4 and regulation of the group 4 paralog genes. Development 124:3135–3146.
   PubMedGoogle Scholar
• Nowling, T., W. Zhou, K. E. Krieger, C. Larochelle, M. C. Nguyen-Huu, L. Jeannotte, and C. K. Tuggle. 1999. Hoxa5 gene regulation: a gradient of binding activity to a brachial spinal cord element. Dev. Biol. 208:134–146.
   PubMedGoogle Scholar
• Oosterveen, T., K. Niederreither, P. Dollé, P. Chambon, F. Meijlink, and J. Deschamps. 2003. Retinoids regulate the anterior expression boundaries of 5′ Hoxb genes in posterior hindbrain. EMBO J. 22:262–269.
   PubMedGoogle Scholar
• Papenbrock, T., R. L. Peterson, R. S. Lee, T. Hsu, A. Kuroiwa, and A. Awgulewitsch. 1998. Murine Hoxc-9 gene contains a structurally and functionally conserved enhancer. Dev. Dyn. 212:540–547.
   PubMedGoogle Scholar
• Pöpperl, H., M. Bienz, M. Studer, S. K. Chan, S. Aparicio, S. Brenner, R. S. Mann, and R. Krumlauf. 1995. Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81:1031–1042.
   PubMed Web of Science ®Google Scholar
• Pownall, M. E., A. S. Tucker, J. M. Slack, and H. V. Isaacs. 1996. eFGF, Xcad3 and Hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus. Development 122:3881–3892.
   PubMedGoogle Scholar
• Prinos, P., S. Joseph, K. Oh, B. I. Meyer, P. Gruss, and D. Lohnes. 2001. Multiple pathways governing Cdx1 expression during murine development. Dev. Biol. 239:257–269.
   PubMedGoogle Scholar
• Rancourt, D. E., T. Tsuzuki, and M. R. Capecchi. 1995. Genetic interaction between hoxb-5 and hoxb-6 is revealed by nonallelic noncomplementation. Genes Dev. 9:108–122.
   PubMedGoogle Scholar
• Rivera-Pomar, R., X. Lu, N. Perrimon, H. Taubert, and H. Jackle. 1995. Activation of posterior gap gene expression in the Drosophila blastoderm. Nature 376:253–256.
   PubMed Web of Science ®Google Scholar
• Sharpe, J., S. Nonchev, A. Gould, J. Whiting, and R. Krumlauf. 1998. Selectivity, sharing and competitive interactions in the regulation of Hoxb genes. EMBO J. 17:1788–1798.
   PubMedGoogle Scholar
• Shashikant, C. S., C. J. Bieberich, H. G. Belting, J. C. Wang, M. A. Borbely, and F. H. Ruddle. 1995. Regulation of Hoxc-8 during mouse embryonic development: identification and characterization of critical elements involved in early neural tube expression. Development 121:4339–4347.
   PubMedGoogle Scholar
• Spitz, F., F. Gonzalez, and D. Duboule. 2003. A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 113:405–417.
   PubMed Web of Science ®Google Scholar
• Stein, S., R. Fritsch, L. Lemaire, and M. Kessel. 1996. Checklist: vertebrate homeobox genes. Mech. Dev. 55:91–108.
   PubMedGoogle Scholar
• Studer, M., H. Pöpperl, H. Marshall, A. Kuroiwa, and R. Krumlauf. 1994. Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1. Science 265:1728–1732.
   PubMedGoogle Scholar
• Subramanian, V., B. I. Meyer, and P. Gruss. 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.
   PubMedGoogle Scholar
• Suh, E., L. Chen, J. Taylor, and P. G. Traber. 1994. A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol. Cell. Biol. 14:7340–7351.
   PubMed Web of Science ®Google Scholar
• Taylor, J. K., T. Levy, E. R. Suh, and P. G. Traber. 1997. Activation of enhancer elements by the homeobox gene Cdx2 is cell line specific. Nucleic Acids Res. 25:2293–2300.
   PubMedGoogle Scholar
• Tuggle, C. K., J. Zakany, L. Cianetti, C. Peschle, and M. C. Nguyen-Huu. 1990. Region-specific enhancers near two mammalian homeobox genes define adjacent rostrocaudal domains in the central nervous system. Genes Dev. 4:180–189.
   PubMedGoogle Scholar
• van den Akker, A. E., S. Forlani, K. Chawengsaksophak, W. de Graaff, F. Beck, B. I. Meyer, and J. Deschamps. 2002. Cdx1 and Cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development 129:2181–2193.
   PubMedGoogle Scholar
• Wang, W., and B. A. Malcolm. 1999. Two-stage PCR protocol allowing introductions of multiple mutation deletions and insertions using quick-change site-directed mutagenesis. BioTechniques 26:680–682.
   PubMed Web of Science ®Google Scholar
• Zakany, J., C. K. Tuggle, M. D. Patel, and M. C. Nguyen-Huu. 1988. Spatial regulation of homeobox gene fusions in the embryonic central nervous system of transgenic mice. Neuron 1:679–691.
   PubMedGoogle Scholar
• Zakany, J., M. Gérard, B. Favier, and D. Duboule. 1997. Deletion of a HoxD enhancer induces transcriptional heterochrony leading to transposition of the sacrum. EMBO J. 16:4393–4402.
   PubMedGoogle Scholar