Conserved cis-regulatory regions in a large genomic landscape control SHH and BMP-regulated Gremlin1 expression in mouse limb buds

BMC Developmental Biology

Volumn 12, Issue , 2012, Pages

  Zuniga, Aimée ^a   Laurent, Frédéric ^a   Lopez Rios, Javier ^a   Klasen, Christian ^b,c   Matt, Nicolas ^a,d   Zeller, Rolf ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

VERTEBRATA;

BONE MORPHOGENETIC PROTEIN RECEPTOR; CKTSF1B1 PROTEIN, MOUSE; GLI3 PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; NERVE PROTEIN; SHH PROTEIN, MOUSE; SIGNAL PEPTIDE; SONIC HEDGEHOG PROTEIN;

ANIMAL; ARTICLE; BIOSYNTHESIS; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; LIMB BUD; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; PRENATAL DEVELOPMENT; REGULATORY SEQUENCE; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIMB BUDS; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; REGULATORY SEQUENCES, NUCLEIC ACID; SIGNAL TRANSDUCTION;

MLCS; MLOWN;

EID: 84872121376     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-12-23     Document Type: Article

References (55)

1. Long-range regulation at the SOX9 locus in development and disease. Gordon CT, Tan TY, Benko S, Fitzpatrick D, Lyonnet S, et al. Journal of medical genetics 2009 46 649 656 10.1136/jmg.2009.068361 19473998
2. cis-regulatory mutations are a genetic cause of human limb malformations. Vandermeer JE, Ahituv N, Dev Dyn 2011 240 920 930 10.1002/dvdy.22535 21509892
3. Zuniga A, Probst S, Zeller R, The molecular basis of human congenital limb malformations Wiley Interdisciplinary Reviews: Developmental Biology 2012
4. Large-scale analysis of the regulatory architecture of the mouse genome with a transposon-associated sensor. Ruf S, Symmons O, Uslu VV, Dolle D, Hot C, et al. Nat Genet 2011 43 379 386 10.1038/ng.790 21423180
5. Disruption of a long-range cis-acting regulator for Shh causes preaxial polydactyly. Lettice LA, Horikoshi T, Heaney SJ, Van Baren MJ, Van Der Linde HC, et al. Proc Natl Acad Sci U S A 2002 99 7548 7553 10.1073/pnas.112212199 12032320
6. A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Spitz F, Gonzalez F, Duboule D, Cell 2003 113 405 417 10.1016/S0092-8674(03)00310-6 12732147
7. Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for Gremlin expression. Zuniga A, Michos O, Spitz F, Haramis AP, Panman L, et al. Genes Dev 2004 18 1553 1564 10.1101/gad.299904 15198975
8. A regulatory archipelago controls Hox genes transcription in digits. Montavon T, Soshnikova N, Mascrez B, Joye E, Thevenet L, et al. Cell 2011 147 1132 1145 10.1016/j.cell.2011.10.023 22118467
9. Control of vertebrate Hox clusters by remote and global cis-acting regulatory sequences. Spitz F, Adv Exp Med Biol 2010 689 63 78 10.1007/978-1-4419-6673-5-4 20795322
10. Shh and Gremlin1 chromosomal landscapes in development and disease. Zeller R, Zuniga A, Curr Opin Genet Dev 2007 17 428 434 10.1016/j.gde.2007.07. 006 17714931
11. A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Benazet JD, Bischofberger M, Tiecke E, Goncalves A, Martin JF, et al. Science 2009 323 1050 1053 10.1126/science.1168755 19229034
12. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Capdevila J, Tsukui T, Rodriquez Esteban C, Zappavigna V, Izpisua Belmonte JC, Mol Cell 1999 4 839 849 10.1016/S1097-2765(00)80393-7 10619030
13. Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Michos O, Panman L, Vintersten K, Beier K, Zeller R, et al. Development 2004 131 3401 3410 10.1242/dev.01251 15201225
14. Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Zuniga A, Haramis AP, McMahon AP, Zeller R, Nature 1999 401 598 602 10.1038/44157 10524628
15. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Zeller R, Lopez-Rios J, Zuniga A, Nat Rev Genet 2009 10 845 858 10.1038/nrg2681 19920852
16. Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Sagai T, Hosoya M, Mizushina Y, Tamura M, Shiroishi T, Development 2005 132 797 803 10.1242/dev.01613 15677727
17. Point mutations in a distant sonic hedgehog cis-regulator generate a variable regulatory output responsible for preaxial polydactyly. Lettice LA, Hill AE, Devenney PS, Hill RE, Hum Mol Genet 2008 17 978 985 18156157
18. Identification of spontaneous mutations within the long-range limb-specific Sonic hedgehog enhancer (ZRS) that alter Sonic hedgehog expression in the chicken limb mutants oligozeugodactyly and silkie breed. Maas SA, Suzuki T, Fallon JF, Dev Dyn 2011 240 1212 1222 10.1002/dvdy.22634 21509895
19. Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Amano T, Sagai T, Tanabe H, Mizushina Y, Nakazawa H, et al. Dev Cell 2009 16 47 57 10.1016/j.devcel.2008.11. 011 19097946
20. Pbx1/Pbx2 requirement for distal limb patterning is mediated by the hierarchical control of Hox gene spatial distribution and Shh expression. Capellini TD, Di Giacomo G, Salsi V, Brendolan A, Ferretti E, et al. Development 2006 133 2263 2273 10.1242/dev.02395 16672333
21. Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. Galli A, Robay D, Osterwalder M, Bao X, Benazet JD, et al. PLoS Genet 2010 6 1000901 10.1371/journal.pgen.1000901 20386744
22. Opposing Functions of the ETS Factor Family Define Shh Spatial Expression in Limb Buds and Underlie Polydactyly. Lettice LA, Williamson I, Wiltshire JH, Peluso S, Devenney PS, et al. Dev Cell 2012 22 459 467 10.1016/j.devcel.2011.12. 010 22340503
23. Hedgehog-Regulated Processing of Gli3 Produces an Anterior/Posterior Repressor gradient in the Developing Vertebrate Limb. Wang B, Fallon JF, Beachy PA, Cell 2000 100 423 434 10.1016/S0092-8674(00)80678-9 10693759
24. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Mo R, Freer AM, Zinyk DL, Crackower MA, Michaud J, et al. Development 1997 124 113 123 9006072
25. Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Litingtung Y, Dahn RD, Li Y, Fallon JF, Chiang C, Nature 2002 418 979 983 10.1038/nature01033 12198547
26. GLI3 Constrains Digit Number by Controlling Both Progenitor Proliferation and BMP-Dependent Exit to Chondrogenesis. Lopez-Rios J, Speziale D, Robay D, Scotti M, Osterwalder M, et al. Developmental Cell 2012 22 837 848 10.1016/j.devcel.2012.01.006 22465667
27. Progression of Vertebrate Limb Development through SHH-Mediated Counteraction of GLI3. te Welscher P, Zuniga A, Kuijper S, Drenth T, Goedemans HJ, et al. Science 2002 298 827 830 10.1126/science.1075620 12215652
28. Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Khokha MK, Hsu D, Brunet LJ, Dionne MS, Harland RM, Nat Genet 2003 34 303 307 10.1038/ng1178 12808456
29. Formin1 disruption confers oligodactylism and alters Bmp signaling. Zhou F, Leder P, Zuniga A, Dettenhofer M, Hum Mol Genet 2009 18 2472 2482 10.1093/hmg/ddp185 19383632
30. Differential regulation of gene expression in the digit forming area of the mouse limb bud by SHH and gremlin 1/FGF-mediated epithelial-mesenchymal signalling. Panman L, Galli A, Lagarde N, Michos O, Soete G, et al. Development 2006 133 3419 3428 10.1242/dev.02529 16908629
31. Functional analysis of CTCF during mammalian limb development. Soshnikova N, Montavon T, Leleu M, Galjart N, Duboule D, Dev Cell 2010 19 819 830 10.1016/j.devcel.2010.11.009 21145498
32. A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Vokes SA, Ji H, Wong WH, McMahon AP, Genes Dev 2008 22 2651 2663 10.1101/gad.1693008 18832070
33. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, et al. Nature 2007 447 799 816 10.1038/nature05874 17571346
34. A user's guide to the encyclopedia of DNA elements (ENCODE). Myers RM, Stamatoyannopoulos J, Snyder M, Dunham I, Hardison RC, et al. PLoS biology 2011 9 1001046 10.1371/journal.pbio.1001046 21526222
35. Identification of genes associated with regenerative success of Xenopus laevis hindlimbs. Pearl EJ, Barker D, Day RC, Beck CW, BMC Dev Biol 2008 8 66 10.1186/1471-213X-8-66 18570684
36. Regulated expression pattern of gremlin during zebrafish development. Nicoli S, Gilardelli CN, Pozzoli O, Presta M, Cotelli F, Gene expression patterns: GEP 2005 5 539 544 10.1016/j.modgep.2004.11.001 15749084
37. The pectoral fin of Panderichthys and the origin of digits. Boisvert CA, Mark-Kurik E, Ahlberg PE, Nature 2008 456 636 638 10.1038/nature07339 18806778
38. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Lettice LA, Heaney SJ, Purdie LA, Li L, de Beer P, et al. Hum Mol Genet 2003 12 1725 1735 10.1093/hmg/ddg180 12837695
39. The limb bud Shh-Fgf feedback loop is terminated by expansion of former ZPA cells. Scherz PJ, Harfe BD, McMahon AP, Tabin CJ, Science 2004 305 396 399 10.1126/science.1096966 15256670
40. An Fgf/Gremlin inhibitory feedback loop triggers termination of limb bud outgrowth. Verheyden JM, Sun X, Nature 2008 454 638 641 10.1038/nature07085 18594511
41. Genetic Analysis of the Roles of BMP2, BMP4, and BMP7 in Limb Patterning and Skeletogenesis. Bandyopadhyay A, Tsuji K, Cox K, Harfe BD, Rosen V, et al. PLoS Genet 2006 2 216 10.1371/journal.pgen.0020216 17194222
42. LIM homeobox transcription factors integrate signaling events that control three-dimensional limb patterning and growth. Tzchori I, Day TF, Carolan PJ, Zhao Y, Wassif CA, et al. Development 2009 136 1375 1385 10.1242/dev.026476 19304889
43. Regulation of Gremlin expression in the posterior limb bud. Nissim S, Hasso SM, Fallon JF, Tabin CJ, Dev Biol 2006 299 12 21 10.1016/j.ydbio.2006.05. 026 16989805
44. Mutual genetic antagonism involving GLI3 and dHAND prepatterns the vertebrate limb bud mesenchyme prior to SHH signaling. te Welscher P, Fernandez-Teran M, Ros MA, Zeller R, Genes Dev 2002 16 421 426 10.1101/gad.219202 11850405
45. Generation of Smad4/Dpc4 conditional knockout mice. Yang X, Li C, Herrera PL, Deng CX, Genesis 2002 32 80 81 10.1002/gene.10029 11857783
46. Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Logan M, Martin JF, Nagy A, Lobe C, Olson EN, et al. Genesis 2002 33 77 80 10.1002/gene.10092 12112875
47. Kinetics of hedgehog-dependent full-length Gli3 accumulation in primary cilia and subsequent degradation. Wen X, Lai CK, Evangelista M, Hongo JA, de Sauvage FJ, et al. Molecular and cellular biology 2010 30 1910 1922 10.1128/MCB.01089-09 20154143
48. Enhancer function: new insights into the regulation of tissue-specific gene expression. Ong CT, Corces VG, Nature reviews Genetics 2011 12 283 293 21358745
49. The temporal dynamics of vertebrate limb development, teratogenesis and evolution. Zeller R, Curr Opin Genet Dev 2010 20 384 390 10.1016/j.gde.2010.04. 014 20537528
50. Sonic hedgehog signaling is essential for hair development. St-Jacques B, Dassule HR, Karavanova I, Botchkarev VA, Li J, et al. Curr Biol 1998 8 1058 1068 10.1016/S0960-9822(98)70443-9 9768360
51. High-resolution mapping of the Gli3 mutation extra-toes reveals a 51.5-kb deletion. Maynard TM, Jain MD, Balmer CW, LaMantia AS, Mamm Genome 2002 13 58 61 10.1007/s00335-001-2115-X 11773971
52. Transposon tools for recombinant DNA manipulation: characterization of transcriptional regulators from yeast, Xenopus, and mouse. Morgan BA, Conlon FL, Manzanares M, Millar JB, Kanuga N, et al. Proc Natl Acad Sci U S A 1996 93 2801 2806 10.1073/pnas.93.7.2801 8610121
53. Rapid and accurate determination of zygosity in transgenic animals by real-time quantitative PCR. Tesson L, Heslan JM, Menoret S, Anegon I, Transgenic research 2002 11 43 48 10.1023/A:1013928600442 11874102
54. ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Ovcharenko I, Nobrega MA, Loots GG, Stubbs L, Nucleic acids research 2004 32 280 W286 10.1093/nar/gkh355 15215395
55. ClustalW and ClustalX version 2. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG, Bioinformatics 2007 23 2947 2948 10.1093/bioinformatics/btm404 17846036