In vivo interactions of the Drosophila Hairy and Runt transcriptional repressors with target promoters

EMBO Journal

Volumn 15, Issue 24, 1996, Pages 7088-7098

  Jiménez, Gerardo ^a   Pinchin, Sheena M ^a   Ish Horowicz, David ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Basic helix loop helix; Embryonic patterning; Segmentation; Sex determination; Transcriptional repression

Indexed keywords

DNA; REPRESSOR PROTEIN;

ARTICLE; BLASTODERM; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; DROSOPHILA; EMBRYO; EMBRYO SEGMENTATION; LETHALITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA INTERACTION; SEX DETERMINATION; TRANSCRIPTION REGULATION;

EID: 0030480103     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb01100.x     Document Type: Article

References (79)

1. Akazawa,C., Sasai,Y., Nakanishi,S. and Kageyama,R. (1992) Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system. J. Biol. Chem., 267, 21879-21885.
2. Anderson,K.V. and Nüsslein-Volhard,C. (1984) Information for the dorsal-ventral pattern of the Drosophila embryo is stored as maternal mRNA. Nature, 311, 223-227.
3. Badiani,P., Corbella,P., Kioussis,D., Marvel,J. and Weston,K. (1994) Dominant interfering alleles define a role for c-Myb in T-cell development. Genes Dev., 8, 770-782.
4. Bier,E., Vässin,H., Younger-Shepherd,S., Jan,L.Y. and Jan,Y.N. (1992) deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev., 6, 2137-2151.
5. Bopp,D., Bell,L.R., Cline,T.W. and Schedl,P. (1991) Developmental distribution of female-specific Sex-lethal proteins in Drosophila melanogaster. Genes Dev., 5, 403-415.
6. Brennan,T.J., Chakraborty,T. and Olson,E.N. (1991) Mutagenesis of the myogenin basic region identifies an ancient protein motif critical for activation of myogenesis. Proc. Natl Acad. Sci. USA, 88, 5675-5679.
7. Cabrera,C.V. and Alonso,M.C. (1991) Transcriptional activation by heterodimers of the achaete-scute and daughterless gene products of Drosophila. EMBO J., 10, 2965-2973.
8. Carroll,S.B. (1990) Zebra patterns in fly embryos: activation of stripes or repression of interstripes? Cell, 60, 9-16.
9. Carroll,S.B. and Scott,M.P. (1986) Zygotically active genes that affect the spatial expression of the fushi tarazu segmentation gene during early Drosophila embryogenesis. Cell, 45, 113-126.
10. Cline,T.W. (1993) The Drosophila sex determination signal - how do flies count to two? Trends Genet., 9, 385-390.
11. Coulter,D.E., Swaykus,E.A., Beran-Koehl,M.A., Goldberg,D., Wieschaus,E. and Schedl,P. (1990) Molecular analysis of odd-skipped, a zinc finger encoding segmentation gene with a novel pair-rule expression pattern. EMBO J., 9, 3795-3804.
12. Cousens,E.J., Greaves,R., Goding,C.R. and O'Hare,P. (1989) The C-terminal 79 amino acids of the herpes simplex virus regulatory protein, Vmw65, efficiently activate transcription in yeast and mammalian cells in chimeric DNA-binding proteins. EMBO J., 8, 2337-2342.
13. Davis,R.L. and Weintraub,H. (1992) Acquisition of myogenic specificity by replacement of three amino acid residues from MyoD into E12. Science, 256, 1027-1030.
14. Davis,R.L., Cheng,P.-F., Lassar,A.B. and Weintraub,H. (1990) The MyoD binding domain contains a recognition code for muscle-specific gene activation. Cell, 60, 733-746.
15. Dawson,S.R., Turner,D.L., Weintraub,H. and Parkhurst,S.M. (1995) Specificity for the Hairy/Enhancer of split basic helix-loop-helix (bHLH) proteins maps outside the bHLH domain and suggests two separable modes of transcriptional repression. Mol. Cell. Biol., 15, 6923-6931.
16. Dearolf,C.R., Topol,J. and Parker,C.S. (1989) Transcriptional control of Drosophila fushi tarazu zebra stripe expression. Genes Dev., 3, 384-398.
17. Delidakis,C. and Artavanis-Tsakonas,S. (1992) The Enhancer-of-split [E(spl)] locus of Drosophila encodes seven independent helix-loop-helix proteins. Proc. Natl Acad. Sci. USA, 89, 8731-8735.
18. Delidakis,C., Preiss,A., Hartley,D.A. and Artavanis-Tsakonas,S. (1991) Two genetically and molecularly distinct functions involved in early neurogenesis reside within the Enhancer-of-split locus of Drosophila melanogaster. Genetics, 129, 803-823.
19. Duffy,J.B. and Gergen,J.P. (1991) The Drosophila segmentation gene runt acts as a position-specific numerator element necessary for the uniform expression of the sex-determining gene Sex-lethal. Genes Dev., 5, 2176-2187.
20. Frasch,M. and Levine,M. (1987) Complementary patterns of even-skipped and fushi tarazu expression involve their differential regulation by a common set of segmentation genes in Drosophila. Genes Dev., 1, 981-995.
21. Goodrich,J.A., Cutler,G. and Tjian,R. (1996) Contacts in context - promoter specificity and macromolecular interactions in transcription. Cell, 84, 825-830.
22. Hartley,D.A., Preiss,A. and Artavanis-Tsakonas,S. (1988) A deduced gene product from the Drosophila neurogenic locus, Enhancer-of-split, shows homology to mammalian G-protein beta subunit. Cell, 55, 785-795.
23. Hartmann,C., Taubert,H., Jäckle,H. and Pankratz,M.J. (1994) A 2-step mode of stripe formation in the Drosophila blastoderm requires interactions among primary pair-rule genes. Mech. Dev., 45, 3-13.
24. Hemesath,T.J. et al. (1994) microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes Dev., 8, 2770-2780.
25. Higuchi,R., Krummel,B. and Saiki,R.K. (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res., 16, 7351-7364.
26. Hiromi,Y. and Gehring,W.J. (1987) Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell, 50, 963-974.
27. Holmgren,R. (1984) Cloning sequences from the hairy gene of Drosophila. EMBO J., 3, 569-573.
28. Hooper,K.L., Parkhurst,S.M. and Ish-Horowicz,D. (1989) Spatial control of hairy protein expression during embryogenesis. Development, 107, 489-504.
29. Hoshijima,K., Kohyama,A., Watakabe,I., Inoue,K., Sakamoto,H. and Shimura,Y. (1995) Transcriptional regulation of the Sex-lethal gene by helix-loop-helix proteins. Nucleic Acids Res., 23, 3441-3448.
30. Howard,K. and Ingham,P. (1986) Regulatory interactions between the segmentation genes fushi tarazu, hairy and engrailed in the Drosophila blastoderm. Cell, 44, 949-957.
31. Ingham,P.W. and Gergen,J.P. (1988) Interactions between the pair-rule genes runt, hairy, even-skipped and fushi tarazu and the establishment of periodic pattern in the Drosophila embryo. In French,V., Ingham,P.W., Cooke,J. and Smith,J. (eds), Mechanisms of Segmentation. Development, Suppl. 104, pp. 51-60.
32. Ingham,P.W., Pinchin,S.M., Howard,K.R. and Ish-Horowicz,D. (1985) Genetic analysis of the hairy locus in Drosophila melanogaster. Genetics, 111, 463-486.
33. Ish-Horowicz,D. and Pinchin,S.M. (1987) Pattern abnormalities induced by ectopic expression of the Drosophila gene hairy are associated with repression of fushi tarazu transcription. Cell, 51, 405-415.
34. Ish-Horowicz,D., Pinchin,S.M., Ingham,P.W. and Gyurkovics,H.G. (1989) Autocalalytic ftz activation and metameric instability induced by ectopic ftz expression. Cell, 57, 223-232.
35. Ishibashi,M., Sasai,Y., Nakanishi,S. and Kageyama,R. (1993) Molecular characterization of HES-2, a mammalian helix-loop-helix factor structurally related to Drosophila hairy and Enhancer of split. Eur. J. Biochem., 215, 645-652.
36. John,A., Smith,S.T. and Jaynes,J.B. (1995) Inserting the ftz homeodomain into engrailed creates a dominant transcriptional represser that specifically turns off ftz target genes in vivo. Development, 121, 1801-1813.
37. Kagoshima,H., Shigesada,K., Satake,M., Ito,Y., Miyoshi,H., Ohki,M., Pepling,M. and Gergen,P. (1993) The Runt domain identifies a new family of heteromeric transcriptional regulators. Trends Genet., 9, 338-341.
38. Kania,M.A., Bonner,A.S., Duffy,J.B. and Gergen,J.P. (1990) The Drosophila segmentation gene runt encodes a novel nuclear regulatory protein that is also expressed in the developing nervous system. Genes Dev., 4, 1701-1713.
39. King,V., Korn,R., Kwok,C., Ramkissoon,Y., Wunderle,V. and Goodfellow,P. (1995) Sex determination - one for a boy, two for a girl? Curr. Biol., 5, 37-39.
40. Klämbt,C., Knust,E., Tietze,K. and Campos-Ortega,J.A. (1989) Closely related transcripts encoded by the neurogenic gene complex Enhancer of split of Drosophila melanogaster. EMBO J., 8, 203-210.
41. Klingler,M. and Gergen,J.P. (1993) Regulation of runt transcription by Drosophila segmentation genes. Mech. Dev., 43, 3-19.
42. Knust,E., Schrons,H., Grawe,F. and Campos-Ortega,J.A. (1992) Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics, 132, 505-518.
43. Kreig,P.A. and Melton,D.A. (1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res., 12, 7057-7070.
44. Ma,J. and Ptashne,M. (1987) Deletion analysis of GAL4 defines two transcriptional activating segments. Cell, 48, 847-853.
45. Ma,P.C., Rould,M.A., Weintraub,H. and Pabo,C.O. (1994) Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell, 77, 451-459.
46. Manoukian,A.S. and Krause,H.M. (1992) Concentration-dependent regulatory activities of the even-skipped protein in Drosophila embryos. Genes Dev., 6, 1740-1751.
47. Manoukian,A.S. and Krause,H.M. (1993) Control of segmental asymmetry in Drosophila embryos. Development, 118, 785-796.
48. Murre,C., Schonleber McCaw,P. and Baltimore,D. (1989a) A new DNA binding and dimerisation motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell, 56, 777-783.
49. Murre,C. et al. (1989b) Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell, 58, 537-544.
50. Oellers,N., Dehio,M. and Knust,E. (1994) bHLH proteins encoded by the Enhancer of split complex of Drosophila negatively interfere with transcriptional activation mediated by proneural genes. Mol. Gen. Genet., 244, 465-473.
51. Ogawa,E., Maruyama,M., Kagoshima,H., Inuzuka,M., Lu,J., Satake,M., Shigesada,K. and Ito,Y. (1993) PEBP2/PEA2 represents a family of transcription factors homologous to the products of the Drosophila runt gene and the human AMLI gene. Proc. Natl Acad. Sci. USA, 90, 6859-6863.
52. Ohsako,S., Hyer,J., Panganiban,G., Oliver,J. and Caudy,M. (1994) Hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev., 8, 2743-2755.
53. Pankratz,M.J. and Jäckle,H. (1993) Blastoderm segmentation. In Bate,M. and Martinez-Arias,A. (eds). The Development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 467-516.
54. Parkhurst,S.M. and Meneely,P.M. (1994) Sex determination and dosage compensation: lessons from flies and worms. Science, 264, 924-932.
55. Parkhurst,S.M., Bopp,D. and Ish-Horowicz,D. (1990) X:A ratio, the primary sex determining signal in Drosophila, is transduced by helix-loop-helix proteins. Cell, 63, 1179-1191.
56. Parkhurst,S.M., Lipshitz,H.D. and Ish-Horowicz,D. (1993) achaete-scute feminizing activities and Drosophila sex determination. Development, 117, 737-749.
57. Paroush,Z., Finley,R.L.Jr, Kidd,T., Wainwright,S.M., Ingham,P.W., Brent,R. and Ish-Horowicz,D. (1994) Groucho is required for Drosophila neurogenesis, segmentation and sex-determination, and interacts directly with Hairy-related bHLH proteins. Cell, 79, 805-815.
58. Pirrotta,V. (1988) Vectors for P-mediated transformation in Drosophila. In Rodriquez,R.L. and Denhanrdt,D.T. (eds), Vectors, a Survey of Molecular Cloning Vectors and their Uses. Butterworth, Boston. MA, pp. 437-456.
59. Rushlow,C.A., Hogan,A., Pinchin,S.M., Howe,K.R., Lardelli,M.T. and Ish-Horowicz,D. (1989) The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J., 8, 3095-3103.
60. Sadowski,I., Ma,J., Triezenberg,S. and Ptashne,M. (1988) GAL4-VP16 is an unusually potent transcriptional activator. Nature, 335, 563-564.
61. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
62. Sasai,Y., Kageyama,R., Tagawa,Y., Shigemoto,R. and Nakanishi,S. (1992) Two mammalian helix loop helix factors structurally related to Drosophila hairy and Enhancer-of-split. Genes Dev., 6, 2620-2634.
63. Schrons,H., Knust,E. and Campos-Ortega,J.A. (1992) The Enhancer of split complex and adjacent genes in the 96F region of Drosophila melanogaster are required for segregation of neural and epidermal progenitor cells. Genetics, 132, 481-503.
64. Spradling,A.C. (1986) P element-mediated transformation. In Roberts,D.B. (ed.), Drosophila: A Practical Approach. IRL Press, Oxford, UK, pp. 175-197.
65. Steller,H. and Pirrotta,V. (1985) A transposable P vector that confers G418 resistance to Drosophila larvae. EMBO J., 4, 167-171.
66. Struhl,G. (1985) Near-reciprocal phenotypes caused by inactivation or indiscriminate expression of the Drosophila segmentation gene ftz. Nature, 318, 677-680.
67. Takebayashi,K., Sasai,Y., Sakai,Y., Watanabe,T., Nakanishi,S. and Kageyama,R. (1994) Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-1. J. Biol. Chem., 269, 5150-5156.
68. 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.
69. D, a dominant mutation of Drosophila, and its use in the study of functional domains of a helix-loop-helix protein. Proc. Natl Acad. Sci. USA, 89, 6152-6156.
70. Tietze,K., Schrons,H., Campos-Ortega,J.A. and Knust,E. (1993) A functional-analysis of the genes Enhancer of split and HLH-m5 during early neurogenesis in Drosophila melanogaster. Roux's Arch. Dev. Biol., 203, 10-17.
71. Topol,J., Dearolf,C.R., Prakash,K. and Parker,C.S. (1991) Synthetic oligonucleotides recreate Drosophila fushi tarazu zebra-stripe expression. Genes Dev., 5, 855-867.
72. Triezenberg,S.J., Kingsbury,R.C. and McKnight,S.L. (1988) Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes Dev., 2, 718-729.
73. Tsai,C. and Gergen,J.P. (1994) Gap gene properties of the pair-rule gene runt during Drosophila segmentation. Development, 120, 1671-1683.
74. Tsai,C. and Gergen,P. (1995) Pair-rule expression of the Drosophila fushi tarazu gene - a nuclear receptor response element mediates the opposing regulatory effects of runt and hairy. Development, 121, 453-462.
75. van Doren,M., Bailey,A.M., Esnayra,J., Ede,K. and Posakony,J.W. (1994) Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete. Genes Dev., 8, 2729-2742.
76. Wainwright,S.M. and Ish-Horowicz,D. (1992) Point mutations in the Drosophila hairy gene demonstrate in vivo requirements for basic, helix-loop-helix, and WRPW domains. Mol. Cell. Biol., 12, 2475-2483.
77. Weintraub,H., Dwarki,V.J., Verma,I., Davis,R., Hollenberg,S., Snider,L., Lassar,A. and Tapscott,S.J. (1991) Muscle-specific transcriptional activation by MyoD. Genes Dev., 5, 1377-1386.
78. Wieschaus,E. and Nüsslein-Volhard,C. (1986) Looking at embryos. In Roberts,D.B. (ed.), Drosophila: A Practical Approach. IRL Press, Oxford, UK, pp. 199-226.
79. Younger-Shepherd,S., Vässin,H., Bier,E., Jan,L.Y. and Jan,Y.N. (1992) deadpan, an essential pan-neural gene encoding an HLH protein, acts as a denominator in Drosophila sex determination. Cell, 70, 911-922.