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. 1987 Sep 25;15(18):7463–7476. doi: 10.1093/nar/15.18.7463

Structural and functional characterization of a Dictyostelium gene encoding a DIF inducible, prestalk-enriched mRNA sequence.

A Ceccarelli 1, S J McRobbie 1, K A Jermyn 1, K Duffy 1, A Early 1, J G Williams 1
PMCID: PMC306261  PMID: 3658700

Abstract

The pDd56 mRNA sequence is highly enriched in prestalk over prespore cells and is inducible by DIF, the putative Dictyostelium stalk-specific morphogen. We show that the pDd56 gene is composed of forty one copies of a twenty four amino acid, cysteine rich repeat. This is highly homologus to a repeat which we have previously shown to compose the major fraction of the pDd63 mRNA, another DIF inducible, prestalk-enriched sequence. The predicted pDd56 protein contains a putative signal peptide but does not appear to contain a transmembrane segment. In combination these features suggest it to be an extrinsic protein and we confirm this elsewhere by showing that the pDd56 gene encodes a known, extracellular protein of the stalk. The pDd56 mRNA is dependent upon exogenous DIF for its accumulation. We show that this control is exerted at the transcriptional level and that a restriction fragment containing 1.7Kb of upstream sequence directs temporally-regulated expression of the gene.

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Selected References

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  1. Barklis E., Lodish H. F. Regulation of dictyostelium discoideum mRNAs specific for prespore or prestalk cells. Cell. 1983 Apr;32(4):1139–1148. doi: 10.1016/0092-8674(83)90297-0. [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. Chung S., Landfear S. M., Blumberg D. D., Cohen N. S., Lodish H. F. Synthesis and stability of developmentally regulated dictyostelium mRNAs are affected by cell--cell contact and cAMP. Cell. 1981 Jun;24(3):785–797. doi: 10.1016/0092-8674(81)90104-5. [DOI] [PubMed] [Google Scholar]
  4. Dente L., Cesareni G., Cortese R. pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 1983 Mar 25;11(6):1645–1655. doi: 10.1093/nar/11.6.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Devine J. M., Tsang A. S., Williams J. G. Differential expression of the members of the discoidin I multigene family during growth and development of Dictyostelium discoideum. Cell. 1982 Apr;28(4):793–800. doi: 10.1016/0092-8674(82)90058-7. [DOI] [PubMed] [Google Scholar]
  6. Devine K. M., Loomis W. F. Molecular characterization of anterior-like cells in Dictyostelium discoideum. Dev Biol. 1985 Feb;107(2):364–372. doi: 10.1016/0012-1606(85)90318-5. [DOI] [PubMed] [Google Scholar]
  7. Dowds B. C., Loomis W. F. Hexapeptide repeat structure in Dictyostelium spore coat protein. Biochem Biophys Res Commun. 1986 Feb 26;135(1):336–339. doi: 10.1016/0006-291x(86)90982-4. [DOI] [PubMed] [Google Scholar]
  8. Greenwald I. lin-12, a nematode homeotic gene, is homologous to a set of mammalian proteins that includes epidermal growth factor. Cell. 1985 Dec;43(3 Pt 2):583–590. doi: 10.1016/0092-8674(85)90230-2. [DOI] [PubMed] [Google Scholar]
  9. Gross J. D., Town C. D., Brookman J. J., Jermyn K. A., Peacey M. J., Kay R. R. Cell patterning in Dictyostelium. Philos Trans R Soc Lond B Biol Sci. 1981 Oct 7;295(1078):497–508. doi: 10.1098/rstb.1981.0156. [DOI] [PubMed] [Google Scholar]
  10. Kay R. R., Garrod D., Tilly R. Requirement for cell differentiation in Dictyostelium discoideum. Nature. 1978 Jan 5;271(5640):58–60. doi: 10.1038/271058a0. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Kimmel A. R., Firtel R. A. Sequence organization in Dictyostelium: unique structure at the 5'-ends of protein coding genes. Nucleic Acids Res. 1983 Jan 25;11(2):541–552. doi: 10.1093/nar/11.2.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kochan J., Perkins M., Ravetch J. V. A tandemly repeated sequence determines the binding domain for an erythrocyte receptor binding protein of P. falciparum. Cell. 1986 Mar 14;44(5):689–696. doi: 10.1016/0092-8674(86)90834-2. [DOI] [PubMed] [Google Scholar]
  14. Kopachik W. J., Dhokia B., Kay R. R. Selective induction of stalk-cell-specific proteins in Dictyostelium. Differentiation. 1985;28(3):209–216. doi: 10.1111/j.1432-0436.1985.tb00827.x. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Krefft M., Voet L., Gregg J. H., Williams K. L. Use of a monoclonal antibody recognizing a cell surface determinant to distinguish prestalk and prespore cells of Dictyostelium discoideum slugs. J Embryol Exp Morphol. 1985 Aug;88:15–24. [PubMed] [Google Scholar]
  17. Landfear S. M., Lefebvre P., Chung S., Lodish H. F. Transcriptional control of gene expression during development of Dictyostelium discoideum. Mol Cell Biol. 1982 Nov;2(11):1417–1426. doi: 10.1128/mcb.2.11.1417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Loomis W. F. The spatial pattern of cell-type differentiation in Dictyostelium. Dev Biol. 1982 Oct;93(2):279–284. doi: 10.1016/0012-1606(82)90117-8. [DOI] [PubMed] [Google Scholar]
  19. Mangiarotti G., Ceccarelli A., Lodish H. F. Cyclic AMP stabilizes a class of developmentally regulated Dictyostelium discoideum mRNAs. Nature. 1983 Feb 17;301(5901):616–618. doi: 10.1038/301616a0. [DOI] [PubMed] [Google Scholar]
  20. Mangiarotti G., Lefebvre P., Lodish H. F. Differences in the stability of developmentally regulated mRNAs in aggregated and disaggregated Dictyostelium discoideum cells. Dev Biol. 1982 Jan;89(1):82–91. doi: 10.1016/0012-1606(82)90296-2. [DOI] [PubMed] [Google Scholar]
  21. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mehdy M. C., Ratner D., Firtel R. A. Induction and modulation of cell-type-specific gene expression in Dictyostelium. Cell. 1983 Mar;32(3):763–771. doi: 10.1016/0092-8674(83)90062-4. [DOI] [PubMed] [Google Scholar]
  23. Morrissey J. H., Devine K. M., Loomis W. F. The timing of cell-type-specific differentiation in Dictyostelium discoideum. Dev Biol. 1984 Jun;103(2):414–424. doi: 10.1016/0012-1606(84)90329-4. [DOI] [PubMed] [Google Scholar]
  24. Nellen W., Silan C., Firtel R. A. DNA-mediated transformation in Dictyostelium discoideum: regulated expression of an actin gene fusion. Mol Cell Biol. 1984 Dec;4(12):2890–2898. doi: 10.1128/mcb.4.12.2890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ozaki L. S., Svec P., Nussenzweig R. S., Nussenzweig V., Godson G. N. Structure of the plasmodium knowlesi gene coding for the circumsporozoite protein. Cell. 1983 Oct;34(3):815–822. doi: 10.1016/0092-8674(83)90538-x. [DOI] [PubMed] [Google Scholar]
  26. Petersen T. E., Thøgersen H. C., Skorstengaard K., Vibe-Pedersen K., Sahl P., Sottrup-Jensen L., Magnusson S. Partial primary structure of bovine plasma fibronectin: three types of internal homology. Proc Natl Acad Sci U S A. 1983 Jan;80(1):137–141. doi: 10.1073/pnas.80.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Prat A., Katinka M., Caron F., Meyer E. Nucleotide sequence of the Paramecium primaurelia G surface protein. A huge protein with a highly periodic structure. J Mol Biol. 1986 May 5;189(1):47–60. doi: 10.1016/0022-2836(86)90380-3. [DOI] [PubMed] [Google Scholar]
  28. Rowekamp W., Firtel R. A. Isolation of developmentally regulated genes from Dictyostelium. Dev Biol. 1980 Oct;79(2):409–418. doi: 10.1016/0012-1606(80)90126-8. [DOI] [PubMed] [Google Scholar]
  29. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Tasaka M., Noce T., Takeuchi I. Prestalk and prespore differentiation in Dictyostelium as detected by cell type-specific monoclonal antibodies. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5340–5344. doi: 10.1073/pnas.80.17.5340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Town C., Stanford E. An oligosaccharide-containing factor that induces cell differentiation in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1979 Jan;76(1):308–312. doi: 10.1073/pnas.76.1.308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Twigg A. J., Sherratt D. Trans-complementable copy-number mutants of plasmid ColE1. Nature. 1980 Jan 10;283(5743):216–218. doi: 10.1038/283216a0. [DOI] [PubMed] [Google Scholar]
  35. Ullrich A., Bell J. R., Chen E. Y., Herrera R., Petruzzelli L. M., Dull T. J., Gray A., Coussens L., Liao Y. C., Tsubokawa M. Human insulin receptor and its relationship to the tyrosine kinase family of oncogenes. 1985 Feb 28-Mar 6Nature. 313(6005):756–761. doi: 10.1038/313756a0. [DOI] [PubMed] [Google Scholar]
  36. Ullrich A., Coussens L., Hayflick J. S., Dull T. J., Gray A., Tam A. W., Lee J., Yarden Y., Libermann T. A., Schlessinger J. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. 1984 May 31-Jun 6Nature. 309(5967):418–425. doi: 10.1038/309418a0. [DOI] [PubMed] [Google Scholar]
  37. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Wharton K. A., Johansen K. M., Xu T., Artavanis-Tsakonas S. Nucleotide sequence from the neurogenic locus notch implies a gene product that shares homology with proteins containing EGF-like repeats. Cell. 1985 Dec;43(3 Pt 2):567–581. doi: 10.1016/0092-8674(85)90229-6. [DOI] [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]
  41. Williams J. G., Lloyd M. M., Devine J. M. Characterization and transcription analysis of a cloned sequence derived from a major developmentally regulated mRNA of D. discoideum. Cell. 1979 Aug;17(4):903–913. doi: 10.1016/0092-8674(79)90330-1. [DOI] [PubMed] [Google Scholar]

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