Integration of Hedgehog and BMP signalling by the engrailed2a gene in the zebrafish myotome

Development

Volumn 138, Issue 4, 2011, Pages 755-765

  Maurya, Ashish K ^a,b   Tan, Haihan ^a   Souren, Marcel ^a,c   Wang, Xingang ^a   Wittbrodt, Joachim ^c   Ingham, Philip W ^a,b  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

BiFC; BMP; Engrailed; Gli; Muscle pioneers; Myotome; Patched; Smad; Sonic Hedgehog; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN; ENGRAILED2A PROTEIN; MUSCLE PROTEIN; SMAD PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE TARGETING; IN VIVO STUDY; MOLECULAR INTERACTION; MYOTOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; BASE SEQUENCE; BONE MORPHOGENETIC PROTEINS; CELL LINE; CRICETINAE; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; NERVE TISSUE PROTEINS; PROTEIN BINDING; SIGNAL TRANSDUCTION; SMAD5 PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; ERINACEIDAE; MYOXUS;

EID: 79951542472     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.062521     Document Type: Article

References (80)

1. Agren, M., Kogerman, P., Kleman, M. I., Wessling, M. and Toftgard, R. (2004). Expression of the PTCH1 tumor suppressor gene is regulated by alternative promoters and a single functional Gli-binding site. Gene 330, 101-114. (Pubitemid 38490423)
2. Alexandre, C., Jacinto, A. and Ingham, P. W. (1996). Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev. 10, 2003-2013.
3. Aza-Blanc, P., Ramirez-Weber, F. A., Laget, M. P., Schwartz, C. and Kornberg, T. B. (1997). Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89, 1043-1053.
4. Bakkers, J., Hild, M., Kramer, C., Furutani-Seiki, M. and Hammerschmidt, M. (2002). Zebrafish Np63 Is a direct target of Bmp signalling and encodes a transcriptional repressor blocking neural specification in the ventral ectoderm. Dev. Cell 2, 617-627. (Pubitemid 34538142)
5. Baxendale, S., Davison, C., Muxworthy, C., Wolff, C., Ingham, P. W. and Roy, S. (2004). The B-cell maturation factor Blimp-1 specifies vertebrate slow-twitch muscle fiber identity in response to Hedgehog signalling. Nat. Genet. 36, 88-93.
6. Beaster-Jones, L., Schubert, M. and Holland, L. Z. (2007). Cis-regulation of the amphioxus engrailed gene: insights into evolution of a muscle-specific enhancer. Mech. Dev. 124, 532-542.
7. Blagden, C. S., Currie, P. D., Ingham, P. W. and Hughes, S. M. (1997). Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev. 11, 2163-2175.
8. Burke, R., Nellen, D., Bellotto, M., Hafen, E., Senti, K. A., Dickson, B. J. and Basler, K. (1999). Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signalling cells. Cell 99, 803-815. (Pubitemid 30017650)
9. Caspary, T., Garcia-Garcia, M. J., Huangfu, D., Eggenschwiler, J. T., Wyler, M. R., Rakeman, A. S., Alcorn, H. L. and Anderson, K. V. (2002). Mouse Dispatched homolog1 is required for long-range, but not juxtacrine, Hh signalling. Curr. Biol. 12, 1628-1632.
10. Chen, C. R., Kang, Y., Siegel, P. M. and Massague, J. (2002). E2F4/5 and p107 as Smad cofactors linking the TGFβ receptor to c-myc repression. Cell 110, 19-32. (Pubitemid 34874603)
11. Concordet, J. P., Lewis, K. E., Moore, J. W., Goodrich, L. V., Johnson, R. L., Scott, M. P. and Ingham, P. W. (1996). Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122, 2835-2846.
12. Currie, P. D. and Ingham, P. W. (1996). Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 382, 452-455.
13. Dai, P., Akimaru, H., Tanaka, Y., Maekawa, T., Nakafuku, M. and Ishii, S. (1999). Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274, 8143-8152.
14. Degenhardt, K., Rentschler, S., Fishman, G. and Sassoon, D. A. (2002). Cellular and cis-regulation of En-2 expression in the mandibular arch. Mech. Dev. 111, 125-136.
15. Devoto, S. H., Melancon, E., Eisen, J. S. and Westerfield, M. (1996). Identification of separate slow and fast muscle precursor cells in-vivo, prior to somite formation. Development 122, 3371-3380. (Pubitemid 26395980)
16. Dick, A., Andrea, M. and Matthias, H. (1999). Smad1 and Smad5 have distinct roles during dorsoventral patterning of the zebrafish embryo. Dev. Dyn. 216, 285-298.
17. Du, S. J., Devoto, S. H., Westerfield, M. and Moon, R. T. (1997). Positive and negative regulation of muscle cell identity by members of the hedgehog and TGF-β gene families. J. Cell Biol. 139, 145-156.
18. Dunaeva, M., Michelson, P., Kogerman, P. and Toftgard, R. (2003). Characterization of the physical interaction of Gli proteins with SUFU proteins. J. Biol. Chem. 278, 5116-5122.
19. Ekker, M., Wegner, J., Akimenko, M. A. and Westerfield, M. (1992). Coordinate embryonic expression of three zebrafish engrailed genes. Development 116, 1001-1010. (Pubitemid 23042440)
20. Elworthy, S., Hargrave, M., Knight, R., Mebus, K. and Ingham, P. W. (2008). Expression of multiple slow myosin heavy chain genes reveals a diversity of zebrafish slow twitch muscle fibres with differing requirements for Hedgehog and Prdm1 activity. Development 135, 2115-2126.
21. Ericson, J., Briscoe, J., Rashbass, P., van Heyningen, V. and Jessell, T. M. (1997). Graded sonic hedgehog signalling and the specification of cell fate in the ventral neural tube. Cold Spring Harb. Symp. Quant. Biol. 62, 451-466.
22. Graff, J. M., Bansal, A. and Melton, D. A. (1996). Xenopus Mad proteins transduce distinct subsets of signals for the TGF-β superfamily. Cell 85, 479-487.
23. Gustafsson, M. K., Pan, H., Pinney, D. F., Liu, Y., Lewandowski, A., Epstein, D. J. and Emerson, C. P., Jr (2002). Myf5 is a direct target of long-range Shh signalling and Gli regulation for muscle specification. Genes Dev. 16, 114-126.
24. Hallikas, O., Palin, K., Sinjushina, N., Rautiainen, R., Partanen, J., Ukkonen, E. and Taipale, J. (2006). Genome-wide prediction of mammalian enhancers based on analysis of transcription-factor binding affinity. Cell 124, 47-59. (Pubitemid 43069309)
25. Hammerschmidt, M., Bitgood, M. J. and McMahon, A. P. (1996). Protein kinase A is a common negative regulator of Hedgehog signalling in the vertebrate embryo. Genes Dev. 10, 647-658. (Pubitemid 26112420)
26. Harvey, S. A. and Smith, J. C. (2009). Visualisation and quantification of morphogen gradient formation in the zebrafish. PLoS Biol. 7, e1000101.
27. Henningfeld, K. A., Rastegar, S., Adler, G. and Knochel, W. (2000). Smad1 and Smad4 are components of the bone morphogenetic protein-4 (BMP-4)- induced transcription complex of the Xvent-2B promoter. J. Biol. Chem. 275, 21827-21835.
28. Hirsinger, E., Stellabotte, F., Devoto, S. H. and Westerfield, M. (2004). Hedgehog signalling is required for commitment but not initial induction of slow muscle precursors. Dev. Biol. 275, 143-157.
29. Hoodless, P. A. (1996). MADR1, a MAD-related protein that functions in BMP2 signalling pathways. Cell 85, 489-500.
30. Hu, C. D., Chinenov, Y. and Kerppola, T. K. (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9, 789-798.
31. Humke, E. W., Dorn, K. V., Milenkovic, L., Scott, M. P. and Rohatgi, R. (2010). The output of Hedgehog signalling is controlled by the dynamic association between Suppressor of Fused and the Gli proteins. Genes Dev. 24, 670-682.
32. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signalling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087. (Pubitemid 33115673)
33. Ingham, P. W. and Kim, H. R. (2005). Hedgehog signalling and the specification of muscle cell identity in the zebrafish embryo. Exp. Cell Res. 306, 336-342.
34. Karlstrom, R. O., Tyurina, O. V., Kawakami, A., Nishioka, N., Talbot, W. S., Sasaki, H. and Schier, A. F. (2003). Genetic analysis of zebrafish gli1 and gli2 reveals divergent requirements for gli genes in vertebrate development. Development 130, 1549-1564.
35. Kawakami, A., Nojima, Y., Toyoda, A., Takahoko, M., Satoh, M., Tanaka, H., Wada, H., Masai, I., Terasaki, H., Sakaki, Y. et al. (2005). The zebrafish-secreted matrix protein you/scube2 is implicated in long-range regulation of hedgehog signalling. Curr. Biol. 15, 480-488.
36. Kawakami, T., Kawcak, T., Li, Y. J., Zhang, W., Hu, Y. and Chuang, P. T. (2002). Mouse dispatched mutants fail to distribute hedgehog proteins and are defective in hedgehog signalling. Development 129, 5753-5765.
37. Koudijs, M. J., den Broeder, M. J., Keijser, A., Wienholds, E., Houwing, S., van Rooijen, E. M., Geisler, R. and van Eeden, F. J. (2005). The zebrafish mutants dre, uki, and lep encode negative regulators of the hedgehog signalling pathway. PLoS Genet. 1, e19.
38. Koudijs, M. J., den Broeder, M. J., Groot, E. and van Eeden, F. J. (2008). Genetic analysis of the two zebrafish patched homologues identifies novel roles for the hedgehog signalling pathway. BMC Dev. Biol. 8, 15.
39. Krauss, S., Concordet, J. P. and Ingham, P. W. (1993). A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431-1444.
40. Kretzschmar, M., Liu, F., Hata, A., Doody, J. and Massague, J. (1997). The TGF-β family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11, 984-995. (Pubitemid 27199878)
41. Laner-Plamberger, S., Kaser, A., Paulischta, M., Hauser-Kronberger, C., Eichberger, T. and Frischauf, A. M. (2009). Cooperation between GLI and JUN enhances transcription of JUN and selected GLI target genes. Oncogene 28, 1639-1651.
42. Lee, E. C., Yu, D., Martinez de Velasco, J., Tessarollo, L., Swing, D. A., Court, D. L., Jenkins, N. A. and Copeland, N. G. (2001). A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73, 56-65.
43. Liem, K. F., Jr, Jessell, T. M. and Briscoe, J. (2000). Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development 127, 4855-4866.
44. Liew, H. P., Choksi, S. P., Wong, K. N. and Roy, S. (2008). Specification of vertebrate slow-twitch muscle fiber fate by the transcriptional regulator Blimp1. Dev. Biol. 324, 226-235.
45. Liu, F. (1996). A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381, 620-623.
46. Liu, F., Massague, J. and Ruiz i Altaba, A. (1998). Carboxy-terminally truncated Gli3 proteins associate with Smads. Nat. Genet. 20, 325-326.
47. Logan, C., Khoo, W. K., Cado, D. and Joyner, A. L. (1993). Two enhancer regions in the mouse En-2 locus direct expression to the mid/hindbrain region and mandibular myoblasts. Development 117, 905-916.
48. Ma, Y., Erkner, A., Gong, R., Yao, S., Taipale, J., Basler, K. and Beachy, P. A. (2002). Hedgehog-mediated patterning of the mammalian embryo requires transporter-like function of dispatched. Cell 111, 63-75.
49. Monteiro, R., van Dinther, M., Bakkers, J., Wilkinson, R., Patient, R., ten Dijke, P. and Mummery, C. (2008). Two novel type II receptors mediate BMP signalling and are required to establish left-right asymmetry in zebrafish. Dev. Biol. 315, 55-71.
50. Nakano, Y., Kim, H. R., Kawakami, A., Roy, S., Schier, A. F. and Ingham, P. W. (2004). Inactivation of dispatched 1 by the chameleon mutation disrupts Hedgehog signalling in the zebrafish embryo. Dev. Biol. 269, 381-392.
51. Nikaido, M., Tada, M. and Ueno, N. (1999). Restricted expression of the receptor serine/threonine kinase BMPR-IB in zebrafish. Mech. Dev. 82, 219-222.
52. Pan, Y., Wang, C. and Wang, B. (2009). Phosphorylation of Gli2 by protein kinase A is required for Gli2 processing and degradation and the Sonic Hedgehog-regulated mouse development. Dev. Biol. 326, 177-189.
53. Patten, I. and Placzek, M. (2002). Opponent activities of Shh and BMP signalling during floor plate induction in vivo. Curr. Biol. 12, 47-52.
54. Patterson, S. E., Bird, N. C. and Devoto, S. H. (2010). BMP regulation of myogenesis in zebrafish. Dev. Dyn. 239, 806-817.
55. Pearse, R. V., 2nd, Collier, L. S., Scott, M. P. and Tabin, C. J. (1999). Vertebrate homologs of Drosophila suppressor of fused interact with the gli family of transcriptional regulators. Dev. Biol. 212, 323-336.
56. Rissi, M., Wittbrodt, J., Délot, E., Naegeli, M. and Rosa, F. M. (1995). Zebrafish Radar: a new member of the TGF-β superfamily defines dorsal regions of the neural plate and the embryonic retina. Mech. Dev. 49, 223-234.
57. Roy, S., Wolff, C. and Ingham, P. W. (2001). The u-boot mutation identifies a Hedgehog-regulated myogenic switch for fiber-type diversification in the zebrafish embryo. Genes Dev. 15, 1563-1576.
58. Ruiz i Altaba, A. (1998). Combinatorial Gli gene function in floor plate and neuronal inductions by Sonic hedgehog. Development 125, 2203-2212.
59. Saka, Y., Hagemann, A. I., Piepenburg, O. and Smith, J. C. (2007). Nuclear accumulation of Smad complexes occurs only after the midblastula transition in Xenopus. Development 134, 4209-4218.
60. Sasaki, H., Hui, C., Nakafuku, M. and Kondoh, H. (1997). A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124, 1313-1322. (Pubitemid 27190104)
61. Scheer, N. and Campos-Ortega, J. A. (1999). Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mech. Dev. 80, 153-158.
62. Souren, M., Martinez-Morales, J., Makri, P., Wittbrodt, B. and Wittbrodt, J. (2009). A global survey identifies novel upstream components of the Ath5 neurogenic network. Genome Biol. 10, R92.
63. Stamataki, D., Ulloa, F., Tsoni, S. V., Mynett, A. and Briscoe, J. (2005). A gradient of Gli activity mediates graded Sonic Hedgehog signalling in the neural tube. Genes Dev. 19, 626-641. (Pubitemid 40314994)
64. Stone, D. M., Murone, M., Luoh, S., Ye, W., Armanini, M. P., Gurney, A., Phillips, H., Brush, J., Goddard, A., de Sauvage, F. J. et al. (1999). Characterization of the human suppressor of fused, a negative regulator of the zinc-finger transcription factor Gli. J. Cell Sci. 112, 4437-4448. (Pubitemid 30122035)
65. Suzuki, A., Chang, C., Yingling, J. M., Wang, X. F. and Hemmati-Brivvanlous, A. (1997). Smad5 induces ventral fates in Xenopus embryo. Dev. Biol. 184, 402-405.
66. Tanimoto, H., Itoh, S., ten Dijke, P. and Tabata, T. (2000). Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol. Cell 5, 59-71.
67. Thisse, B., Pflumio, S., Fürthauer, M., Loppin, B., Heyer, V., Degrave, A., Woehl, R., Lux, A., Steffan, T., Charbonnier, X. Q. et al. (2001). Expression of the zebrafish genome during embryogenesis (NIH R01 RR15402). ZFIN Direct Data Submission (http://zfin.org).
68. Thomsen, G. H. (1996). Xenopus mothers against decapentaplegic is an embryonic ventralizing agent that acts downstream of the BMP-2/4 receptor. Development 122, 2359-2366.
69. Ulloa, F., Itasaki, N. and Briscoe, J. (2007). Inhibitory Gli3 activity negatively regulates Wnt/beta-catenin signalling. Curr. Biol. 17, 545-550.
70. Urasaki, A., Morvan, G. and Kawakami, K. (2006). Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics 174, 639-649. (Pubitemid 44656456)
71. van Eeden, F. J., Granato, M., Schach, U., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J., Kane, D. A. et al. (1996). Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123, 153-164. (Pubitemid 27056744)
72. Varga, Z. M., Amores, A., Lewis, K. E., Yan, Y. L., Postlethwait, J. H., Eisen, J. S. and Westerfield, M. (2001). Zebrafish smoothened functions in ventral neural tube specification and axon tract formation. Development 128, 3497-3509. (Pubitemid 32962718)
73. Vokes, S. A., Ji, H., McCuine, S., Tenzen, T., Giles, S., Zhong, S., Longabaugh, W. J., Davidson, E. H., Wong, W. H. and McMahon, A. P. (2007). Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 134, 1977-1989. (Pubitemid 46939242)
74. Vokes, S. A., Ji, H., Wong, W. H. and McMahon, A. P. (2008). A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev. 22, 2651-2663.
75. von Hofsten, J., Elworthy, S., Gilchrist, M. J., Smith, J. C., Wardle, F. C. and Ingham, P. W. (2008). Prdm1- and Sox6-mediated transcriptional repression specifies muscle fibre type in the zebrafish embryo. EMBO Rep. 9, 683-689.
76. Wang, B., Fallon, J. F. and Beachy, P. A. (2000). Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100, 423-434.
77. Wen, X., Lai, C. K., Evangelista, M., Hongo, J.-A., de Sauvage, F. J. and Scales, S. J. (2010). Kinetics of Hedgehog-dependent full-length Gli3 accumulation in primary cilia and subsequent degradation. Mol. Cell. Biol. 30, 1910-1922.
78. Wieser, R., Wrana, J. L. and Massague, J. (1995). GS domain mutations that constitutively activate TβR-I, the downstream signalling component in the TGF-β receptor complex. EMBO J. 14, 2199-2208.
79. Winklmayr, M., Schmid, C., Laner-Plamberger, S., Kaser, A., Aberger, F., Eichberger, T. and Frischauf, A. M. (2010). Non-consensus GLI binding sites in Hedgehog target gene regulation. BMC Mol. Biol. 11, 2.
80. Wolff, C., Roy, S. and Ingham, P. W. (2003). Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo. Curr. Biol. 13, 1169-1181.