The relative role of the T-domain and flanking sequences for developmental control and transcriptional regulation in protein chimeras of Drosophila OMB and ORG-1

Mechanisms of Development

Volumn 122, Issue 1, 2005, Pages 81-96

  Porsch, Matthias ^a   Sauer, Markus ^a   Schulze, Sabine ^a   Bahlo, Angela ^a   Roth, Martin ^a   Pflugfelder, Gert O ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Antenna; Developmental control; Domain swap; Drosophila; Eye; Omb; Org 1; T box; Transcription factor

Indexed keywords

INSECT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTENNA; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; DNA FLANKING REGION; DROSOPHILA; EYE DEVELOPMENT; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; LEG; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; QUALITATIVE ANALYSIS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSGENE;

ANIMALS; CHIMERA; CLONING, MOLECULAR; DROSOPHILA; DROSOPHILA PROTEINS; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TRANSFER TECHNIQUES; MICROSCOPY, ELECTRON, SCANNING; NERVE TISSUE PROTEINS; PROTEIN STRUCTURE, TERTIARY; T-BOX DOMAIN PROTEINS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION, GENETIC; TRANSGENES;

INVERTEBRATA; VERTEBRATA;

EID: 9944255121     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2004.08.007     Document Type: Article

References (91)

1. P. Agarwal, J.N. Wylie, J. Galceran, O. Arkhitko, C. Li, and C. Deng Tbx5 is essential for forelimb bud initiation following patterning of the limb field in the mouse embryo Development 130 2003 623 633
2. M. Bamshad, R.C. Lin, D.J. Law, W.S. Watkins, P.A. Krakowiak, and M.E. Moore Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome Nat. Genet. 16 1997 311 315
3. A.H. Brand, and N. Perrimon Targeted gene expression as a means of altering cell fates and generating dominant phenotypes Development 118 1993 401 415
4. B.G. Bruneau, G. Nemer, J.P. Schmitt, F. Charron, L. Robitaille, and S. Caron A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease Cell 106 2001 709 721
5. P.J. Bryant Pattern formation in imaginal discs M. Ashburner T.R.F. Wright Genetics and Biology of Drosophila vol. 2c 1978 Academic Press New York 230 335
6. K.M. Cadigan, and R. Nusse Wingless signaling in the Drosophila eye and embryonic epidermis Development 122 1996 2801 2812
7. H. Carlson, S. Ota, C.E. Campbell, and P.J. Hurlin A dominant repression domain in Tbx3 mediates transcriptional repression and cell immortalization: relevance to mutations in Tbx3 that cause ulnar-mammary syndrome Hum. Mol. Genet. 10 2001 2403 2413
8. S. Carreira, T.J. Dexter, U. Yavuzer, D.J. Easty, and C.R. Goding Brachyury-related transcription factor Tbx2 and repression of the melanocyte-specific TRP-1 promoter Mol. Cell. Biol. 18 1998 5099 5108
9. E.S. Casey, M.A. O'Reilly, F.L. Conlon, and J.C. Smith The T-box transcription factor Brachyury regulates expression of eFGF through binding to a non-palindromic response element Development 125 1998 3887 3894
10. E.S. Casey, M. Tada, L. Fairclough, C.C. Wylie, J. Heasman, and J.C. Smith Bix4 is activated directly by VegT and mediates endoderm formation in Xenopus development Development 126 1999 4193 4200
11. S.K. Chan, and R.S. Mann The segment identity functions of ultrabithorax are contained within its homeo domain and carboxy-terminal sequences Genes Dev. 7 1993 796 811
12. D.L. Chapman, N. Garvey, S. Hancock, M. Alexiou, S.I. Agulnik, and J.J. Gibson-Brown Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development Dev. Dyn. 206 1996 379 390
13. S. Chauvet, S. Merabet, D. Bilder, M.P. Scott, J. Pradel, and Y. Graba Distinct hox protein sequences determine specificity in different tissues Proc. Natl Acad. Sci. USA 97 2000 4064 4069
14. J. Chen, Q. Zhong, J. Wang, R.S. Cameron, J.L. Borke, C.M. Isales, and R.J. Bollag Microarray analysis of Tbx2-directed gene expression: a possible role in osteogenesis Mol. Cell. Endocrinol. 177 2001 43 54
15. J.R. Chen, B. Chatterjee, R. Meyer, J.C. Yu, J.L. Borke, and C.M. Isales Tbx2 represses expression of Connexin43 in osteoblastic-like cells Calcif. Tissue Int. 17 2004 17
16. A. Collavoli, C.J. Hatcher, J. He, D. Okin, R. Deo, and C.T. Basson TBX5 nuclear localization is mediated by dual cooperative intramolecular signals J. Mol. Cell. Cardiol. 35 2003 1191 1195
17. F.L. Conlon, L. Fairclough, B.M. Price, E.S. Casey, and J.C. Smith Determinants of T box protein specificity Development 128 2001 3749 3758
18. D. Del Alamo Rodriguez, J. Terriente Felix, and F.J. Diaz-Benjumea The role of the T-box gene optomotor-blind in patterning the Drosophila wing Dev. Biol. 268 2004 481 492
19. U. Dietrich, and J. Campos-Ortega The expression of neurogenic loci in imaginal epidermal cells of Drosophila melanogaster J. Neurogenet. 1 1984 315 322
20. A. Di Gregorio, and M. Levine Regulation of Ci-tropomyosin-like, a Brachyury target gene in the ascidian, Ciona intestinalis Development 126 1999 5599 5609
21. M.C. Ellis, E.M. O'Neill, and G.M. Rubin Expression of Drosophila glass protein and evidence for negative regulation of its activity in non-neuronal cells by another DNA-binding protein Development 119 1993 855 865
22. A. Erives, and M. Levine Characterization of a maternal T-Box gene in Ciona intestinalis Dev. Biol. 225 2000 169 178
23. C. Fan, M. Liu, and Q. Wang Functional analysis of TBX5 missense mutations associated with Holt-Oram syndrome J. Biol. Chem. 278 2003 8780 8785 (Epub 2002 December 23)
24. K. Furukubo-Tokunaga, S. Flister, and W.J. Gehring Functional specificity of the Antennapedia homeodomain Proc. Natl Acad. Sci. USA 90 1993 6360 6364
25. R. Galant, and S.B. Carroll Evolution of a transcriptional repression domain in an insect Hox protein Nature 415 2002 910 913
26. M.D. Galibert, U. Yavuzer, T.J. Dexter, and C.R. Goding Pax3 and regulation of the melanocyte-specific tyrosinase-related protein-1 promoter J. Biol. Chem. 274 1999 26894 26900
27. V. Garg, I.S. Kathiriya, R. Barnes, M.K. Schluterman, I.N. King, and C.A. Butler GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5 Nature 424 2003 443 447
28. T.K. Ghosh, E.A. Packham, A.J. Bonser, T.E. Robinson, S.J. Cross, and J.D. Brook Characterization of the TBX5 binding site and analysis of mutations that cause Holt-Oram syndrome Hum. Mol. Genet. 10 2001 1983 1994
29. J.J. Gibson-Brown, S.I. Agulnik, D.L. Chapman, M. Alexiou, N. Garvey, L.M. Silver, and V.E. Papaioannou Evidence of a role for T-box genes in the evolution of limb morphogenesis and the specification of forelimb/hindlimb identity Mech. Dev. 56 1996 93 101
30. L.M. Goering, K. Hoshijima, B. Hug, B. Bisgrove, A. Kispert, and D.J. Grunwald An interacting network of T-box genes directs gene expression and fate in the zebrafish mesoderm Proc. Natl Acad. Sci. USA 100 2003 9410 9415 (Epub 2003 July 25)
31. Grimm, S, 1997. Das T-Box Protein Optomotor-blind von Drosophila melanogaster: DNA-Bindungseigenschaften und die Rolle in der Imaginalentwicklung, Dissertation Thesis, Universität Würzburg.
32. S. Grimm, and G.O. Pflugfelder Control of the gene optomotor-blind in Drosophila wing development by decapentaplegic and wingless Science 271 1996 1601 1603
33. P.E. Habets, A.F. Moorman, D.E. Clout, M.A. van Roon, M. Lingbeek, and M. van Lohuizen Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation Genes Dev. 16 2002 1234 1246
34. G. Halder, P. Callaerts, and W.J. Gehring Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila Science 267 1995 1788 1792
35. M. He, L. Wen, C.E. Campbell, J.Y. Wu, and Y. Rao Transcription repression by Xenopus ET and its human ortholog TBX3, a gene involved in ulnar-mammary syndrome [published erratum appears in Proc Natl Acad Sci USA 1999 Nov 9;96(23):13589] Proc. Natl Acad. Sci. USA 96 1999 10212 10217
36. A. Heicklen-Klein, and T. Evans T-box binding sites are required for activity of a cardiac GATA-4 enhancer Dev. Biol. 267 2004 490 504
37. B.G. Herrmann, S. Labeit, A. Poustka, T.R. King, and H. Lehrach Cloning of the T gene required in mesoderm formation in the mouse Nature 343 1990 617 622
38. Y. Hiroi, S. Kudoh, K. Monzen, Y. Ikeda, Y. Yazaki, R. Nagai, and I. Komuro Tbx5 associates with Nkx2-5 and synergistically promotes cardiomyocyte differentiation Nat. Genet. 28 2001 276 280
39. J.J. Jacobs, P. Keblusek, E. Robanus-Maandag, P. Kristel, M. Lingbeek, and P.M. Nederlof Senescence bypass screen identifies TBX2, which represses Cdkn2a (p19(ARF)) and is amplified in a subset of human breast cancers Nat. Genet. 26 2000 291 299
40. L.A. Jerome, and V.E. Papaioannou DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1 Nat. Genet. 27 2001 286 291
41. Y. Kamachi, K.S. Cheah, and H. Kondoh Mechanism of regulatory target selection by the SOX high-mobility-group domain proteins as revealed by comparison of SOX1/2/3 and SOX9 Mol. Cell. Biol. 19 1999 107 120
42. A. Kispert The Brachyury protein: a T-domain transcription factor Semin. Dev. Biol. 6 1995 395 403
43. A. Kispert, and B.G. Herrmann The Brachyury gene encodes a novel DNA binding protein Eur. Mol. Biol. Org. J. 12 1993 3211 3220
44. A. Kispert, B.G. Herrmann, M. Leptin, and R. Reuter Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila, Tribolium, and Locusta Genes Dev. 8 1994 2137 2150
45. A. Kispert, B. Koschorz, and B.G. Herrmann The T protein encoded by Brachyury is a tissue-specific transcription factor Eur. Mol. Biol. Org. J. 14 1995 4763 4772
46. A. Kopp, and I. Duncan Control of cell fate and polarity in the abdominal segments of Drosophila by optomotor-blind Development 124 1997 3715 3726
47. A. Kopp, and I. Duncan Anteroposterior patterning in adult abdominal segments of Drosophila Dev. Biol. 242 2002 15 30
48. T. Kusch, and R. Reuter Functions for Drosophila brachyenteron and forkhead in mesoderm specification and cell signalling Development 126 1999 3991 4003
49. T. Kusch, T. Storck, U. Walldorf, and R. Reuter Brachyury proteins regulate target genes through modular binding sites in a cooperative fashion Genes Dev. 16 2002 518 529
50. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
51. B. Lamolet, A.M. Pulichino, T. Lamonerie, Y. Gauthier, T. Brue, A. Enjalbert, and J. Drouin A pituitary cell-restricted T box factor, Tpit, activates POMC transcription in cooperation with Pitx homeoproteins Cell 104 2001 849 859
52. H.H. Lee, A. Norris, J.B. Weiss, and M. Frasch Jelly belly protein activates the receptor tyrosine kinase Alk to specify visceral muscle pioneers Nature 425 2003 507 512
53. X. Li, and W. McGinnis Activity regulation of Hox proteins, a mechanism for altering functional specificity in development and evolution Proc. Natl Acad. Sci. USA 96 1999 6802 6807
54. L. Lin, and W. McGinnis Mapping functional specificity in the Dfd and Ubx homeo domains Genes Dev. 6 1992 1071 1081
55. E.A. Lindsay, F. Vitelli, H. Su, M. Morishima, T. Huynh, and T. Pramparo Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice Nature 410 2001 97 101
56. M.E. Lingbeek, J.J. Jacobs, and M. van Lohuizen The T-box repressors TBX2 and TBX3 specifically regulate the tumor suppressor gene p14ARF via a variant T-site in the initiator J. Biol. Chem. 277 2002 26120 26127
57. M. Logan, and C.J. Tabin Role of Pitx1 upstream of Tbx4 in specification of hindlimb identity (see comments) Science 283 1999 1736 1739
58. S. Marcellini, U. Technau, J.C. Smith, and P. Lemaire Evolution of Brachyury proteins: identification of a novel regulatory domain conserved within Bilateria Dev. Biol. 260 2003 352 361
59. S. Merscher, B. Funke, J.A. Epstein, J. Heyer, A. Puech, and M.M. Lu TBX1 is responsible for cardiovascular defects in velo-cardio- facial/DiGeorge syndrome Cell 104 2001 619 629
60. Y. Mitani, H. Takahashi, and N. Satoh Regulation of the muscle-specific expression and function of an ascidian T-box gene, As-T2 Development 128 2001 3717 3728
61. C.W. Müller, and B.G. Herrmann Crystallographic structure of the T domain-DNA complex of the Brachyury transcription factor Nature 389 1997 884 888
62. R. Murakami, A. Shigenaga, M. Kawakita, K. Takimoto, I. Yamaoka, K. Akasaka, and H. Shimada Aproctous, a locus that is necessary for the development of the proctodeum in Drosophila embryos, encodes a homolog of the vertebrate Brachyury gene Roux's Arch. Dev. Biol. 205 1995 89 96
63. E.A. Packham, and J.D. Brook T-box genes in human disorders Hum. Mol. Genet. 12 2003 R37 R44
64. V.E. Papaioannou T-box genes in development: from hydra to humans Int. Rev. Cytol. 207 2001 1 70
65. C. Papapetrou, Y.H. Edwards, and J.C. Sowden The T transcription factor functions as a dimer and exhibits a common human polymorphism Gly-177-Asp in the conserved DNA-binding domain Fed. Eur. Biochem. Soc. Lett. 409 1997 201 206
66. C. Paxton, H. Zhao, Y. Chin, K. Langner, and J. Reecy Murine Tbx2 contains domains that activate and repress gene transcription Gene 283 2002 117 124
67. G.O. Pflugfelder, and M. Heisenberg Optomotor-blind of Drosophila melanogaster: a neurogenetic approach to optic lobe development and optomotor behaviour Comp. Biochem. Physiol. 110A 1995 185 202
68. G.O. Pflugfelder, H. Roth, B. Poeck, S. Kerscher, H. Schwarz, B. Jonschker, and M. Heisenberg The lethal(1)optomotor-blind gene of Drosophila melanogaster is a major organizer of optic lobe development: isolation and charcterization of the gene Proc. Natl Acad. Sci. USA 89 1992 1199 1203
69. G.O. Pflugfelder, H. Roth, and B. Poeck A homology domain shared between Drosophila melanogaster and mouse Brachyury is involved in DNA binding Biochem. Biophys. Res. Commun. 186 1992 918 925
70. B. Poeck, A. Hofbauer, and G.O. Pflugfelder Expression of the Drosophila optomotor-blind gene transcript in neuronal and glial cells of the developing nervous system Development 117 1993 1017 1029
71. M. Porsch, K. Hofmeyer, B.S. Bausenwein, S. Grimm, B.H.F. Weber, R. Miassod, and G.O. Pflugfelder Isolation of a Drosophila T-box gene closely related to human TBX1 Gene 212 1998 237 248
72. S. Prince, S. Carreira, K.W. Vance, A. Abrahams, and C.R. Goding Tbx2 directly represses the expression of the p21(WAF1) cyclin-dependent kinase inhibitor Cancer Res. 64 2004 1669 1674
73. C. Rodriguez-Esteban, T. Tsukui, S. Yonei, J. Magallon, K. Tamura, and J.C. Izpisua Belmonte The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identity (see comments) Nature 398 1999 814 818
74. M. Ronshaugen, N. McGinnis, and W. McGinnis Hox protein mutation and macroevolution of the insect body plan Nature 415 2002 914 917
75. I. Ruvinsky, and J.J. Gibson-Brown Genetic and developmental bases of serial homology in vertebrate limb evolution Development 127 2000 5233 5244
76. P. Santamaria Injecting eggs D.B. Roberts Drosophila: A Practical Approach 1986 IRL Press Oxford, Washington DC 159 173
77. C.S. Sinclair, C. Adem, A. Naderi, C.L. Soderberg, M. Johnson, and K. Wu TBX2 is preferentially amplified in BRCA1- and BRCA2-related breast tumors Cancer Res. 62 2002 3587 3591
78. J.B. Singer, R. Harbecke, T. Kusch, R. Reuter, and J.A. Lengyel Drosophila brachyenteron regulates gene activity and morphogenesis in the gut Development 122 1996 3707 3718
79. S. Sinha, S. Abraham, R.M. Gronostajski, and C.E. Campbell Differential DNA binding and transcription modulation by three T-box proteins, T, TBX1 and TBX2 Gene 258 2000 15 29
80. E.M. Small, and P.A. Krieg Transgenic analysis of the atrialnatriuretic factor (ANF) promoter: Nkx2-5 and GATA-4 binding sites are required for atrial specific expression of ANF Dev. Biol. 261 2003 116 131
81. W.P. Spencer D. robusta. New mutant report Drosophila Inf. Serv. 20 1946 78 81
82. A.C. Spradling P element-mediated transformation D.B. Roberts Drosophila: A Practical Approach 1986 IRL Press Oxford 175 198
83. T.L. Sreenath, R.A. Pollock, and C.J. Bieberich Functional specificity of Hoxa-4 in vertebral patterning lies outside of the homeodomain Proc. Natl Acad. Sci. USA 93 1996 9636 9640
84. K. Staehling-Hampton, P.D. Jackson, M.J. Clark, A.H. Brand, and F.M. Hoffmann Specificity of bone morphogenetic protein-related factors: cell fate and gene expression changes in Drosophila embryo induced by decapentaplegic but not 60A Cell Growth Differ. 5 1994 585 593
85. F.A. Stennard, M.W. Costa, D.A. Elliott, S. Rankin, S.J. Haast, and D. Lai Cardiac T-box factor Tbx20 directly interacts with Nkx2-5, GATA4, and GATA5 in regulation of gene expression in the developing heart Dev. Biol. 262 2003 206 224
86. M. Tada, E.S. Casey, L. Fairclough, and J.C. Smith Bix1, a direct target of Xenopus T-box genes, causes formation of ventral mesoderm and endoderm Development 125 1998 3997 4006
87. H. Takahashi, Y. Mitani, G. Satoh, and N. Satoh Evolutionary alterations of the minimal promoter for notochord-specific Brachyury expression in ascidian embryos Development 126 1999 3725 3734
88. J.K. Takeuchi, K. Koshiba-Takeuchi, K. Matsumoto, A. Vogel-Hopker, M. Naitoh-Matsuo, and K. Ogura Tbx5 and Tbx4 genes determine the wing/leg identity of limb buds Nature 398 1999 810 814
89. J.K. Takeuchi, M. Ohgi, K. Koshiba-Takeuchi, H. Shiratori, I. Sakaki, and K. Ogura Tbx5 specifies the left/right ventricles and ventricular septum position during cardiogenesis Development 130 2003 5953 5964 Epub 2003 Oct. 22
90. W. Zeng, D.J. Andrew, L.D. Mathies, M.A. Horner, and M.P. Scott Ectopic expression and function of the Antp and Scr homeotic genes: the N terminus of the homeodomain is critical to functional specificity Development 118 1993 339 352
91. J. Zhang, and M.L. King Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning Development 122 1996 4119 4129