Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for Gremlin expression

Genes and Development

Volumn 18, Issue 13, 2004, Pages 1553-1564

  Zuniga, Aimée ^a,b   Michos, Odyssé ^a,b   Spitz, François ^c   Haramis, Anna Pavlina G ^d,e   Panman, Lia ^b   Galli, Antonella ^a   Vintersten, Kristina ^d,f   Klasen, Christian ^d   Mansfield, William ^d   Kuc, Sylwia ^b   Duboule, Denis ^c   Dono, Rosanna ^b,g   Zeller, Rolf ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^e HUBRECHT INSTITUTE   (Netherlands)

^f MOUNT SINAI HOSPITAL   (Canada)

^g AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Cis regulation; Formin; Global control region; Gremlin; Limb development; Regulatory landscape

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GENE PRODUCT; GREMLIN; METHENAMINE; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ALLELE; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; FORMIN GENE; GENE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GLOBAL CONTROL REGION; GREMLIN GENE; LIMB BUD; LIMB DEFORMITY; LIMB DEVELOPMENT; MESENCHYME; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; FETAL PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIMB BUD; LIMB DEFORMITIES, CONGENITAL; MESODERM; MICE; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; REGULATORY SEQUENCES, NUCLEIC ACID; RNA SPLICING; TRANS-ACTIVATORS;

ANIMALIA; MAMMALIA;

EID: 3042696502     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.299904     Document Type: Article

References (45)

1. Avsian-Kretchmer, O. and Hsueh, A.J. 2003. Comparative genomic analysis of the eight-membered-ring cystine-knot-containing bone morphogenetic protein (BMP) antagonists. Mol. Endocrinol. 18: 1-12.
2. Bacchelli, C., Goodman, F.R., Scambler, P.J., and Winter, R.M. 2001. Cenani-Lenz syndrome with renal hypoplasia is not linked to FORMIN or GREMLIN. Clin. Genet. 59: 203-205.
3. Chao, C.W., Chan, D.C., Kuo, A., and Leder, P. 1998. The mouse formin (Fmn) gene: Abundant circular RNA transcripts and gene-targeted deletion analysis. Mol. Med. 4: 614-628.
4. Evangelista, M., Zigmond, S., and Boone, C. 2003. Formins: Signaling effectors for assembly and polarization of actin filaments. J. Cell Sci. 116: 2603-2611.
5. Faustino, N.A. and Cooper, T.A. 2003. Pre-mRNA splicing and human disease. Genes & Dev. 17: 419-437.
6. Gurrieri, F., Kjaer, K.W., Sangiorgi, E., and Neri, G. 2002. Limb anomalies: Developmental and evolutionary aspects. Am. J. Med. Genet. 115: 231-244.
7. 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.
8. Jansen, G., Hazendonk, E., Thijssen, K.L., and Plasterk, R.H. 1997. Reverse genetics by chemical mutagenesis in Caenorhabditis elegans. Nat. Genet. 17: 119-121.
9. Justice, M.J. 2000. Capitalizing on large-scale mouse mutagenesis screens. Nat. Rev. Genet. 1: 109-115.
10. Khokha, M.K., Hsu, D., Brunet, L.J., Dionne, M.S., and Harland, R.M. 2003. Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat. Genet. 34: 303-307.
11. Knittel, T., Kessel, M., Kim, M.H., 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.
12. Kobielak, A., Pasolli, H.A., and Fuchs, E. 2004. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat. Cell Biol. 6: 21-30.
13. Leader, B. and Leder, P. 2000. Formin-2, a novel formin homology protein of the cappuccino subfamily, is highly expressed in the developing and adult central nervous system. Mech. Dev. 93: 221-231.
14. Lettice, L.A., Horikoshi, T., Heaney, S.J., Van Baren, M.J., Van Der Linde, H.C., Breedveld, G.J., Joosse, M., Akarsu, N., Oostra, B.A., Endo, N., et al. 2002. Disruption of a long-range cis-acting regulator for Shh causes preaxial polydactyly. Proc. Natl. Acad. Sci. 99: 7548-7553.
15. Maas, R.L., Zeller, R., Woychik, R.P., Vogt, T.F., and Leder, P. 1990. Disruption of formin-encoding transcripts in two mutant limb deformity alleles. Nature 346: 853-855.
16. Maas, R.L., Jepeal, L.I., Elfering, S.L., Holcombe, R.F., Morton, C.C., Eddy, R.L., Byers, M.G., Shows, T.B., and Leder, P. 1991. A human gene homologous to the formin gene residing at the murine limb deformity locus: Chromosomal location and RFLPs. Am. J. Hum. Genet. 48:687-695.
17. Maas, R., Elfering, S., Glaser, T., and Jepeal, L. 1994. Deficient outgrowth of the ureteric bud underlies the renal agenesis phenotype in mice manifesting the limb deformity (1d) mutation. Dev. Dyn. 199: 214-228.
18. Mayor, C., Brudno, M., Schwartz, J.R., Poliakov, A., Rubin, E.M., Frazer, K.A., Pachter, L.S., and Dubchak, I. 2000. VISTA: Visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16: 1046-1047.
19. Merino, R., Rodriguez-Leon, J., Macias, D., Ganan, Y., Economides, A.N., and Hurle, J.M. 1999. The BMP antagonist Gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb. Development 126: 5515-5522.
20. Michos, O., Panman, L., Vintersten, K., Beier, K., Zeller, R., and Zuniga, A. 2004. Gremlin mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development (in press).
21. Minabe-Saegusa, C., Saegusa, H., Tsukahara, M., and Noguchi, S. 1998. Sequence and expression of a novel mouse gene PRDC (protein related to DAN and cerberus) identified by a gene trap approach. Dev. Growth Differ. 40: 343-353.
22. Mohammadi, M., McMahon, G., Sun, L., Tang, C., Hirth, P., Yeh, B.K., Hubbard, S.R., and Schlessinger, J. 1997. Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276: 955-960.
23. Morgan, B.A., Conlon, F.L., Manzanares, M., Millar, J.B., Kanuga, N., Sharpe, J., Krumlauf, R., Smith, J.C., and Sedgwick, S.G. 1996. Transposon tools for recombinant DNA manipulation: Characterization of transcriptional regulators from yeast, Xenopus, and mouse. Proc. Natl. Acad. Sci. 93: 2801-2806.
24. Morgan, N.V., Bacchelli, C., Gissen, P., Morton, J., Ferrero, G.B., Silengo, M., Labrune, P., Casteels, I., Hall, C., Cox, P., et al. 2003. A locus for asphyxiating thoracic dystrophy, ATD, maps to chromosome 15q13. J. Med. Genet. 40: 431-435.
25. Mountford, P., Zevnik, B., Duwel, A., Nichols, J., Li, M., Dani, C., Robertson, M., Chambers, I., and Smith, A. 1994. Dicistronic targeting constructs: Reporters and modifiers of mammalian gene expression. Proc. Natl. Acad. Sci. 91: 4303-4307.
26. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W., and Roder, J.C. 1993. Viable cell culture-derived mice from early passage embryonic stem cells. Proc. Natl. Acad. Sci, 90: 8424-8428.
27. Nagy, A., Gertsensten, M., Vintersten, K., and Behringer, R. 2002. Manipulating the mouse embryo: A laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, New York.
28. Niehrs, C. and Pollet, N. 1999. Synexpression groups in eukaryotes. Nature 402: 483-487.
29. Panman, L. and Zeller, R. 2003. Patterning the limb before and after SHH signalling. J. Anat. 202: 3-12.
30. Perkins, A.S. 2002. Functional genomics in the mouse. Funct. Integr. Genomics 2: 81-91.
31. Schwenk, F., Baron, U., and Rajewsky, K. 1995. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 23: 5080-5081.
32. Spitz, F., Gonzalez, F., Peichel, C., Vogt, T.F., Duboule, D., and Zakany, J. 2001. Large scale transgenic and cluster deletion analysis of the HoxD complex separate an ancestral regulatory module from evolutionary innovations. Genes & Dev. 15: 2209-2214.
33. Spitz, F., Gonzalez, F., and Duboule, D. 2003. A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 113: 405-417.
34. Sun, X., Mariani, F.V., and Martin, G.R. 2002. Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418: 501-508.
35. Vogt, T.F., Jackson Grusby, L., Wynshaw Boris, A.J., Chan, D.C., and Leder, P. 1992. The same genomic region is disrupted in two transgene-induced limb deformity alleles. Mamm. Genome 3: 431-437.
36. Wang, C.C., Chan, D.C., and Leder, P. 1997. The mouse formin (Fmn) gene: Genomic structure, novel exons, and genetic mapping. Genomics 39: 303-311.
37. Waterston, R.H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J.F., Agarwal, P., Agarwala, R., Ainscough, R., Alexandersson, M., An, P., et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
38. Woychik, R.P., Stewart, T.A., Davis, L.G., D'Eustachio, P. and Leder, P. 1985. An inherited limb deformity created by insertional mutagenesis in a transgenic mouse. Nature 318: 36-40.
39. Woychik, R.P., Generoso, W.M., Russell, L.B., Cain, K.T., Cacheiro, N.L.A., Bultman, S.J., Selby, P.B., Dickinson, M.E., Hogan, B.L.M., and Rutledge, J.C. 1990. Molecular and genetic characterisation of a radiation-induced structural rearrangement in mouse chromosome 2 causing mutations at the limb deformity and agouti loci. Proc. Natl. Acad. Sci. 87: 2588-2592.
40. Wynshaw-Boris, A., Ryan, G., Deng, C.X., Chan, D.C., Jackson-Grusby, L., Larson, D., Dunmore, J.H., and Leder, P. 1997. The role of a single formin isoform in the limb and renal phenotypes of limb deformity. Mol. Med. 3: 372-384.
41. Zákány, J. and Duboule, D. 1996. Synpolydactyly in mice with a targeted deficiency in the HoxD complex. Nature 384: 69-71.
42. Zeller, R. and Deschamps, J. 2002. Developmental biology: First come, first served. Nature 420: 138-139.
43. Zeller, R., Haramis, A., Zuniga, A., McGuigan, C., Dono, R., Davidson, G., Chabanis, S., and Gibson, T. 1999. Formin defines a large family of morphoregulatory genes and functions in establishment of the polarising region. Cell Tissue Res. 296: 85-93.
44. Zuniga, A. and Zeller, R. 1999. Gli3 (Xt) and formin (1d) participate in the positioning of the polarising region and control of posterior limb-bud identity. Development 126: 13-21.
45. Zuniga, A., Haramis, A.P., McMahon, A.P., and Zeller, R. 1999. Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature 401: 598-602.