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. 1993 Oct;135(2):455–468. doi: 10.1093/genetics/135.2.455

Genetic Dissection of Pointed, a Drosophila Gene Encoding Two Ets-Related Proteins

H Scholz 1, J Deatrick 1, A Klaes 1, C Klambt 1
PMCID: PMC1205648  PMID: 8244007

Abstract

The Drosophila gene pointed (pnt) is required for the differentiation of a number of tissues during embryogenesis, including the ventral ectoderm, the nervous system, the tracheal system and certain muscle fibers. The phenotypes associated with strong pointed alleles are reflected by a complex pointed expression pattern during embryogenesis. Two promoters, P1 and P2, separated by some 50 kb of genomic sequences, direct the transcription of two different transcript forms, encoding two different proteins related to the ETS family of transcription factors. To assess the individual functions of the two different pointed protein forms, we have generated new pointed alleles affecting either the P1 or the P2 transcript, termed P1 and P2 alleles, respectively. Genetic analysis reveals partial heteroallelic complementation between certain pointed P1 and P2 alleles. Surviving trans-heterozygous flies have rough eyes, abnormal wings and halteres, suggesting a requirement for pointed function during their imaginal disc development. Further genetic analysis demonstrates that expression of a given pointed P2 allele depends on trans-acting transcriptional regulatory sequences. We have identified two chromosomal domains with opposite regulatory effects on the transcriptional activity of the pointed P2 promoter, one trans-activates and the other trans-represses pointed P2 expression. By deletion mapping we were able to localize these control regions within the 5' region of the pointed P2 transcript.

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Selected References

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  1. Ben-David Y., Giddens E. B., Letwin K., Bernstein A. Erythroleukemia induction by Friend murine leukemia virus: insertional activation of a new member of the ets gene family, Fli-1, closely linked to c-ets-1. Genes Dev. 1991 Jun;5(6):908–918. doi: 10.1101/gad.5.6.908. [DOI] [PubMed] [Google Scholar]
  2. Bryant P. J. Pattern formation in the imaginal wing disc of Drosophila melanogaster: fate map, regeneration and duplication. J Exp Zool. 1975 Jul;193(1):49–77. doi: 10.1002/jez.1401930106. [DOI] [PubMed] [Google Scholar]
  3. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dalton S., Treisman R. Characterization of SAP-1, a protein recruited by serum response factor to the c-fos serum response element. Cell. 1992 Feb 7;68(3):597–612. doi: 10.1016/0092-8674(92)90194-h. [DOI] [PubMed] [Google Scholar]
  5. Dreesen T. D., Henikoff S., Loughney K. A pairing-sensitive element that mediates trans-inactivation is associated with the Drosophila brown gene. Genes Dev. 1991 Mar;5(3):331–340. doi: 10.1101/gad.5.3.331. [DOI] [PubMed] [Google Scholar]
  6. Fitzpatrick V. D., Percival-Smith A., Ingles C. J., Krause H. M. Homeodomain-independent activity of the fushi tarazu polypeptide in Drosophila embryos. Nature. 1992 Apr 16;356(6370):610–612. doi: 10.1038/356610a0. [DOI] [PubMed] [Google Scholar]
  7. Freeman M., Kimmel B. E., Rubin G. M. Identifying targets of the rough homeobox gene of Drosophila: evidence that rhomboid functions in eye development. Development. 1992 Oct;116(2):335–346. doi: 10.1242/dev.116.2.335. [DOI] [PubMed] [Google Scholar]
  8. French V., Bryant P. J., Bryant S. V. Pattern regulation in epimorphic fields. Science. 1976 Sep 10;193(4257):969–981. doi: 10.1126/science.948762. [DOI] [PubMed] [Google Scholar]
  9. Heberlein U., Rubin G. M. Star is required in a subset of photoreceptor cells in the developing Drosophila retina and displays dosage sensitive interactions with rough. Dev Biol. 1991 Apr;144(2):353–361. doi: 10.1016/0012-1606(91)90427-5. [DOI] [PubMed] [Google Scholar]
  10. Henikoff S., Dreesen T. D. Trans-inactivation of the Drosophila brown gene: evidence for transcriptional repression and somatic pairing dependence. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6704–6708. doi: 10.1073/pnas.86.17.6704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hipskind R. A., Rao V. N., Mueller C. G., Reddy E. S., Nordheim A. Ets-related protein Elk-1 is homologous to the c-fos regulatory factor p62TCF. Nature. 1991 Dec 19;354(6354):531–534. doi: 10.1038/354531a0. [DOI] [PubMed] [Google Scholar]
  12. Jack J. W., Judd B. H. Allelic pairing and gene regulation: A model for the zeste-white interaction in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1368–1372. doi: 10.1073/pnas.76.3.1368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Judd B. H. Transvection: allelic cross talk. Cell. 1988 Jun 17;53(6):841–843. doi: 10.1016/s0092-8674(88)90209-7. [DOI] [PubMed] [Google Scholar]
  14. Klämbt C., Glazer L., Shilo B. Z. breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev. 1992 Sep;6(9):1668–1678. doi: 10.1101/gad.6.9.1668. [DOI] [PubMed] [Google Scholar]
  15. Klämbt C., Jacobs J. R., Goodman C. S. The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell. 1991 Feb 22;64(4):801–815. doi: 10.1016/0092-8674(91)90509-w. [DOI] [PubMed] [Google Scholar]
  16. Klämbt C. The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of the midline glial cells. Development. 1993 Jan;117(1):163–176. doi: 10.1242/dev.117.1.163. [DOI] [PubMed] [Google Scholar]
  17. Korge G. Direct correlation between a chromosome puff and the synthesis of a larval saliva protein in Drosophila melanogaster. Chromosoma. 1977 Jul 5;62(2):155–174. doi: 10.1007/BF00292637. [DOI] [PubMed] [Google Scholar]
  18. Kornher J. S., Brutlag D. Proximity-dependent enhancement of Sgs-4 gene expression in D. melanogaster. Cell. 1986 Mar 28;44(6):879–883. doi: 10.1016/0092-8674(86)90010-3. [DOI] [PubMed] [Google Scholar]
  19. LaMarco K., Thompson C. C., Byers B. P., Walton E. M., McKnight S. L. Identification of Ets- and notch-related subunits in GA binding protein. Science. 1991 Aug 16;253(5021):789–792. doi: 10.1126/science.1876836. [DOI] [PubMed] [Google Scholar]
  20. Mayer U., Nüsslein-Volhard C. A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes Dev. 1988 Nov;2(11):1496–1511. doi: 10.1101/gad.2.11.1496. [DOI] [PubMed] [Google Scholar]
  21. Rutledge B. J., Zhang K., Bier E., Jan Y. N., Perrimon N. The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes Dev. 1992 Aug;6(8):1503–1517. doi: 10.1101/gad.6.8.1503. [DOI] [PubMed] [Google Scholar]
  22. Schneikert J., Lutz Y., Wasylyk B. Two independent activation domains in c-Ets-1 and c-Ets-2 located in non-conserved sequences of the ets gene family. Oncogene. 1992 Feb;7(2):249–256. [PubMed] [Google Scholar]
  23. Simpson P., Grau Y. The segment polarity gene costal-2 in Drosophila. II. The origin of imaginal pattern duplications. Dev Biol. 1987 Jul;122(1):201–209. doi: 10.1016/0012-1606(87)90345-9. [DOI] [PubMed] [Google Scholar]
  24. Sturtevant M. A., Roark M., Bier E. The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGF-R signaling pathway. Genes Dev. 1993 Jun;7(6):961–973. doi: 10.1101/gad.7.6.961. [DOI] [PubMed] [Google Scholar]
  25. Tautz D., Pfeifle C. 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. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  26. Tei H., Nihonmatsu I., Yokokura T., Ueda R., Sano Y., Okuda T., Sato K., Hirata K., Fujita S. C., Yamamoto D. pokkuri, a Drosophila gene encoding an E-26-specific (Ets) domain protein, prevents overproduction of the R7 photoreceptor. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6856–6860. doi: 10.1073/pnas.89.15.6856. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Thomas J. B., Crews S. T., Goodman C. S. Molecular genetics of the single-minded locus: a gene involved in the development of the Drosophila nervous system. Cell. 1988 Jan 15;52(1):133–141. doi: 10.1016/0092-8674(88)90537-5. [DOI] [PubMed] [Google Scholar]
  28. Thompson C. C., Brown T. A., McKnight S. L. Convergence of Ets- and notch-related structural motifs in a heteromeric DNA binding complex. Science. 1991 Aug 16;253(5021):762–768. doi: 10.1126/science.1876833. [DOI] [PubMed] [Google Scholar]
  29. Wasylyk B., Hahn S. L., Giovane A. The Ets family of transcription factors. Eur J Biochem. 1993 Jan 15;211(1-2):7–18. doi: 10.1007/978-3-642-78757-7_2. [DOI] [PubMed] [Google Scholar]
  30. Wasylyk B., Wasylyk C., Flores P., Begue A., Leprince D., Stehelin D. The c-ets proto-oncogenes encode transcription factors that cooperate with c-Fos and c-Jun for transcriptional activation. Nature. 1990 Jul 12;346(6280):191–193. doi: 10.1038/346191a0. [DOI] [PubMed] [Google Scholar]
  31. Wasylyk C., Kerckaert J. P., Wasylyk B. A novel modulator domain of Ets transcription factors. Genes Dev. 1992 Jun;6(6):965–974. doi: 10.1101/gad.6.6.965. [DOI] [PubMed] [Google Scholar]

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