Schnurri transcription factors from Drosophila and vertebrates can mediate Bmp signaling through a phylogenetically conserved mechanism

Development

Volumn 133, Issue 20, 2006, Pages 4025-4034

  Yao, Li Chin ^a   Blitz, Ira L ^a   Peiffer, Daniel A ^a   Phin, Sopheap ^a   Wang, Ying ^a   Ogata, Souichi ^a   Cho, Ken W Y ^a   Arora, Kavita ^a   Warrior, Rahul ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bmp; Bone morphogenetic protein signaling; Evolutionary conservation; Schnurri; Smad; Transcription; Transcriptional activation; Transcriptional repression

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; DECAPENTAPLEGIC PROTEIN; SIGNAL PEPTIDE; SMAD PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SCHNURRI; TRANSCRIPTION FACTOR SHN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; BIOTRANSFORMATION; CELL CULTURE; CONSERVATION GENETICS; DROSOPHILA; GENE REPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC CONSERVATION; INSECT DEVELOPMENT; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PHYLOGENY; PRIORITY JOURNAL; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; XENOPUS;

ANIMALIA; ANURA; VERTEBRATA;

EID: 33751050017     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02561     Document Type: Article

References (56)

1. Affolter, M., Marty, T., Vigano, M. A. and Jazwinska, A. (2001). Nuclear interpretation of Dpp signaling in Drosophila. EMBO J. 20, 3298-3305.
2. Arora, K., Dai, H., Kazuko, S. G., Jamal, J., O'Connor, M. B., Letsou, A. and Warrior, R. (1995). The Drosophila schnurri gene acts in the Dpp/ TGFβ signaling pathway and encodes a transcription factor homologous to the human MBP family. Cell 81, 781-790.
3. Barolo, S., Carver, L. A. and Posakony, J. W. (2000). GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques 29, 726-732.
4. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
5. Bray, S. J. and Kafatos, F. C. (1991). Developmental function of Elf-1: an essential transcription factor during embryogenesis in Drosophila. Genes Dev. 5, 1672-1683.
6. Campbell, G. and Tomlinson, A. (1999). Transducing the Dpp morphogen gradient in the wing of Drosophila: regulation of Dpp targets by brinker. Cell 96, 553-562.
7. Candia, A. F., Watabe, T., Hawley, S. H., Onichtchouk, D., Zhang, Y., Derynck, R., Niehrs, C. and Cho, K. W. (1997). Cellular interpretation of multiple TGF-beta signals: intracellular antagonism between activin/ BVg1 and BMP-2/4 signaling mediated by Smads. Development 124, 4467-4480.
8. Dai, H., Hogan, C., Gopalakrishnan, B., Torres-Vazquez, J., Nguyen, M., Park, S., Raftery, L. A., Warrior, R. and Arora, K. (2000). The zinc finger protein schnurri acts as a Smad partner in mediating the transcriptional response to decapentaplegic. Dev. Biol. 227, 373-387.
9. Dorfman, R. and Shilo, B. Z. (2001). Biphasic activation of the BMP pathway patterns the Drosophila embryonic dorsal region. Development 128, 965-972.
10. Durr, U., Henningfeld, K. A., Hollemann, T., Knochel, W. and Pieler, T. (2004). Isolation and characterization of the Xenopus HIVEP gene family. Eur. J. Biochem. 271, 1135-1144.
11. Fan, C. M. and Maniatis, T. (1990). A DNA-binding protein containing two widely separated zinc finger motifs that recognize the same DNA sequence. Genes Dev. 4, 29-42.
12. Furriols, M. and Bray, S. (2001). A model Notch response element detects Suppressor of Hairless-dependent molecular switch. Curr. Biol. 11, 60-64.
13. Gao, S. and Laughon, A. (2006). DPP-responsive silencers contain overlapping mad binding sites. J. Biol. Chem. Doi: 10.1074/ jbc.M603371200.
14. Gao, S., Steffen, J. and Laughon, A. (2005). Dpp-responsive silencers are bound by a trimeric Mad-Medea complex. J. Biol. Chem. 280, 36158-36164.
15. Gonzalez-Crespo, S. and Levine, M. (1994). Related target enhancers for Dorsal and NF-κB signaling pathways. Science 264, 255-258.
16. Grieder, N. C., Nellen, D., Burke, R., Basler, K. and Affolter M. (1995). schnurri is required for Drosophila Dpp signaling and encodes a zinc finger protein similar to the mammalian transcription factor PRDII-BF1. Cell 81, 791-800.
17. Hata, A., Seoane, J., Lagna, G., Montalvo, E., Hemmati-Brivanlou, A. and Massague, J. (2000). OAZ uses distinct DNA- and protein-binding zinc fingers in separate BMP-Smad and Olf signaling pathways. Cell 100, 229-240.
18. Hayward, D. C., Samuel, G., Pontynen, P. C., Catmull, J., Saint, R., Miller, D. J. and Ball, E. E. (2002). Localized expression of a dpp/BMP2/ 4 ortholog in a coral embryo. Proc. Natl. Acad. Sci. USA 99, 8106-8111.
19. 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.
20. Holstein, T. W., Hobmayer, E. and Technau, U. (2003). Cnidarians: an evolutionarily conserved model system for regeneration? Dev. Dyn. 226, 257-267.
21. Jin, W., Takagi, T., Kanesashi, S. N., Kurahashi, T., Nomura, T., Harada, J. and Ishii, S. (2006). Schnurri-2 controls BMP-dependent adipogenesis via interaction with Smad proteins. Dev. Cell 10, 461-471.
22. Johnson, K., Kirkpatrick, H., Comer, A., Hoffmann, F. M. and Laughon, A. (1999). Interaction of Smad complexes with tripartite DNA-binding sites. J. Biol. Chem. 274, 20709-20716.
23. Karaulanov, E., Knochel, W. and Niehrs, C. (2004). Transcriptional regulation of BMP4 synexpression in transgenic Xenopus. EMBO J. 23, 844-856.
24. Kim, J., Johnson, K., Chen, H. J., Carroll, S. and Laughon, A. (1997). Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature 388, 304-308.
25. Kirov, N., Childs, S., O'Connor, M. and Rushlow, C. (1994). The Drosophila dorsal morphogen represses the tolloid gene by interacting with a silencer element. Mol. Cell. Biol. 14, 713-722.
26. Kroll, K. L. and Amaya, E. (1996). Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. Development 122, 3173-3183.
27. Liang, J., Lints, R., Foehr, M. L., Tokarz, R., Yu, L., Emmons, S. W., Liu, J. and Savage-Dunn, C. (2003). The Caenorhabditis elegans schnurri homolog sma-9 mediates stage- and cell type-specific responses to DBL-1 BMP-related signaling. Development 130, 6453-6464.
28. Ludwig, M. Z. (2002). Functional evolution of noncoding DNA. Curr. Opin. Genet. Dev. 12, 634-639.
29. Mace, K. A., Pearson, J. C. and McGinnis, W. (2005). An epidermal barrier wound repair pathway in Drosophila is mediated by grainy head. Science 308, 381-385.
30. Marty, T., Muller, B., Basler, K. and Affolter, M. (2000). Schnurri mediates Dpp-dependent repression of brinker transcription. Nat. Cell Biol. 2, 745-749.
31. Massague, J., Seoane, J. and Wotton, D. (2005). Smad transcription factors. Genes Dev. 19, 2783-2810.
32. Muller, B., Hartmann, B., Pyrowolakis, G., Affolter, M. and Basler K. (2003). Conversion of an extracellular Dpp/BMP morphogen gradient into an inverse transcriptional gradient. Cell 113, 221-233.
33. Niehrs, C. and Pollet, N. (1999). Synexpression groups in eukaryotes. Nature 402, 483-487.
34. Onichtchouk, D., Gawantka, V., Dosch, R., Delius, H., Hirschfeld, K., Blumenstock, C. and Niehrs, C. (1996). The Xvent-2 homeobox gene is part of the BMP-4 signalling pathway controlling [correction of controling] dorsoventral patterning of Xenopus mesoderm. Development 122, 3045-3053.
35. Oukka, M., Kim, S. T., Lugo, G., Sun, J., Wu, L. C. and Glimcher, L. H. (2002). A mammalian homolog of Drosophila schnurri, KRC, regulates TNF receptor-driven responses and interacts with TRAF2. Mol. Cell 9, 121-131.
36. Oukka, M., Wein, M. N. and Glimcher, L. H. (2004). Schnurri-3 (KRC) interacts with c-Jun to regulate the IL-2 gene in T cells. J. Exp. Med. 199, 15-24.
37. Padgett, R. W., Wozney, J. M. and Gelbart, W. M. (1993). Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 90, 2905-2909.
38. Pyrowolakis, G., Hartmann, B., Muller, B., Basler, K. and Affolter, M. (2004). A simple molecular complex mediates widespread BMP-induced repression during Drosophila development. Dev. Cell 7, 229-240.
39. Raftery, L. A. and Sutherland, D. J. (1999). TGF-beta family signal transduction in Drosophila development: from Mad to Smads. Dev. Biol. 210, 251-268.
40. Rastegar, S., Friedle, H., Frommer, G. and Knochel, W. (1999). Transcriptional regulation of Xvent homeobox genes. Mech. Dev. 81, 139-149.
41. Sampath, T. K., Rashka, K. E., Doctor, J. S., Tucker, R. F. and Hoffmann, F. M. (1993). Drosophila transforming growth factor beta superfamily proteins induce endochondral bone formation in mammals. Proc. Natl. Acad. Sci. USA 90, 6004-6008.
42. Shi, Y. and Massague, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113, 685-700.
43. Staehling-Hampton, K., Laughon, A. S. and Hoffmann, F. M. (1995). Drosophila protein related to the human zinc finger transcription factor PRDII/MBPI/HIV-EP1 is required for dpp signaling. Development 121, 3393-3403.
44. Sutherland, D. J., Li, M., Liu, X. Q., Stefancsik, R. and Raftery, L. A. (2003). Stepwise formation of a SMAD activity gradient during dorsal-ventral patterning of the Drosophila embryo. Development 130, 5705-5716.
45. Suzuki, A., Thies, R. S., Yamaji, N., Song, J. J., Wozney, J. M., Murakami, K. and Ueno, N. (1994). A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. USA 91, 10255-10259.
46. 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.
47. Tautz, D. (2000). Evolution of transcriptional regulation. Curr. Opin. Genet. Dev 10, 575-579.
48. Torres-Vazquez, J., Warrior, R. and Arora, K. (2000). schnurri is required for dpp-dependent patterning of the Drosophila wing. Dev. Biol. 227, 388-402.
49. Torres-Vazquez, J., Park, S., Warrior, R. and Arora, K. (2001). The transcription factor Schnurri plays a dual role in mediating Dpp signaling during embryogenesis. Development 128, 1657-1670.
50. Udagawa, Y., Hanai, J., Tada, K., Grieder, N. C., Momoeda, M., Taketani, Y., Affolter, M., Kawabata, M. and Miyazono, K. (2000). Schnurri interacts with Mad in a Dpp-dependent manner. Genes Cells 5, 359-369.
51. von Bubnoff, A., Peiffer, D. A., Blitz, I. L., Hayata, T., Ogata, S., Zeng, Q., Trunnell, M. and Cho, K. W. (2005). Phylogenetic footprinting and genome scanning identify vertebrate BMP response elements and new target genes. Dev. Biol. 281, 210-226.
52. Watabe, T., Kim, S., Candia, A., Rothbacher, U., Hashimoto, C., Inoue, K. and Cho, K. W. (1995). Molecular mechanisms of Spemann's organizer formation: conserved growth factor synergy between Xenopus and mouse. Genes Dev. 9, 3038-3050.
53. Wu, L. C. (2002). ZAS: C2H2 zinc finger proteins involved in growth and development. Gene Expr 10, 137-152.
54. Xu, X., Yin, Z., Hudson, J. B., Ferguson, E. L. and Frasch, M. (1998). Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev. 12, 2354-2370.
55. Yang, X., Li, J., Qin, H., Yang, H., Li, J., Zhou, P., Liang, Y. and Han, H. (2005). Mint represses transactivation of the type II collagen gene enhancer through interaction with alpha A-crystallin-binding protein 1. J. Biol. Chem. 280, 18710-18716.
56. Zhao, G. Q. (2003). Consequences of knocking out BMP signaling in the mouse. Genesis 35, 43-56.