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. 1996 Jun 17;15(12):3085–3092.

Evidence that a combined activator-repressor protein regulates Dictyostelium stalk cell differentiation.

T Kawata 1, A Early 1, J Williams 1
PMCID: PMC450250  PMID: 8670809

Abstract

The ecmA gene is expressed in Dictyostelium prestalk cells and is inducible by differentiation-inducing factor (DIF), a low-molecular-weight lipophilic substance. The ecmB gene is expressed in stalk cells and is under negative control by two repressor elements. Each repressor element contains two copies of the sequence TTGA in an inverted relative orientation. There are activator elements in the ecmA promoter that also contain two TTGA sequences, but in the same relative orientation. Gel retardation assays suggest that the same protein binds to the ecmB repressor and the ecmA activator. We propose that DIF induces prestalk cell differentiation by activating this protein and that the protein also binds to the promoters of stalk-specific genes, acting as a repressor that holds cells in the prestalk state until culmination is triggered.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abe T., Early A., Siegert F., Weijer C., Williams J. Patterns of cell movement within the Dictyostelium slug revealed by cell type-specific, surface labeling of living cells. Cell. 1994 Jun 3;77(5):687–699. doi: 10.1016/0092-8674(94)90053-1. [DOI] [PubMed] [Google Scholar]
  2. Brookman J. J., Town C. D., Jermyn K. A., Kay R. R. Developmental regulation of a stalk cell differentiation-inducing factor in Dictyostelium discoideum. Dev Biol. 1982 May;91(1):191–196. doi: 10.1016/0012-1606(82)90022-7. [DOI] [PubMed] [Google Scholar]
  3. Bühl B., Fischer K., MacWilliams H. K. Cell sorting within the prespore zone of Dictyostelium discoideum. Dev Biol. 1993 Apr;156(2):481–489. doi: 10.1006/dbio.1993.1094. [DOI] [PubMed] [Google Scholar]
  4. Ceccarelli A., Mahbubani H. J., Insall R., Schnitzler G., Firtel R. A., Williams J. G. A G-rich sequence element common to Dictyostelium genes which differ radically in their patterns of expression. Dev Biol. 1992 Jul;152(1):188–193. doi: 10.1016/0012-1606(92)90169-h. [DOI] [PubMed] [Google Scholar]
  5. Ceccarelli A., Mahbubani H., Williams J. G. Positively and negatively acting signals regulating stalk cell and anterior-like cell differentiation in Dictyostelium. Cell. 1991 Jun 14;65(6):983–989. doi: 10.1016/0092-8674(91)90550-i. [DOI] [PubMed] [Google Scholar]
  6. Ceccarelli A., McRobbie S. J., Jermyn K. A., Duffy K., Early A., Williams J. G. Structural and functional characterization of a Dictyostelium gene encoding a DIF inducible, prestalk-enriched mRNA sequence. Nucleic Acids Res. 1987 Sep 25;15(18):7463–7476. doi: 10.1093/nar/15.18.7463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Datta S., Firtel R. A. An 80-bp cis-acting regulatory region controls cAMP and development regulation of a prestalk gene in Dictyostelium. Genes Dev. 1988 Mar;2(3):294–304. doi: 10.1101/gad.2.3.294. [DOI] [PubMed] [Google Scholar]
  8. Davies L., Satre M., Martin J. B., Gross J. D. The target of ammonia action in dictyostelium. Cell. 1993 Oct 22;75(2):321–327. doi: 10.1016/0092-8674(93)80073-n. [DOI] [PubMed] [Google Scholar]
  9. Dingermann T., Reindl N., Werner H., Hildebrandt M., Nellen W., Harwood A., Williams J., Nerke K. Optimization and in situ detection of Escherichia coli beta-galactosidase gene expression in Dictyostelium discoideum. Gene. 1989 Dec 28;85(2):353–362. doi: 10.1016/0378-1119(89)90428-9. [DOI] [PubMed] [Google Scholar]
  10. Early A. E., Gaskell M. J., Traynor D., Williams J. G. Two distinct populations of prestalk cells within the tip of the migratory Dictyostelium slug with differing fates at culmination. Development. 1993 Jun;118(2):353–362. doi: 10.1242/dev.118.2.353. [DOI] [PubMed] [Google Scholar]
  11. Early A. E., Williams J. G. Two vectors which facilitate gene manipulation and a simplified transformation procedure for Dictyostelium discoideum. Gene. 1987;59(1):99–106. doi: 10.1016/0378-1119(87)90270-8. [DOI] [PubMed] [Google Scholar]
  12. Early A., Abe T., Williams J. Evidence for positional differentiation of prestalk cells and for a morphogenetic gradient in Dictyostelium. Cell. 1995 Oct 6;83(1):91–99. doi: 10.1016/0092-8674(95)90237-6. [DOI] [PubMed] [Google Scholar]
  13. Harwood A. J., Early A., Williams J. G. A repressor controls the timing and spatial localisation of stalk cell-specific gene expression in Dictyostelium. Development. 1993 Aug;118(4):1041–1048. doi: 10.1242/dev.118.4.1041. [DOI] [PubMed] [Google Scholar]
  14. Harwood A. J., Hopper N. A., Simon M. N., Driscoll D. M., Veron M., Williams J. G. Culmination in Dictyostelium is regulated by the cAMP-dependent protein kinase. Cell. 1992 May 15;69(4):615–624. doi: 10.1016/0092-8674(92)90225-2. [DOI] [PubMed] [Google Scholar]
  15. Hjorth A. L., Pears C., Williams J. G., Firtel R. A. A developmentally regulated trans-acting factor recognizes dissimilar G/C-rich elements controlling a class of cAMP-inducible Dictyostelium genes. Genes Dev. 1990 Mar;4(3):419–432. doi: 10.1101/gad.4.3.419. [DOI] [PubMed] [Google Scholar]
  16. Hopper N. A., Harwood A. J., Bouzid S., Véron M., Williams J. G. Activation of the prespore and spore cell pathway of Dictyostelium differentiation by cAMP-dependent protein kinase and evidence for its upstream regulation by ammonia. EMBO J. 1993 Jun;12(6):2459–2466. doi: 10.1002/j.1460-2075.1993.tb05900.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Insall R., Kay R. R. A specific DIF binding protein in Dictyostelium. EMBO J. 1990 Oct;9(10):3323–3328. doi: 10.1002/j.1460-2075.1990.tb07532.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jermyn K. A., Duffy K. T., Williams J. G. A new anatomy of the prestalk zone in Dictyostelium. Nature. 1989 Jul 13;340(6229):144–146. doi: 10.1038/340144a0. [DOI] [PubMed] [Google Scholar]
  19. Jermyn K. A., Williams J. G. An analysis of culmination in Dictyostelium using prestalk and stalk-specific cell autonomous markers. Development. 1991 Mar;111(3):779–787. doi: 10.1242/dev.111.3.779. [DOI] [PubMed] [Google Scholar]
  20. Kay R. R., Jermyn K. A. A possible morphogen controlling differentiation in Dictyostelium. Nature. 1983 May 19;303(5914):242–244. doi: 10.1038/303242a0. [DOI] [PubMed] [Google Scholar]
  21. Kopachik W., Bergen L. G., Barclay S. L. Genes selectively expressed in proliferating Dictyostelium amoebae. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8540–8544. doi: 10.1073/pnas.82.24.8540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kopachik W., Oohata A., Dhokia B., Brookman J. J., Kay R. R. Dictyostelium mutants lacking DIF, a putative morphogen. Cell. 1983 Jun;33(2):397–403. doi: 10.1016/0092-8674(83)90421-x. [DOI] [PubMed] [Google Scholar]
  23. Kubohara Y., Maeda M., Okamoto K. Analysis of the maturation process of prestalk cells in Dictyostelium discoideum. Exp Cell Res. 1993 Jul;207(1):107–114. doi: 10.1006/excr.1993.1168. [DOI] [PubMed] [Google Scholar]
  24. Mann S. K., Richardson D. L., Lee S., Kimmel A. R., Firtel R. A. Expression of cAMP-dependent protein kinase in prespore cells is sufficient to induce spore cell differentiation in Dictyostelium. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10561–10565. doi: 10.1073/pnas.91.22.10561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McRobbie S. J., Jermyn K. A., Duffy K., Blight K., Williams J. G. Two DIF-inducible, prestalk-specific mRNAs of Dictyostelium encode extracellular matrix proteins of the slug. Development. 1988 Oct;104(2):275–284. doi: 10.1242/dev.104.2.275. [DOI] [PubMed] [Google Scholar]
  26. McRobbie S. J., Tilly R., Blight K., Ceccarelli A., Williams J. G. Identification and localization of proteins encoded by two DIF-inducible genes of Dictyostelium. Dev Biol. 1988 Jan;125(1):59–63. doi: 10.1016/0012-1606(88)90058-9. [DOI] [PubMed] [Google Scholar]
  27. Morris H. R., Taylor G. W., Masento M. S., Jermyn K. A., Kay R. R. Chemical structure of the morphogen differentiation inducing factor from Dictyostelium discoideum. 1987 Aug 27-Sep 2Nature. 328(6133):811–814. doi: 10.1038/328811a0. [DOI] [PubMed] [Google Scholar]
  28. Morrison A., Harwood A. A simple method of generating axenic derivatives of Dictyostelium strains. Exp Cell Res. 1992 Apr;199(2):383–386. doi: 10.1016/0014-4827(92)90449-i. [DOI] [PubMed] [Google Scholar]
  29. När A. M., Boutin J. M., Lipkin S. M., Yu V. C., Holloway J. M., Glass C. K., Rosenfeld M. G. The orientation and spacing of core DNA-binding motifs dictate selective transcriptional responses to three nuclear receptors. Cell. 1991 Jun 28;65(7):1267–1279. doi: 10.1016/0092-8674(91)90021-p. [DOI] [PubMed] [Google Scholar]
  30. Pears C. J., Williams J. G. Multiple copies of a G-rich element upstream of a cAMP-inducible Dictyostelium gene are necessary but not sufficient for efficient gene expression. Nucleic Acids Res. 1988 Sep 12;16(17):8467–8486. doi: 10.1093/nar/16.17.8467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Powell-Coffman J. A., Firtel R. A. Characterization of a novel Dictyostelium discoideum prespore-specific gene, PspB, reveals conserved regulatory sequences. Development. 1994 Jun;120(6):1601–1611. doi: 10.1242/dev.120.6.1601. [DOI] [PubMed] [Google Scholar]
  32. Powell-Coffman J. A., Schnitzler G. R., Firtel R. A. A GBF-binding site and a novel AT element define the minimal sequences sufficient to direct prespore-specific expression in Dictyostelium discoideum. Mol Cell Biol. 1994 Sep;14(9):5840–5849. doi: 10.1128/mcb.14.9.5840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Richardson D. L., Loomis W. F., Kimmel A. R. Progression of an inductive signal activates sporulation in Dictyostelium discoideum. Development. 1994 Oct;120(10):2891–2900. doi: 10.1242/dev.120.10.2891. [DOI] [PubMed] [Google Scholar]
  34. Schindler J., Sussman M. Ammonia determines the choice of morphogenetic pathways in Dictyostelium discoideum. J Mol Biol. 1977 Oct 15;116(1):161–169. doi: 10.1016/0022-2836(77)90124-3. [DOI] [PubMed] [Google Scholar]
  35. Schnitzler G. R., Fischer W. H., Firtel R. A. Cloning and characterization of the G-box binding factor, an essential component of the developmental switch between early and late development in Dictyostelium. Genes Dev. 1994 Feb 15;8(4):502–514. doi: 10.1101/gad.8.4.502. [DOI] [PubMed] [Google Scholar]
  36. Simon M. N., Pelegrini O., Veron M., Kay R. R. Mutation of protein kinase A causes heterochronic development of Dictyostelium. Nature. 1992 Mar 12;356(6365):171–172. doi: 10.1038/356171a0. [DOI] [PubMed] [Google Scholar]
  37. Sternfeld J., David C. N. Fate and regulation of anterior-like cells in Dictyostelium slugs. Dev Biol. 1982 Sep;93(1):111–118. doi: 10.1016/0012-1606(82)90244-5. [DOI] [PubMed] [Google Scholar]
  38. Town C. D., Gross J. D., Kay R. R. Cell differentiation without morphogenesis in Dictyostelium discoideum. Nature. 1976 Aug 19;262(5570):717–719. doi: 10.1038/262717a0. [DOI] [PubMed] [Google Scholar]
  39. Watts D. J., Ashworth J. M. Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J. 1970 Sep;119(2):171–174. doi: 10.1042/bj1190171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Williams J. G., Ceccarelli A., McRobbie S., Mahbubani H., Kay R. R., Early A., Berks M., Jermyn K. A. Direct induction of Dictyostelium prestalk gene expression by DIF provides evidence that DIF is a morphogen. Cell. 1987 Apr 24;49(2):185–192. doi: 10.1016/0092-8674(87)90559-9. [DOI] [PubMed] [Google Scholar]

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