The Torso signaling pathway modulates a dual transcriptional switch to regulate tailless expression

Nucleic Acids Research

Volumn 37, Issue 4, 2009, Pages 1061-1072

  Chen, Yu Chien ^a   Lin, Suewei I ^a,c   Chen, Ying Kuan ^a   Chiang, Chuen Sheue ^b   Liaw, Gwo Jen ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b CENTER FOR DISEASE CONTROL   (Taiwan)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; NONHISTONE PROTEIN; PROTEIN GAF; PROTEIN GAGA; PROTEIN TAILLESS; PROTEIN TORSO; REPRESSOR PROTEIN; TRAMTRACK69 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRITHORAX LIKE TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE ACTIVITY; GENE EXPRESSION; GENE REPRESSION; GENE SWITCHING; GENETIC TRANSCRIPTION; GENOTYPE; MALE; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; WILD TYPE;

ANIMALS; DNA FOOTPRINTING; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTOR PROTEIN-TYROSINE KINASES; REPRESSOR PROTEINS; RESPONSE ELEMENTS; RNA INTERFERENCE; SERINE; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 62549149947     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn1036     Document Type: Article

References (76)

1. Li,W.X. (2005) Functions and mechanisms of receptor tyrosine kinase Torso signaling: Lessons from Drosophila embryonic terminal development. Dev. Dyn., 232, 656-672.
2. Schlessinger,J. (2000) Cell signaling by receptor tyrosine kinases. Cell, 103, 211-225.
3. Hill,C.S. and Treisman,R. (1995) Transcriptional regulation by extracellular signals: Mechanisms and specificity. Cell, 80, 199-211.
4. Barolo,S. and Posakony,J.W. (2002) Three habits of highly effective signaling pathways: Principles of transcriptional control by developmental cell signaling. Genes Dev., 16, 1167-1181.
5. Sprenger,F., Stevens,L.M. and Nusslein-Volhard,C. (1989) The Drosophila gene torso encodes a putative receptor tyrosine kinase. Nature, 338, 478-483.
6. St Johnston,D. and Nusslein-Volhard,C. (1992) The origin of pattern and polarity in the Drosophila embryo. Cell, 68, 201-219.
7. Furriols,M. and Casanova,J. (2003) In and out of Torso RTK signalling. EMBO J., 22, 1947-1952.
8. Sprenger,F. and Nusslein-Volhard,C. (1992) Torso receptor activity is regulated by a diffuusible ligand produced at the extracellular terminal regions of the Drosophila egg. Cell, 71, 987-1001.
9. Strecker,T.R., Kongsuwan,K., Lengyel,J.A. and Merriam,J.R. (1986) The zygotic mutant tailless affects the anterior and posterior ectodermal regions of the Drosophila embryo. Dev. Biol., 113, 64-76.
10. Pignoni,F., Baldarelli,R.M., Steingrimsson,E., Diaz,R.J., Patapoutian,A., Merriam,J.R. and Lengyel,J.A. (1990) The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell, 62, 151-163.
11. Pignoni,F., Steingrimsson,E. and Lengyel,J.A. (1992) bicoid and the terminal system activate tailless expression in the early Drosophila embryo. Development, 115, 239-251.
12. Liaw,G.J. and Lengyel,J.A. (1992) Control of tailless expression by bicoid, dorsal and synergistically interacting terminal system regulatory elements. Mech. Dev., 40, 47-61.
13. Liaw,G.J., Rudolph,K.M., Huang,J.D., Dubnico.,T., Courey,A.J. and Lengyel,J.A. (1995) The torso response element binds GAGA and NTF-1/Elf-1, and regulates tailless by relief of repression. Genes Dev., 9, 3163-3176.
14. Liaw,G.J., Steingrimsson,E., Pignoni,F., Courey,A.J. and Lengyel,J.A. (1993) Characterization of downstream elements in a Raf-1 pathway. Proc. Natl Acad. Sci. USA, 90, 858-862.
15. Brown,J.L. and Wu,C. (1993) Repression of Drosophila pair-rule segmentation genes by ectopic expression of tramtrack. Development 117, 45-58.
16. Chen,Y.J., Chiang,C.S., Weng,L.C., Lengyel,J.A. and Liaw,G.J. (2002) Tramtrack69 is required for the early repression of tailless expression. Mech. Dev., 116, 75-83.
17. Wen,Y., Nguyen,D., Li,Y. and Lai,Z.C. (2000) The N-terminal BTB/POZ domain and C-terminal sequences are essential for Tramtrack69 to specify cell fate in the developing Drosophila eye. Genetics, 156 195-203.
18. Jimenez,G., Guichet,A., Ephrussi,A. and Casanova,J. (2000) Relief of gene repression by torso RTK signaling: Role of capicua in Drosophila terminal and dorsoventral patterning. Genes Dev., 14, 224-231.
19. Paroush,Z., Wainwright,S.M. and Ish-Horowicz,D. (1997) Torso signalling regulates terminal patterning in Drosophila by antagonising Groucho-mediated repression. Development, 124, 3827-3834.
20. Farkas,G., Gausz,J., Galloni,M., Reuter,G., Gyurkovics,H. and Karch,F. (1994) The Trithorax-like gene encodes the Drosophila GAGA factor. Nature, 371, 806-808.
21. Pedone,P.V., Ghirlando,R., Clore,G.M., Gronenborn,A.M., Felsenfeld,G. and Omichinski,J.G. (1996) The single Cys2-His2 zinc finger domain of the GAGA protein flanked by basic residues is sufficient for high-affinity specific DNA binding. Proc. Natl Acad. Sci. USA, 93, 2822-2826.
22. Adkins,N.L., Hagerman,T.A. and Georgel,P. (2006) GAGA protein: A multi-faceted transcription factor. Biochem. Cell Biol., 84, 559-567.
23. Lehmann,M. (2004) Anything else but GAGA: A nonhistone protein complex reshapes chromatin structure. Trends Genet., 20, 15-22.
24. Tsukiyama,T., Becker,P.B. and Wu,C. (1994) ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature, 367, 525-532.
25. Mason,P.B. Jr and Lis,J.T. (1997) Cooperative and competitive protein interactions at the hsp70 promoter. J. Biol. Chem., 272 33227-33233.
26. Clos,J., Rabindran,S., Wisniewski,J. and Wu,C. (1993) Induction temperature of human heat shock factor is reprogrammed in a Drosophila cell environment. Nature, 364, 252-255.
27. Morimoto,R.I. (1993) Cells in stress: Transcriptional activation of heat shock genes. Science, 259, 1409-1410.
28. Morimoto,R.I. (1998) Regulation of the heat shock transcriptional response: Cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev., 12, 3788-3796.
29. Calderwood,S.K. (2005) Regulatory interfaces between the stress protein response and other gene expression programs in the cell. Methods, 35, 139-148.
30. Inouye,S., Fujimoto,M., Nakamura,T., Takaki,E., Hayashida,N., Hai,T. and Nakai,A. (2007) Heat shock transcription factor 1 opens chromatin structure of interleukin-6 promoter to facilitate binding of an activator or a repressor. J. Biol. Chem., 282, 33210-33217.
31. Shi,Y., Mosser,D.D. and Morimoto,R.I. (1998) Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev., 12, 654-666.
32. Xiong,W.C. and Montell,C. (1993) tramtrack is a transcriptional repressor required for cell fate determination in the Drosophila eye. Genes Dev., 7, 1085-1096.
33. Jedlicka,P., Mortin,M.A. and Wu,C. (1997) Multiple functions of Drosophila heat shock transcription factor in vivo. EMBO J., 16, 2452-2462.
34. Greenspan, R.J. (2004) Fly Pushing: The Theory and Practice of Drosophila Genetics, 2nd edn. Cold Spring Harbor Laboratory Press, New York.
35. Chou,T.B., Noll,E. and Perrimon,N. (1993) Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras. Development, 119, 1359-1369.
36. Rorth,P. (1998) Gal4 in the Drosophila female germline. Mech. Dev., 78, 113-118.
37. Lee,Y.S. and Carthew,R.W. (2003) Making a better RNAi vector for Drosophila: Use of intron spacers. Methods, 30, 322-329.
38. Rubin,G.M. and Spradling,A.C. (1983) Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res., 11, 6341-6351.
39. Spradling,A.C. and Rubin,G.M. (1983) The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell 34, 47-57.
40. Janody,F., Reischl,J. and Dostatni,N. (2000) Persistence of Hunchback in the terminal region of the Drosophila blastoderm embryo impairs anterior development. Development, 127, 1573-1582.
41. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. (1994) Current Protocols in Molecular Biology. John Wiley & Sons, Inc., New York.
42. Studier,F.W. and Moffatt,B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned gene. J. Mol. Biol., 189, 113-130.
43. Studier,F.W., Rosenberg,A.H., Dunn,J.J. and Dubendor.,J.W. (1990) Use of T7 RNA polymerase to direct the expression of cloned gene. Methods Enzymol., 185, 60-89.
44. Zhong,M. and Wu,C. (1996) Proteolytic mapping of heat shock transcription factor domains. Protein Sci., 5, 2592-2599.
45. Kadonaga,J.T., Carner,K.R., Masiarz,F.R. and Tjian,R. (1987) Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain. Cell, 51, 1079-1090.
46. Demczuk,S., Harbers,M. and Vennstrom,B. (1993) Identification and analysis of all components of a gel retardation assay by combination with immunoblotting. Proc. Natl Acad. Sci. USA, 90, 2574-2578.
47. Rothwell,W.F. and Sullivan,W. (2000) In Sullivan,W., Ashbourner,M. and Hawley,R.S. (eds), Drosophila Protocols, Cold Spring Harbor Laboratory Press, New York, pp. 141-157.
48. Tautz,D. and Pfeifle,C. (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma, 98, 81-85.
49. Singh,A., Kango,M. and Sinha,P. (1995) An improved method for chemical devitellinization of X-gal stained Drosophila embryos. Indian J. Exp. Biol., 33, 150-152.
50. Bernues,J., Pineyro,D. and Kosoy,A. (2007) General, negative feedback mechanism for regulation of Trithorax-like gene expression in vivo: New roles for GAGA factor in flies. Nucleic Acids Res., 35, 7150-7159.
51. Espinas,M.L., Jimenez-Garcia,E., Vaquero,A., Canudas,S., Bernues,J. and Azorin,F. (1999) The N-terminal POZ domain of GAGA mediates the formation of oligomers that bind DNA with high affinity and specificity. J. Biol. Chem., 274, 16461-16469.
52. Pagans,S., Pineyro,D., Kosoy,A., Bernues,J. and Azorin,F. (2004) Repression by TTK69 of GAGA-mediated activation occurs in the absence of TTK69 binding to DNA and solely requires the contribution of the POZ/BTB domain of TTK69. J. Biol. Chem., 279, 9725-9732.
53. Pagans,S., Ortiz-Lombardia,M., Espinas,M.L., Bernues,J. and Azorin,F. (2002) The Drosophila transcription factor tramtrack (TTK) interacts with Trithorax-like (GAGA) and represses GAGA-mediated activation. Nucleic Acids Res., 30, 4406-4413.
54. Aalfs,J.D. and Kingston,R.E. (2000) What does 'chromatin remodeling' mean? Trends Biochem. Sci., 25, 548-555.
55. Bantignies,F. and Cavalli,G. (2006) Cellular memory and dynamic regulation of polycomb group proteins. Curr. Opin. Cell Biol., 18, 275-283.
56. Muller,J. and Kassis,J.A. (2006) Polycomb response elements and targeting of Polycomb group proteins in Drosophila. Curr. Opin. Genet. Dev., 16, 476-484.
57. Fazzio,T.G., Kooperberg,C., Goldmark,J.P., Neal,C., Basom,R., Delrow,J. and Tsukiyama,T. (2001) Widespread collaboration of Isw2 and Sin3-Rpd3 chromatin remodeling complexes in transcriptional repression. Mol. Cell Biol., 21, 6450-6460.
58. Narlikar,G.J., Fan,H.Y. and Kingston,R.E. (2002) Cooperation between complexes that regulate chromatin structure and transcription. Cell 108, 475-487.
59. Chu,B., Soncin,F., Price,B.D., Stevenson,M.A. and Calderwood,S.K. (1996) Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J. Biol. Chem., 271, 30847-30857.
60. Davis,R.J. (1993) The mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem., 268, 14553-14556.
61. Li,W.X., Agaisse,H., Mathey-Prevot,B. and Perrimon,N. (2002) Differential requirement for STAT by gain-of-function and wild-type receptor tyrosine kinase Torso in Drosophila. Development, 129 4241-4248.
62. Granok,H., Leibovitch,B.A., Shaffer,C.D. and Elgin,S.C. (1995) Chromatin. Ga-ga over GAGA factor. Curr. Biol., 5, 238-241.
63. TenHarmsel,A., Austin,R.J., Savenelli,N. and Biggin,M.D. (1993) Cooperative binding at a distance by even-skipped protein correlates with repression and suggests a mechanism of silencing. Mol. Cell Biol., 13, 2742-2752.
64. Ahmad,K.F., Engel,C.K. and Prive,G.G. (1998) Crystal structure of the BTB domain from PLZF. Proc. Natl Acad. Sci. USA, 95, 12123-12128.
65. Farkas,T., Kutskova,Y.A. and Zimarino,V. (1998) Intramolecular repression of mouse heat shock factor 1. Mol. Cell Biol., 18 906-918.
66. Mishra,M. and Deora,R. (2005) Mode of action of the Bordetella BvgA protein: Transcriptional activation and repression of the Bordetella bronchiseptica bipA promoter. J. Bacteriol., 187, 6290-6299.
67. Shimada,T., Fujita,N., Maeda,M. and Ishihama,A. (2005) Systematic search for the Cra-binding promoters using genomic SELEX system. Genes Cells 10, 907-918.
68. Huang,J.D., Schwyter,D.H., Shirokawa,J.M. and Courey,A.J. (1993) The interplay between multiple enhancer and silencer elements defines the pattern of decapentaplegic expression. Genes Dev., 7, 694-704.
69. Harris,M.B., Mostecki,J. and Rothman,P.B. (2005) Repression of an interleukin-4-responsive promoter requires cooperative BCL-6 function. J. Biol. Chem., 280, 13114-13121.
70. Luo,W. and Skalnik,D.G. (1996) CCAAT displacement protein competes with multiple transcriptional activators for binding to four sites in the proximal gp91phox promoter. J. Biol. Chem., 271, 18203-18210.
71. Ashe,H.L. and Briscoe,J. (2006) The interpretation of morphogen gradients. Development, 133, 385-394.
72. Lebrecht,D., Foehr,M., Smith,E., Lopes,F.J., Vanario-Alonso,C.E., Reinitz,J., Burz,D.S. and Hanes,S.D. (2005) Bicoid cooperative DNA binding is critical for embryonic patterning in Drosophila. Proc. Natl Acad. Sci. USA, 102, 13176-13181.
73. Yamamoto,A., Mizukami,Y. and Sakurai,H. (2005) Identification of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae. J. Biol. Chem., 280, 11911-11919.
74. Dickson,B. (1995) Nuclear factors in sevenless signalling. Trends Genet., 11, 106-111.
75. Rebay,I. (2002) Keeping the receptor tyrosine kinase signaling pathway in check: Lessons from Drosophila. Dev. Biol., 251, 1-17.
76. Gaston,K. and Jayaraman,P.S. (2003) Transcriptional repression in eukaryotes: Repressors and repression mechanisms. Cell Mol. Life Sci. 60, 721-741.