HAND2 targets define a network of transcriptional regulators that compartmentalize the early limb bud mesenchyme

Developmental Cell

Volumn 31, Issue 3, 2014, Pages 345-357

  Osterwalder, Marco ^a   Speziale, Dario ^a   Shoukry, Malak ^b   Mohan, Rajiv ^c   Ivanek, Robert ^a   Kohler, Manuel ^d   Beisel, Christian ^d   Wen, Xiaohui ^e   Scales, Suzie J ^e   Christoffels, Vincent M ^c   Visel, Axel ^b,f,g   Lopez Rios, Javier ^a   Zeller, Rolf ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d ETH ZURICH   (Switzerland)

^e GENENTECH INC   (United States)

^f DOE JOINT GENOME INSTITUTE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HAND2 PROTEIN; PEPTIDE; PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI3; TRANSCRIPTION FACTOR TBX3; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HAND2 PROTEIN, MOUSE; NERVE PROTEIN; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CHROMATIN; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; GENE FUNCTION; GENE TARGETING; GENOME; LIMB BUD; MESENCHYME; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; LIMB; MESODERM; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

VERTEBRATA;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIMB BUDS; MESODERM; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; TRANS-ACTIVATORS;

EID: 84919862317     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.09.018     Document Type: Article

References (56)

1. Abbasi A.A., Paparidis Z., Malik S., Bangs F., Schmidt A., Koch S., Lopez-Rios J., Grzeschik K.H. Human intronic enhancers control distinct sub-domains of Gli3 expression during mouse CNS and limb development. BMC Dev. Biol. 2010, 10:44.
2. Agulnik S.I., Garvey N., Hancock S., Ruvinsky I., Chapman D.L., Agulnik I., Bollag R., Papaioannou V., Silver L.M. Evolution of mouse T-box genes by tandem duplication and cluster dispersion. Genetics 1996, 144:249-254.
3. Ahn S., Joyner A.L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 2004, 118:505-516.
4. Alon U. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 2007, 8:450-461.
5. Anderson E., Peluso S., Lettice L.A., Hill R.E. Human limb abnormalities caused by disruption of hedgehog signaling. Trends Genet. 2012, 28:364-373.
6. Attanasio C., Nord A.S., Zhu Y., Blow M.J., Li Z., Liberton D.K., Morrison H., Plajzer-Frick I., Holt A., Hosseini R., et al. Fine tuning of craniofacial morphology by distant-acting enhancers. Science 2013, 342:1241006.
7. Barron F., Woods C., Kuhn K., Bishop J., Howard M.J., Clouthier D.E. Downregulation of Dlx5 and Dlx6 expression by Hand2 is essential for initiation of tongue morphogenesis. Development 2011, 138:2249-2259.
8. Belo J.A., Leyns L., Yamada G., De Robertis E.M. The prechordal midline of the chondrocranium is defective in Goosecoid-1 mouse mutants. Mech. Dev. 1998, 72:15-25.
9. Capdevila J., Tsukui T., Rodríquez Esteban C., Zappavigna V., Izpisúa Belmonte J.C. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol. Cell 1999, 4:839-849.
10. Capellini T.D., Di Giacomo G., Salsi V., Brendolan A., Ferretti E., Srivastava D., Zappavigna V., Selleri L. Pbx1/Pbx2 requirement for distal limb patterning is mediated by the hierarchical control of Hox gene spatial distribution and Shh expression. Development 2006, 133:2263-2273.
11. Capellini T.D., Vaccari G., Ferretti E., Fantini S., He M., Pellegrini M., Quintana L., Di Giacomo G., Sharpe J., Selleri L., Zappavigna V. Scapula development is governed by genetic interactions of Pbx1 with its family members and with Emx2 via their cooperative control of Alx1. Development 2010, 137:2559-2569.
12. Charité J., McFadden D.G., Olson E.N. The bHLH transcription factor dHAND controls Sonic hedgehog expression and establishment of thezone of polarizing activity during limb development. Development 2000, 127:2461-2470.
13. Chiang C., Litingtung Y., Harris M.P., Simandl B.K., Li Y., Beachy P.A., Fallon J.F. Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev. Biol. 2001, 236:421-435.
14. Cotney J., Leng J., Oh S., DeMare L.E., Reilly S.K., Gerstein M.B., Noonan J.P. Chromatin state signatures associated with tissue-specific gene expression and enhancer activity in the embryonic limb. Genome Res. 2012, 22:1069-1080.
15. Dai Y.S., Cserjesi P. The basic helix-loop-helix factor, HAND2, functions as a transcriptional activator by binding to E-boxes as a heterodimer. J.Biol. Chem. 2002, 277:12604-12612.
16. Davenport T.G., Jerome-Majewska L.A., Papaioannou V.E. Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human ulnar mammary syndrome. Development 2003, 130:2263-2273.
17. Dudley A.T., Ros M.A., Tabin C.J. A re-examination of proximodistal patterning during vertebrate limb development. Nature 2002, 418:539-544.
18. Farin, H. (2009). Function and regulation of the murine T-box genes Tbx15 and Tbx18. PhD thesis (Hannover: University of Hannover).
19. Farin H.F., Lüdtke T.H., Schmidt M.K., Placzko S., Schuster-Gossler K., Petry M., Christoffels V.M., Kispert A. Tbx2 terminates shh/fgf signaling in the developing mouse limb bud by direct repression of gremlin1. PLoS Genet. 2013, 9:e1003467.
20. Firulli B.A., Krawchuk D., Centonze V.E., Vargesson N., Virshup D.M., Conway S.J., Cserjesi P., Laufer E., Firulli A.B. Altered Twist1 and Hand2 dimerization is associated with Saethre-Chotzen syndrome and limb abnormalities. Nat. Genet. 2005, 37:373-381.
21. Funato N., Chapman S.L., McKee M.D., Funato H., Morris J.A., Shelton J.M., Richardson J.A., Yanagisawa H. Hand2 controls osteoblast differentiation in the branchial arch by inhibiting DNA binding of Runx2. Development 2009, 136:615-625.
22. Galli A., Robay D., Osterwalder M., Bao X., Bénazet J.D., Tariq M., Paro R., Mackem S., Zeller R. Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet. 2010, 6:e1000901.
23. Harfe B.D., Scherz P.J., Nissim S., Tian H., McMahon A.P., Tabin C.J. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 2004, 118:517-528.
24. Horsthuis T., Buermans H.P., Brons J.F., Verkerk A.O., Bakker M.L., Wakker V., Clout D.E., Moorman A.F., 't Hoen P.A., Christoffels V.M. Gene expression profiling of the forming atrioventricular node using a novel tbx3-based node-specific transgenic reporter. Circ. Res. 2009, 105:61-69.
25. Kmita M., Tarchini B., Zàkàny J., Logan M., Tabin C.J., Duboule D. Early developmental arrest of mammalian limbs lacking HoxA/HoxD gene function. Nature 2005, 435:1113-1116.
26. Kozhemyakina E., Ionescu A., Lassar A.B. GATA6 is a crucial regulator of Shh in the limb bud. PLoS Genet. 2014, 10:e1004072.
27. Lettice L.A., Heaney S.J., Purdie L.A., Li L., de Beer P., Oostra B.A., Goode D., Elgar G., Hill R.E., de Graaff E. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 2003, 12:1725-1735.
28. Lettice L.A., Williamson I., Wiltshire J.H., Peluso S., Devenney P.S., Hill A.E., Essafi A., Hagman J., Mort R., Grimes G., et al. Opposing functions of the ETS factor family define Shh spatial expression in limb buds and underlie polydactyly. Dev. Cell 2012, 22:459-467.
29. Lettice L.A., Williamson I., Devenney P.S., Kilanowski F., Dorin J., Hill R.E. Development of five digits is controlled by a bipartite long-rangecis-regulator. Development 2014, 141:1715-1725.
30. Li D., Sakuma R., Vakili N.A., Mo R., Puviindran V., Deimling S., Zhang X., Hopyan S., Hui C.C. Formation of proximal and anterior limb skeleton requires early function of Irx3 and Irx5 and is negatively regulated by Shh signaling. Dev. Cell 2014, 29:233-240.
31. Lopez-Rios J., Speziale D., Robay D., Scotti M., Osterwalder M., Nusspaumer G., Galli A., Holländer G.A., Kmita M., Zeller R. GLI3 constrains digit number by controlling both progenitor proliferation and BMP-dependent exit to chondrogenesis. Dev. Cell 2012, 22:837-848.
32. Lopez-Rios J., Duchesne A., Speziale D., Andrey G., Peterson K.A., Germann P., Unal E., Liu J., Floriot S., Barbey S., et al. Attenuated sensing of SHH by Ptch1 underlies evolution of bovine limbs. Nature 2014, 511:46-51.
33. Lowe L.A., Yamada S., Kuehn M.R. HoxB6-Cre transgenic mice express Cre recombinase in extra-embryonic mesoderm, in lateral plate and limb mesoderm and at the midbrain/hindbrain junction. Genesis 2000, 26:118-120.
34. Mao J., McGlinn E., Huang P., Tabin C.J., McMahon A.P. Fgf-dependent Etv4/5 activity is required for posterior restriction of Sonic Hedgehog and promoting outgrowth of the vertebrate limb. Dev. Cell 2009, 16:600-606.
35. Mariani F.V., Ahn C.P., Martin G.R. Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning. Nature 2008, 453:401-405.
36. Mercader N., Leonardo E., Piedra M.E., Martínez-A C., Ros M.A., Torres M. Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 2000, 127:3961-3970.
37. Niederreither K., Vermot J., Schuhbaur B., Chambon P., Dollé P. Embryonic retinoic acid synthesis is required for forelimb growth and anteroposterior patterning in the mouse. Development 2002, 129:3563-3574.
38. Osterwalder M., Galli A., Rosen B., Skarnes W.C., Zeller R., Lopez-Rios J. Dual RMCE for efficient re-engineering of mouse mutant alleles. Nat. Methods 2010, 7:893-895.
39. Rallis C., Del Buono J., Logan M.P. Tbx3 can alter limb position along the rostrocaudal axis of the developing embryo. Development 2005, 132:1961-1970.
40. Sagai T., Hosoya M., Mizushina Y., Tamura M., Shiroishi T. Elimination of a long-rangecis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 2005, 132:797-803.
41. Selleri L., Depew M.J., Jacobs Y., Chanda S.K., Tsang K.Y., Cheah K.S., Rubenstein J.L., O'Gorman S., Cleary M.L. Requirement for Pbx1 in skeletal patterning and programming chondrocyte proliferation and differentiation. Development 2001, 128:3543-3557.
42. Spitz F., Furlong E.E. Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 2012, 13:613-626.
43. Srivastava D., Thomas T., Lin Q., Kirby M.L., Brown D., Olson E.N. Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND. Nat. Genet. 1997, 16:154-160.
44. Tanaka M., Cohn M.J., Ashby P., Davey M., Martin P., Tickle C. Distribution of polarizing activity and potential for limb formation in mouse and chick embryos and possible relationships to polydactyly. Development 2000, 127:4011-4021.
45. te Welscher P., Fernandez-Teran M., Ros M.A., Zeller R. Mutual genetic antagonism involving GLI3 and dHAND prepatterns the vertebrate limb bud mesenchyme prior to SHH signaling. Genes Dev. 2002, 16:421-426.
46. Vincentz J.W., Barnes R.M., Firulli A.B. Hand factors as regulators of cardiac morphogenesis and implications for congenital heart defects. Birth Defects Res. A. Clin. Mol. Terat. 2011, 91:485-494.
47. Visel A., Minovitsky S., Dubchak I., Pennacchio L.A. VISTA Enhancer Browser-a database of tissue-specific human enhancers. Nucleic Acids Res. 2007, 35:D88-D92.
48. Vitobello A., Ferretti E., Lampe X., Vilain N., Ducret S., Ori M., Spetz J.F., Selleri L., Rijli F.M. Hox and Pbx factors control retinoic acid synthesis during hindbrain segmentation. Dev. Cell 2011, 20:469-482.
49. Vokes S.A., Ji H., Wong W.H., McMahon A.P. A genome-scale analysis of thecis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev. 2008, 22:2651-2663.
50. Wang B., Fallon J.F., Beachy P.A. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 2000, 100:423-434.
51. Wen X., Lai C.K., Evangelista M., Hongo J.A., de Sauvage F.J., Scales S.J. Kinetics of hedgehog-dependent full-length Gli3 accumulation in primary cilia and subsequent degradation. Mol. Cell. Biol. 2010, 30:1910-1922.
52. Zeller R., López-Ríos J., Zuniga A. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat. Rev. Genet. 2009, 10:845-858.
53. Zhang Z., Verheyden J.M., Hassell J.A., Sun X. FGF-regulated Etv genes are essential for repressing Shh expression in mouse limb buds. Dev. Cell 2009, 16:607-613.
54. Zhang Z., Sui P., Dong A., Hassell J., Cserjesi P., Chen Y.T., Behringer R.R., Sun X. Preaxial polydactyly: interactions among ETV, TWIST1 and HAND2 control anterior-posterior patterning of the limb. Development 2010, 137:3417-3426.
55. Zhao X., Sirbu I.O., Mic F.A., Molotkova N., Molotkov A., Kumar S., Duester G. Retinoic acid promotes limb induction through effects on body axis extension but is unnecessary for limb patterning. Curr. Biol. 2009, 19:1050-1057.
56. Zhu J., Nakamura E., Nguyen M.T., Bao X., Akiyama H., Mackem S. Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Dev. Cell 2008, 14:624-632.