Direct activation of a mouse Hoxd11 axial expression enhancer by Gdf11/Smad signalling

Developmental Biology

Volumn 383, Issue 1, 2013, Pages 52-60

  Gaunt, Stephen J ^a,b   George, Martin ^b   Paul, Yu Lee ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Enhancer; Gdf11; HepG2 cells; Hoxd11; Mouse embryo; Smad binding elements

Indexed keywords

EID: 84885473367     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.08.025     Document Type: Article

References (46)

1. Andersson O., Reissmann E., Ibanez C.F. Growth differentiation factor 11 signals through the transforming growth factor-beta receptor ALK5 to regionalize the anterior-posterior axis. EMBO Rep. 2006, 7:831-837.
2. Bel-Vialar S., Itasaki N., Krumlauf R. 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 2002, 129:5103-5115.
3. Brown K.A., Pietenpol J.A., Moses H.L. A tale of two proteins: differential roles and regulation of Smad2 and Smad3 in TGF-beta signaling. J. Cell. Biochem. 2007, 101:9-33.
4. Ceballos M.P., Parody J.P., Alvarez Mde L., Ingaramo P.I., Carnovale C.E., Carrillo M.C. Interferon-alpha2b and transforming growth factor-beta1 treatments on HCC cell lines: are Wnt/beta-catenin pathway and Smads signaling connected in hepatocellular carcinoma?. Biochem. Pharmacol. 2011, 82:1682-1691.
5. Charite J., de Graaff W., Consten D., Reijnen M.J., Korving J., Deschamps J. Transducing positional information to the Hox genes: critical interaction of cdx gene products with position-sensitive regulatory elements. Development 1998, 125:4349-4358.
6. Datto M.B., Frederick J.P., Pan L., Borton A.J., Zhuang Y., Wang X.F. Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction. Mol. Cell. Biol. 1999, 19:2495-2504.
7. Davis A.P., Capecchi M.R. Axial homeosis and appendicular skeleton defects in mice with a targeted disruption of hoxd-11. Development 1994, 120:2187-2198.
8. Dennler S., Itoh S., Vivien D., ten Dijke P., Huet S., Gauthier J.M. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 1998, 17:3091-3100.
9. Dunn N.R., Vincent S.D., Oxburgh L., Robertson E.J., Bikoff E.K. Combinatorial activities of Smad2 and Smad3 regulate mesoderm formation and patterning in the mouse embryo. Development 2004, 131:1717-1728.
10. Feng X.H., Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 2005, 21:659-693.
11. Gad J.M., Tam P.P. Axis development: the mouse becomes a dachshund. Curr. Biol.: CB 1999, 9:R783-R786.
12. Gamer L.W., Wolfman N.M., Celeste A.J., Hattersley G., Hewick R., Rosen V. A novel BMP expressed in developing mouse limb, spinal cord, and tail bud is a potent mesoderm inducer in Xenopus embryos. Dev. Biol. 1999, 208:222-232.
13. Gaunt S.J., Cockley A., Drage D. Additional enhancer copies, with intact cdx binding sites, anteriorize Hoxa-7/lacZ expression in mouse embryos: evidence in keeping with an instructional cdx gradient. Int. J. Dev. Biol. 2004, 48:613-622.
14. Gaunt S.J., Drage D., Cockley A. Vertebrate caudal gene expression gradients investigated by use of chick cdx-A/lacZ and mouse cdx-1/lacZ reporters in transgenic mouse embryos: evidence for an intron enhancer. Mech. Dev. 2003, 120:573-586.
15. Gaunt S.J., Paul Y.-L. Origins of Cdx1 regulatory elements suggest roles in vertebrate evolution. Int. J. Dev. Biol. 2011, 55:93-98.
16. Gaunt S.J., Paul Y.-L. Changes in Cis-regulatory Elements during Morphological Evolution. Biology 2012, 1:557-574.
17. Gerard M., Duboule D., Zakany J. Structure and activity of regulatory elements involved in the activation of the Hoxd-11 gene during late gastrulation. EMBO J. 1993, 12:3539-3550.
18. Gerard M., Zakany J., Duboule D. Interspecies exchange of a Hoxd enhancer in vivo induces premature transcription and anterior shift of the sacrum. Dev. Biol. 1997, 190:32-40.
19. Guzman-Ayala M., Lee K.L., Mavrakis K.J., Goggolidou P., Norris D.P., Episkopou V. Graded Smad2/3 activation is converted directly into levels of target gene expression in embryonic stem cells. PloS One 2009, 4:e4268.
20. Hogan B. Manipulating the Mouse Embryo: A Laboratory Manual 1994, Cold Spring Harbor Laboratory Press, Plainview, N.Y. 2nd ed.
21. Hu Y., Tang G., Liu J., Cheng W., Yue Y., Li J., Zhang P. FGF receptor-mediated gene delivery using ligands coupled to PEI-beta-CyD. J. Biomed. Biotechnol. 2012, 2012:989235.
22. Izpisua-Belmonte J.C., Falkenstein H., Dolle P., Renucci A., Duboule D. Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J. 1991, 10:2279-2289.
23. Jinnin M., Ihn H., Tamaki K. Characterization of SIS3, a novel specific inhibitor of Smad3, and its effect on transforming growth factor-beta1-induced extracellular matrix expression. Mol. Pharmacol. 2006, 69:597-607.
24. Jurberg A.D., Aires R., Varela-Lasheras I., Novoa A., Mallo M. Switching axial progenitors from producing trunk to tail tissues in vertebrate embryos. Dev. Cell 2013, 25:451-462.
25. Liu J.P. The function of growth/differentiation factor 11 (Gdf11) in rostrocaudal patterning of the developing spinal cord. Development 2006, 133:2865-2874.
26. Liu J.P., Laufer E., Jessell T.M. Assigning the positional identity of spinal motor neurons: rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids. Neuron 2001, 32:997-1012.
27. Liu P., Jenkins N.A., Copeland N.G. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 2003, 13:476-484.
28. Margalit Y., Yarus S., Shapira E., Gruenbaum Y., Fainsod A. Isolation and characterization of target sequences of the chicken CdxA homeobox gene. Nucleic Acids Res. 1993, 21:4915-4922.
29. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19:2783-2810.
30. McPherron A.C., Lawler A.M., Lee S.J. Regulation of anterior/posterior patterning of the axial skeleton by growth/differentiation factor 11. Nat. Genet. 1999, 22:260-264.
31. Mullen A.C., Orlando D.A., Newman J.J., Loven J., Kumar R.M., Bilodeau S., Reddy J., Guenther M.G., DeKoter R.P., Young R.A. Master transcription factors determine cell-type-specific responses to TGF-beta signaling. Cell 2011, 147:565-576.
32. Nakashima M., Toyono T., Akamine A., Joyner A. Expression of growth/differentiation factor 11, a new member of the BMP/TGFbeta superfamily during mouse embryogenesis. Mech. Dev. 1999, 80:185-189.
33. Oh S.P., Li E. The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes Dev. 1997, 11:1812-1826.
34. Oh S.P., Yeo C.Y., Lee Y., Schrewe H., Whitman M., Li E. Activin type IIA and IIB receptors mediate Gdf11 signaling in axial vertebral patterning. Genes Dev. 2002, 16:2749-2754.
35. Prinos P., Joseph S., Oh K., Meyer B.I., Gruss P., Lohnes D. Multiple pathways governing Cdx1 expression during murine development. Dev. Biol. 2001, 239:257-269.
36. Ravi V., Lam K., Tay B.H., Tay A., Brenner S., Venkatesh B. Elephant shark (Callorhinchus milii) provides insights into the evolution of Hox gene clusters in gnathostomes. Proc. Natl. Acad. Sci. USA 2009, 106:16327-16332.
37. Shi Y., Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700.
38. Takimoto T., Wakabayashi Y., Sekiya T., Inoue N., Morita R., Ichiyama K., Takahashi R., Asakawa M., Muto G., Mori T., Hasegawa E., Saika S., Hara T., Nomura M., Yoshimura A. Smad2 and Smad3 are redundantly essential for the TGF-beta-mediated regulation of regulatory T plasticity and Th1 development. J. Immunol. 2010, 185:842-855.
39. Tremblay K.D., Hoodless P.A., Bikoff E.K., Robertson E.J. Formation of the definitive endoderm in mouse is a Smad2-dependent process. Development 2000, 127:3079-3090.
40. Waldrip W.R., Bikoff E.K., Hoodless P.A., Wrana J.L., Robertson E.J. Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell 1998, 92:797-808.
41. Wellik D.M., Capecchi M.R. Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 2003, 301:363-367.
42. Wittkopp P.J., Kalay G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 2012, 13:59-69.
43. Wu M.Y., Hill C.S. Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev. Cell 2009, 16:329-343.
44. Zakany J., Gerard M., Favier B., Duboule D. Deletion of a HoxD enhancer induces transcriptional heterochrony leading to transposition of the sacrum. EMBO J. 1997, 16:4393-4402.
45. Zawel L., Dai J.L., Buckhaults P., Zhou S., Kinzler K.W., Vogelstein B., Kern S.E. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol. Cell 1998, 1:611-617.
46. Zhang Y., Zolfaghari R., Ross A.C. Multiple retinoic acid response elements cooperate to enhance the inducibility of CYP26A1 gene expression in liver. Gene 2010, 464:32-43.