Siamois and Twin are redundant and essential in formation of the Spemann organizer

Developmental Biology

Volumn 352, Issue 2, 2011, Pages 367-381

  Bae, Sangwoo ^a,b   Reid, Christine D ^a   Kessler, Daniel S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Korea Institute of Radiation and Medical Science   (South Korea)

Author keywords

Goosecoid; Homeodomain; Organizer; Siamois; Transcription; Twin; Wnt

Indexed keywords

HETERODIMER; HOMODIMER; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SIAMOIS; TRANSCRIPTION FACTOR TWIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; EMBRYO; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC SIMILARITY; GOOSECOID GENE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; SPEMANN ORGANIZER; TRANSCRIPTION INITIATION;

SIA;

EID: 79953026088     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.01.034     Document Type: Article

References (59)

1. Blumberg B., Wright C.V., De Robertis E.M., Cho K.W. Organizer-specific homeobox genes in Xenopus laevis embryos. Science 1991, 253:194-196.
2. Blythe S.A., Cha S.W., Tadjuidje E., Heasman J., Klein P.S. beta-Catenin primes organizer gene expression by recruiting a histone H3 arginine 8 methyltransferase, Prmt2. Dev. Cell 2010, 19:220-231.
3. Blythe S.A., Reid C.D., Kessler D.S., Klein P.S. Chromatin immunoprecipitation in early Xenopus laevis embryos. Dev. Dyn. 2009, 238:1422-1432.
4. Brannon M., Gomperts M., Sumoy L., Moon R.T., Kimelman D. A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev. 1997, 11:2359-2370.
5. Brannon M., Kimelman D. Activation of Siamois by the Wnt pathway. Dev. Biol. 1996, 180:344-347.
6. Brenowitz M., Senear D.F., Kingston R.E. DNase I footprint analysis of protein-DNA binding. Curr. Protoc. Mol. Biol. 2001, Chapter 12, Unit 12 4.
7. Carnac G., Kodjabachian L., Gurdon J.B., Lemaire P. The homeobox gene Siamois is a target of the Wnt dorsalisation pathway and triggers organiser activity in the absence of mesoderm. Development 1996, 122:3055-3065.
8. Chen X., Rubock M.J., Whitman M. A transcriptional partner for MAD proteins in TGF-beta signalling. Nature 1996, 383:691-696.
9. Cho K.W., Blumberg B., Steinbeisser H., De Robertis E.M. Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 1991, 67:1111-1120.
10. Crease D.J., Dyson S., Gurdon J.B. Cooperation between the activin and Wnt pathways in the spatial control of organizer gene expression. Proc. Natl. Acad. Sci. USA 1998, 95:4398-4403.
11. De Robertis E.M. Goosecoid and Gastrulation. Gastrulation: From Cells to Embryo 2004, 581-590. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. C. Stern (Ed.).
12. De Robertis E.M. Spemann's organizer and self-regulation in amphibian embryos. Nat. Rev. Mol. Cell Biol. 2006, 7:296.
13. Engleka M.J., Kessler D.S. Siamois cooperates with TGFbeta signals to induce the complete function of the Spemann-Mangold organizer. Int. J. Dev. Biol. 2001, 45:241-250.
14. Fan M.J., Gruning W., Walz G., Sokol S.Y. Wnt signaling and transcriptional control of Siamois in Xenopus embryos. Proc. Natl. Acad. Sci. USA 1998, 95:5626-5631.
15. Fan M.J., Sokol S.Y. A role for Siamois in Spemann organizer formation. Development 1997, 124:2581-2589.
16. Fekany K., Yamanaka Y., Leung T., Sirotkin H.I., Topczewski J., Gates M.A., Hibi M., Renucci A., Stemple D., Radbill A., Schier A.F., Driever W., Hirano T., Talbot W.S., Solnica-Krezel L. The zebrafish bozozok locus encodes Dharma, a homeodomain protein essential for induction of gastrula organizer and dorsoanterior embryonic structures. Development 1999, 126:1427-1438.
17. Geisberg J.V., Struhl K. Quantitative sequential chromatin immunoprecipitation, a method for analyzing co-occupancy of proteins at genomic regions in vivo. Nucleic Acids Res. 2004, 32:e151.
18. Germain S., Howell M., Esslemont G.M., Hill C.S. Homeodomain and winged-helix transcription factors recruit activated Smads to distinct promoter elements via a common Smad interaction motif. Genes Dev. 2000, 14:435-451.
19. Harland R., Gerhart J. Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 1997, 13:611-667.
20. Heasman J. Patterning the early Xenopus embryo. Development 2006, 133:1205-1217.
21. Ishibashi H., Matsumura N., Hanafusa H., Matsumoto K., De Robertis E.M., Kuroda H. Expression of Siamois and Twin in the blastula Chordin/Noggin signaling center is required for brain formation in Xenopus laevis embryos. Mech. Dev. 2008, 125:58-66.
22. Kao K.R., Elinson R.P. Dorsalization of mesoderm induction by lithium. Dev. Biol. 1989, 132:81-90.
23. Kessler D.S. Siamois is required for formation of Spemann's organizer. Proc. Natl. Acad. Sci. USA 1997, 94:13017-13022.
24. Khokha M.K., Yeh J., Grammer T.C., Harland R.M. Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. Dev. Cell 2005, 8:401-411.
25. Kodjabachian L., Lemaire P. Siamois functions in the early blastula to induce Spemann's organiser. Mech. Dev. 2001, 108:71-79.
26. Kodjabachian L., Lemaire P. Role of Siamois before and during gastrulation. Gastrulation: From Cells to Embryo 2004, 609-617. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. C. Stern (Ed.).
27. Kofron M., Birsoy B., Houston D., Tao Q., Wylie C., Heasman J. Wnt11/beta-catenin signaling in both oocytes and early embryos acts through LRP6-mediated regulation of axin. Development 2007, 134:503-513.
28. Kofron M., Puck H., Standley H., Wylie C., Old R., Whitman M., Heasman J. New roles for FoxH1 in patterning the early embryo. Development 2004, 131:5065-5078.
29. Koos D.S., Ho R.K. The nieuwkoid/dharma homeobox gene is essential for bmp2b repression in the zebrafish pregastrula. Dev Biol. 1999, 215:190-207.
30. Kuo J.S., Patel M., Gamse J., Merzdorf C., Liu X., Apekin V., Sive H. Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. Development 1998, 125:2867-2882.
31. Laurent M.N., Blitz I.L., Hashimoto C., Rothbacher U., Cho K.W. The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann's organizer. Development 1997, 124:4905-4916.
32. Lemaire P., Garrett N., Gurdon J.B. Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. Cell 1995, 81:85-94.
33. Mochizuki T., Karavanov A.A., Curtiss P.E., Ault K.T., Sugimoto N., Watabe T., Shiokawa K., Jamrich M., Cho K.W., Dawid I.B., Taira M. Xlim-1 and LIM domain binding protein 1 cooperate with various transcription factors in the regulation of the goosecoid promoter. Dev. Biol. 2000, 224:470-485.
34. Nelson R.W., Gumbiner B.M. Beta-catenin directly induces expression of the Siamois gene, and can initiate signaling indirectly via a membrane-tethered form. Ann. NY Acad. Sci. 1998, 857:86-98.
35. Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin) 1967, North Holland Publishing Company, Amsterdam.
36. Nishita M., Hashimoto M.K., Ogata S., Laurent M.N., Ueno N., Shibuya H., Cho K.W. Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature 2000, 403:781-785.
37. Rivera-Perez J.A., Mallo M., Gendron-Maguire M., Gridley T., Behringer R.R. Goosecoid is not an essential component of the mouse gastrula organizer but is required for craniofacial and rib development. Development 1995, 121:3005-3012.
38. Sander V., Reversade B., De Robertis E.M. The opposing homeobox genes Goosecoid and Vent1/2 self-regulate Xenopus patterning. EMBO J. 2007, 26:2955-2965.
39. Sasai Y., Lu B., Steinbeisser H., Geissert D., Gont L.K., De Robertis E.M. Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 1994, 79:779-790.
40. Shibata M., Ono H., Hikasa H., Shinga J., Taira M. Xenopus crescent encoding a Frizzled-like domain is expressed in the Spemann organizer and pronephros. Mech. Dev. 2000, 96:243-246.
41. Shimizu T., Yamanaka Y., Ryu S.L., Hashimoto H., Yabe T., Hirata T., Bae Y.K., Hibi M., Hirano T. Cooperative roles of Bozozok/Dharma and Nodal-related proteins in the formation of the dorsal organizer in zebrafish. Mech. Dev. 2000, 91:293-303.
42. Sive H.L., Grainger R.M., Harland R.M. Early Development of Xenopus laevis: A Laboratory Manual 2000, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Sokol S., Christian J.L., Moon R.T., Melton D.A. Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 1991, 67:741-752.
44. Solnica-Krezel L., Driever W. The role of the homeodomain protein Bozozok in zebrafish axis formation. Int. J. Dev. Biol. 2001, 45:299-310.
45. Tao Q., Yokota C., Puck H., Kofron M., Birsoy B., Yan D., Asashima M., Wylie C.C., Lin X., Heasman J. Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. Cell 2005, 120:857-871.
46. Van de Peer Y., Maere S., Meyer A. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 2009, 10:725-732.
47. Wakamiya M., Lindsay E.A., Rivera-Perez J.A., Baldini A., Behringer R.R. Functional analysis of Gscl in the pathogenesis of the DiGeorge and velocardiofacial syndromes. Hum. Mol. Genet. 1998, 7:1835-1840.
48. Watabe T., Kim S., Candia A., Rothbacher U., Hashimoto C., Inoue K., Cho K.W. Molecular mechanisms of Spemann's organizer formation: conserved growth factor synergy between Xenopus and mouse. Genes Dev. 1995, 9:3038-3050.
49. Watanabe M., Whitman M. FAST-1 is a key maternal effector of mesoderm inducers in the early Xenopus embryo. Development 1999, 126:5621-5634.
50. White R. Homeodomain proteins. Homeotic genes seek partners. Curr. Biol. 1994, 4:48-50.
51. Wilson D., Sheng G., Lecuit T., Dostatni N., Desplan C. Cooperative dimerization of paired class homeo domains on DNA. Genes Dev. 1993, 7:2120-2134.
52. Wilson D.S., Guenther B., Desplan C., Kuriyan J. High resolution crystal structure of a paired (Pax) class cooperative homeodomain dimer on DNA. Cell 1995, 82:709-719.
53. Wilson P.A., Melton D.A. Mesodermal patterning by an inducer gradient depends on secondary cell-cell communication. Curr. Biol. 1994, 4:676-686.
54. Yaklichkin S., Steiner A.B., Lu Q., Kessler D.S. FoxD3 and Grg4 physically interact to repress transcription and induce mesoderm in Xenopus. J. Biol. Chem. 2007, 282:2548-2557.
55. Yamada G., Mansouri A., Torres M., Stuart E.T., Blum M., Schultz M., De Robertis E.M., Gruss P. Targeted mutation of the murine goosecoid gene results in craniofacial defects and neonatal death. Development 1995, 121:2917-2922.
56. Yamamoto S., Hikasa H., Ono H., Taira M. Molecular link in the sequential induction of the Spemann organizer: direct activation of the cerberus gene by Xlim-1, Xotx2, Mix.1, and Siamois, immediately downstream from Nodal and Wnt signaling. Dev. Biol. 2003, 257:190-204.
57. Yamanaka Y., Mizuno T., Sasai Y., Kishi M., Takeda H., Kim C.H., Hibi M., Hirano T. A novel homeobox gene, dharma, can induce the organizer in a non-cell-autonomous manner. Genes Dev. 1998, 12:2345-2353.
58. Yao J., Kessler D.S. Goosecoid promotes head organizer activity by direct repression of Xwnt8 in Spemann's organizer. Development 2001, 128:2975-2987.
59. Zhu C.C., Yamada G., Nakamura S., Terashi T., Schweickert A., Blum M. Malformation of trachea and pelvic region in goosecoid mutant mice. Dev. Dyn. 1998, 211:374-381.