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. 1995 Dec;15(12):6943–6952. doi: 10.1128/mcb.15.12.6943

Regulation of Drosophila yolk protein genes by an ovary-specific GATA factor.

M Lossky 1, P C Wensink 1
PMCID: PMC230949  PMID: 8524261

Abstract

The divergently transcribed yolk protein genes (Yp1 and Yp2) of Drosophila melanogaster are expressed only in adult females, in fat body tissue and in ovarian follicle cells. Using an in vitro transcription assay, we have identified a single 12-bp DNA element that activates transcription from the promoters of both Yp genes. In vivo, this regulatory element is tissue specific: it activates transcription of Yp1 and Yp2 reporter genes in follicle cells but has no detectable effect in fat body or other tissues. The sequence of the element consists of two recognition sites for the GATA family of transcription factors. We show that among the Drosophila genes known to encode GATA factors, only dGATAb is expressed in ovaries. The single transcript that we detect in ovaries is alternatively spliced or initiated to produce an ovary-specific isoform of the protein. Bacterially expressed dGATAb binds to the 12-bp element; a similar binding activity is also present in the Kc0 nuclear extracts used for in vitro transcription assays. These in vitro and in vivo results lead us to propose that dGATAb makes several developmentally regulated products, one of which is a follicle cell-specific protein activating transcription of Yp1 and Yp2 from a known regulatory element.

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Selected References

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  1. Abel T., Michelson A. M., Maniatis T. A Drosophila GATA family member that binds to Adh regulatory sequences is expressed in the developing fat body. Development. 1993 Nov;119(3):623–633. doi: 10.1242/dev.119.3.623. [DOI] [PubMed] [Google Scholar]
  2. Abrahamsen N., Martinez A., Kjaer T., Søndergaard L., Bownes M. Cis-regulatory sequences leading to female-specific expression of yolk protein genes 1 and 2 in the fat body of Drosophila melanogaster. Mol Gen Genet. 1993 Feb;237(1-2):41–48. doi: 10.1007/BF00282782. [DOI] [PubMed] [Google Scholar]
  3. Aird W. C., Parvin J. D., Sharp P. A., Rosenberg R. D. The interaction of GATA-binding proteins and basal transcription factors with GATA box-containing core promoters. A model of tissue-specific gene expression. J Biol Chem. 1994 Jan 14;269(2):883–889. [PubMed] [Google Scholar]
  4. An W., Wensink P. C. Integrating sex- and tissue-specific regulation within a single Drosophila enhancer. Genes Dev. 1995 Jan 15;9(2):256–266. doi: 10.1101/gad.9.2.256. [DOI] [PubMed] [Google Scholar]
  5. An W., Wensink P. C. Three protein binding sites form an enhancer that regulates sex- and fat body-specific transcription of Drosophila yolk protein genes. EMBO J. 1995 Mar 15;14(6):1221–1230. doi: 10.1002/j.1460-2075.1995.tb07105.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Arceci R. J., King A. A., Simon M. C., Orkin S. H., Wilson D. B. Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol Cell Biol. 1993 Apr;13(4):2235–2246. doi: 10.1128/mcb.13.4.2235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Barnett T., Pachl C., Gergen J. P., Wensink P. C. The isolation and characterization of Drosophila yolk protein genes. Cell. 1980 Oct;21(3):729–738. doi: 10.1016/0092-8674(80)90436-5. [DOI] [PubMed] [Google Scholar]
  8. Barton M. C., Madani N., Emerson B. M. The erythroid protein cGATA-1 functions with a stage-specific factor to activate transcription of chromatin-assembled beta-globin genes. Genes Dev. 1993 Sep;7(9):1796–1809. doi: 10.1101/gad.7.9.1796. [DOI] [PubMed] [Google Scholar]
  9. Bockamp E. O., McLaughlin F., Murrell A., Green A. R. Transcription factors and the regulation of haemopoiesis: lessons from GATA and SCL proteins. Bioessays. 1994 Jul;16(7):481–488. doi: 10.1002/bies.950160707. [DOI] [PubMed] [Google Scholar]
  10. Bonner J. J., Parks C., Parker-Thornburg J., Mortin M. A., Pelham H. R. The use of promoter fusions in Drosophila genetics: isolation of mutations affecting the heat shock response. Cell. 1984 Jul;37(3):979–991. doi: 10.1016/0092-8674(84)90432-x. [DOI] [PubMed] [Google Scholar]
  11. Brennan M. D., Weiner A. J., Goralski T. J., Mahowald A. P. The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster. Dev Biol. 1982 Jan;89(1):225–236. doi: 10.1016/0012-1606(82)90309-8. [DOI] [PubMed] [Google Scholar]
  12. Buratowski S. The basics of basal transcription by RNA polymerase II. Cell. 1994 Apr 8;77(1):1–3. doi: 10.1016/0092-8674(94)90226-7. [DOI] [PubMed] [Google Scholar]
  13. Corbin V., Maniatis T. The role of specific enhancer-promoter interactions in the Drosophila Adh promoter switch. Genes Dev. 1989 Dec;3(12B):2191–2120. doi: 10.1101/gad.3.12b.2191. [DOI] [PubMed] [Google Scholar]
  14. Coschigano K. T., Wensink P. C. Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev. 1993 Jan;7(1):42–54. doi: 10.1101/gad.7.1.42. [DOI] [PubMed] [Google Scholar]
  15. Drevet J. R., Skeiky Y. A., Iatrou K. GATA-type zinc finger motif-containing sequences and chorion gene transcription factors of the silkworm Bombyx mori. J Biol Chem. 1994 Apr 8;269(14):10660–10667. [PubMed] [Google Scholar]
  16. Evans T., Felsenfeld G. The erythroid-specific transcription factor Eryf1: a new finger protein. Cell. 1989 Sep 8;58(5):877–885. doi: 10.1016/0092-8674(89)90940-9. [DOI] [PubMed] [Google Scholar]
  17. Evans T., Felsenfeld G. trans-Activation of a globin promoter in nonerythroid cells. Mol Cell Biol. 1991 Feb;11(2):843–853. doi: 10.1128/mcb.11.2.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fischer J. A., Maniatis T. Drosophila Adh: a promoter element expands the tissue specificity of an enhancer. Cell. 1988 May 6;53(3):451–461. doi: 10.1016/0092-8674(88)90165-1. [DOI] [PubMed] [Google Scholar]
  19. Fischer J. A., Maniatis T. Structure and transcription of the Drosophila mulleri alcohol dehydrogenase genes. Nucleic Acids Res. 1985 Oct 11;13(19):6899–6917. doi: 10.1093/nar/13.19.6899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fischer K. D., Haese A., Nowock J. Cooperation of GATA-1 and Sp1 can result in synergistic transcriptional activation or interference. J Biol Chem. 1993 Nov 15;268(32):23915–23923. [PubMed] [Google Scholar]
  21. Fong T. C., Emerson B. M. The erythroid-specific protein cGATA-1 mediates distal enhancer activity through a specialized beta-globin TATA box. Genes Dev. 1992 Apr;6(4):521–532. doi: 10.1101/gad.6.4.521. [DOI] [PubMed] [Google Scholar]
  22. Garabedian M. J., Hung M. C., Wensink P. C. Independent control elements that determine yolk protein gene expression in alternative Drosophila tissues. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1396–1400. doi: 10.1073/pnas.82.5.1396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Garabedian M. J., Shepherd B. M., Wensink P. C. A tissue-specific transcription enhancer from the Drosophila yolk protein 1 gene. Cell. 1986 Jun 20;45(6):859–867. doi: 10.1016/0092-8674(86)90560-x. [DOI] [PubMed] [Google Scholar]
  24. Garabedian M. J., Shirras A. D., Bownes M., Wensink P. C. The nucleotide sequence of the gene coding for Drosophila melanogaster yolk protein 3. Gene. 1987;55(1):1–8. doi: 10.1016/0378-1119(87)90242-3. [DOI] [PubMed] [Google Scholar]
  25. Gelti-Douka H., Gingeras T. R., Kambysellis M. P. Yolk proteins in Drosophila: identification and site of synthesis. J Exp Zool. 1974 Jan;187(1):167–172. doi: 10.1002/jez.1401870120. [DOI] [PubMed] [Google Scholar]
  26. Ghosh D. New developments of a transcription factors database. Trends Biochem Sci. 1991 Nov;16(11):445–447. doi: 10.1016/0968-0004(91)90173-s. [DOI] [PubMed] [Google Scholar]
  27. Glaser R. L., Wolfner M. F., Lis J. T. Spatial and temporal pattern of hsp26 expression during normal development. EMBO J. 1986 Apr;5(4):747–754. doi: 10.1002/j.1460-2075.1986.tb04277.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gong Q., Dean A. Enhancer-dependent transcription of the epsilon-globin promoter requires promoter-bound GATA-1 and enhancer-bound AP-1/NF-E2. Mol Cell Biol. 1993 Feb;13(2):911–917. doi: 10.1128/mcb.13.2.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Heberlein U., England B., Tjian R. Characterization of Drosophila transcription factors that activate the tandem promoters of the alcohol dehydrogenase gene. Cell. 1985 Jul;41(3):965–977. doi: 10.1016/s0092-8674(85)80077-5. [DOI] [PubMed] [Google Scholar]
  30. Higuchi R., Krummel B., Saiki R. K. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 1988 Aug 11;16(15):7351–7367. doi: 10.1093/nar/16.15.7351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ho I. C., Vorhees P., Marin N., Oakley B. K., Tsai S. F., Orkin S. H., Leiden J. M. Human GATA-3: a lineage-restricted transcription factor that regulates the expression of the T cell receptor alpha gene. EMBO J. 1991 May;10(5):1187–1192. doi: 10.1002/j.1460-2075.1991.tb08059.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hung M. C., Wensink P. C. The sequence of the Drosophila melanogaster gene for yolk protein 1. Nucleic Acids Res. 1981 Dec 11;9(23):6407–6419. doi: 10.1093/nar/9.23.6407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ko L. J., Engel J. D. DNA-binding specificities of the GATA transcription factor family. Mol Cell Biol. 1993 Jul;13(7):4011–4022. doi: 10.1128/mcb.13.7.4011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kornhauser J. M., Leonard M. W., Yamamoto M., LaVail J. H., Mayo K. E., Engel J. D. Temporal and spatial changes in GATA transcription factor expression are coincident with development of the chicken optic tectum. Brain Res Mol Brain Res. 1994 Apr;23(1-2):100–110. doi: 10.1016/0169-328x(94)90216-x. [DOI] [PubMed] [Google Scholar]
  35. Landry D. B., Engel J. D., Sen R. Functional GATA-3 binding sites within murine CD8 alpha upstream regulatory sequences. J Exp Med. 1993 Sep 1;178(3):941–949. doi: 10.1084/jem.178.3.941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Laybourn P. J., Kadonaga J. T. Threshold phenomena and long-distance activation of transcription by RNA polymerase II. Science. 1992 Sep 18;257(5077):1682–1685. doi: 10.1126/science.1388287. [DOI] [PubMed] [Google Scholar]
  37. Leonard M. W., Lim K. C., Engel J. D. Expression of the chicken GATA factor family during early erythroid development and differentiation. Development. 1993 Oct;119(2):519–531. doi: 10.1242/dev.119.2.519. [DOI] [PubMed] [Google Scholar]
  38. Logan S. K., Garabedian M. J., Wensink P. C. DNA regions that regulate the ovarian transcriptional specificity of Drosophila yolk protein genes. Genes Dev. 1989 Sep;3(9):1453–1461. doi: 10.1101/gad.3.9.1453. [DOI] [PubMed] [Google Scholar]
  39. Logan S. K., Wensink P. C. Ovarian follicle cell enhancers from the Drosophila yolk protein genes: different segments of one enhancer have different cell-type specificities that interact to give normal expression. Genes Dev. 1990 Apr;4(4):613–623. doi: 10.1101/gad.4.4.613. [DOI] [PubMed] [Google Scholar]
  40. Lowrey C. H., Bodine D. M., Nienhuis A. W. Mechanism of DNase I hypersensitive site formation within the human globin locus control region. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1143–1147. doi: 10.1073/pnas.89.3.1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Martin D. I., Orkin S. H. Transcriptional activation and DNA binding by the erythroid factor GF-1/NF-E1/Eryf 1. Genes Dev. 1990 Nov;4(11):1886–1898. doi: 10.1101/gad.4.11.1886. [DOI] [PubMed] [Google Scholar]
  42. Merika M., Orkin S. H. DNA-binding specificity of GATA family transcription factors. Mol Cell Biol. 1993 Jul;13(7):3999–4010. doi: 10.1128/mcb.13.7.3999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. O'Connell P. O., Rosbash M. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 1984 Jul 11;12(13):5495–5513. doi: 10.1093/nar/12.13.5495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. O'Donnell K. H., Chen C. T., Wensink P. C. Insulating DNA directs ubiquitous transcription of the Drosophila melanogaster alpha 1-tubulin gene. Mol Cell Biol. 1994 Sep;14(9):6398–6408. doi: 10.1128/mcb.14.9.6398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Orkin S. H. GATA-binding transcription factors in hematopoietic cells. Blood. 1992 Aug 1;80(3):575–581. [PubMed] [Google Scholar]
  46. Penner C. G., Davie J. R. Transcription factor GATA-1-multiprotein complexes and chicken erythroid development. FEBS Lett. 1994 Apr 11;342(3):273–277. doi: 10.1016/0014-5793(94)80515-6. [DOI] [PubMed] [Google Scholar]
  47. Rahuel C., Vinit M. A., Lemarchandel V., Cartron J. P., Roméo P. H. Erythroid-specific activity of the glycophorin B promoter requires GATA-1 mediated displacement of a repressor. EMBO J. 1992 Nov;11(11):4095–4102. doi: 10.1002/j.1460-2075.1992.tb05502.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Ramain P., Heitzler P., Haenlin M., Simpson P. pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc finger protein with homology to the vertebrate transcription factor GATA-1. Development. 1993 Dec;119(4):1277–1291. doi: 10.1242/dev.119.4.1277. [DOI] [PubMed] [Google Scholar]
  49. Shepherd B., Garabedian M. J., Hung M. C., Wensink P. C. Developmental control of Drosophila yolk protein 1 gene by cis-acting DNA elements. Cold Spring Harb Symp Quant Biol. 1985;50:521–526. doi: 10.1101/sqb.1985.050.01.064. [DOI] [PubMed] [Google Scholar]
  50. Simon J. A., Lis J. T. A germline transformation analysis reveals flexibility in the organization of heat shock consensus elements. Nucleic Acids Res. 1987 Apr 10;15(7):2971–2988. doi: 10.1093/nar/15.7.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Simon M. C. Transcription factor GATA-1 and erythroid development. Proc Soc Exp Biol Med. 1993 Feb;202(2):115–121. doi: 10.3181/00379727-202-43519a. [DOI] [PubMed] [Google Scholar]
  52. Skeiky Y. A., Iatrou K. Synergistic interactions of silkmoth chorion promoter-binding factors. Mol Cell Biol. 1991 Apr;11(4):1954–1964. doi: 10.1128/mcb.11.4.1954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Soeller W. C., Poole S. J., Kornberg T. In vitro transcription of the Drosophila engrailed gene. Genes Dev. 1988 Jan;2(1):68–81. doi: 10.1101/gad.2.1.68. [DOI] [PubMed] [Google Scholar]
  54. Steger D. J., Hecht J. H., Mellon P. L. GATA-binding proteins regulate the human gonadotropin alpha-subunit gene in the placenta and pituitary gland. Mol Cell Biol. 1994 Aug;14(8):5592–5602. doi: 10.1128/mcb.14.8.5592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Tamura T., Kunert C., Postlethwait J. Sex- and cell-specific regulation of yolk polypeptide genes introduced into Drosophila by P-element-mediated gene transfer. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7000–7004. doi: 10.1073/pnas.82.20.7000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Thummel C. S. The Drosophila E74 promoter contains essential sequences downstream from the start site of transcription. Genes Dev. 1989 Jun;3(6):782–792. doi: 10.1101/gad.3.6.782. [DOI] [PubMed] [Google Scholar]
  57. Tjian R., Maniatis T. Transcriptional activation: a complex puzzle with few easy pieces. Cell. 1994 Apr 8;77(1):5–8. doi: 10.1016/0092-8674(94)90227-5. [DOI] [PubMed] [Google Scholar]
  58. Tsai S. F., Strauss E., Orkin S. H. Functional analysis and in vivo footprinting implicate the erythroid transcription factor GATA-1 as a positive regulator of its own promoter. Genes Dev. 1991 Jun;5(6):919–931. doi: 10.1101/gad.5.6.919. [DOI] [PubMed] [Google Scholar]
  59. Whyatt D. J., deBoer E., Grosveld F. The two zinc finger-like domains of GATA-1 have different DNA binding specificities. EMBO J. 1993 Dec 15;12(13):4993–5005. doi: 10.1002/j.1460-2075.1993.tb06193.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Winick J., Abel T., Leonard M. W., Michelson A. M., Chardon-Loriaux I., Holmgren R. A., Maniatis T., Engel J. D. A GATA family transcription factor is expressed along the embryonic dorsoventral axis in Drosophila melanogaster. Development. 1993 Dec;119(4):1055–1065. doi: 10.1242/dev.119.4.1055. [DOI] [PubMed] [Google Scholar]
  61. Yamamoto M., Ko L. J., Leonard M. W., Beug H., Orkin S. H., Engel J. D. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev. 1990 Oct;4(10):1650–1662. doi: 10.1101/gad.4.10.1650. [DOI] [PubMed] [Google Scholar]
  62. Yang H. Y., Evans T. Distinct roles for the two cGATA-1 finger domains. Mol Cell Biol. 1992 Oct;12(10):4562–4570. doi: 10.1128/mcb.12.10.4562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Zon L. I., Mather C., Burgess S., Bolce M. E., Harland R. M., Orkin S. H. Expression of GATA-binding proteins during embryonic development in Xenopus laevis. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10642–10646. doi: 10.1073/pnas.88.23.10642. [DOI] [PMC free article] [PubMed] [Google Scholar]

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