Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1992 Sep 1;89(17):8303–8307. doi: 10.1073/pnas.89.17.8303

Chemotactic sorting to cAMP in the multicellular stages of Dictyostelium development.

D Traynor 1, R H Kessin 1, J G Williams 1
PMCID: PMC49906  PMID: 1325653

Abstract

Dictyostelium transformants that overproduce the extracellular form of cyclic nucleotide phosphodiesterase and so accumulate a reduced amount of cAMP are blocked in development after aggregation in the form of a tight mound, prior to formation of the apical tip. In such mounds, prespore cell differentiation is repressed, and the apical accumulation of prestalk cells is greatly retarded. When a source of cAMP is placed below the arrested mounds, prestalk cells that would normally migrate in an apical direction instead sort downwards to the substratum. Thus, by acting as the chemoattractant that draws prestalk cells to the apex, cAMP signaling directs the formation of a patterned structure.

Full text

PDF
8307

Images in this article

8305Image
on p.8305
8306Image
on p.8306
8306Image
on p.8306

Selected References

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

  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. Devine K. M., Bergmann J. E., Loomis W. F. Spore coat proteins of Dictyostelium discoideum are packaged in prespore vesicles. Dev Biol. 1983 Oct;99(2):437–446. doi: 10.1016/0012-1606(83)90293-2. [DOI] [PubMed] [Google Scholar]
  3. Devreotes P. Dictyostelium discoideum: a model system for cell-cell interactions in development. Science. 1989 Sep 8;245(4922):1054–1058. doi: 10.1126/science.2672337. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Early A. E., Williams J. G., Meyer H. E., Por S. B., Smith E., Williams K. L., Gooley A. A. Structural characterization of Dictyostelium discoideum prespore-specific gene D19 and of its product, cell surface glycoprotein PsA. Mol Cell Biol. 1988 Aug;8(8):3458–3466. doi: 10.1128/mcb.8.8.3458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Esch R. K., Firtel R. A. cAMP and cell sorting control the spatial expression of a developmentally essential cell-type-specific ras gene in Dictyostelium. Genes Dev. 1991 Jan;5(1):9–21. doi: 10.1101/gad.5.1.9. [DOI] [PubMed] [Google Scholar]
  7. Faure M., Franke J., Hall A. L., Podgorski G. J., Kessin R. H. The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum contains three promoters specific for growth, aggregation, and late development. Mol Cell Biol. 1990 May;10(5):1921–1930. doi: 10.1128/mcb.10.5.1921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Faure M., Podgorski G. J., Franke J., Kessin R. H. Disruption of Dictyostelium discoideum morphogenesis by overproduction of cAMP phosphodiesterase. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8076–8080. doi: 10.1073/pnas.85.21.8076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Geltosky J. E., Weseman J., Bakke A., Lerner R. A. Identification of a cell surface glycoprotein involved in cell aggregation in D. discoideum. Cell. 1979 Oct;18(2):391–398. doi: 10.1016/0092-8674(79)90058-8. [DOI] [PubMed] [Google Scholar]
  10. Gerisch G. Cyclic AMP and other signals controlling cell development and differentiation in Dictyostelium. Annu Rev Biochem. 1987;56:853–879. doi: 10.1146/annurev.bi.56.070187.004225. [DOI] [PubMed] [Google Scholar]
  11. Gerisch G., Fromm H., Huesgen A., Wick U. Control of cell-contact sites by cyclic AMP pulses in differentiating Dictyostelium cells. Nature. 1975 Jun 12;255(5509):547–549. doi: 10.1038/255547a0. [DOI] [PubMed] [Google Scholar]
  12. Haberstroh L., Firtel R. A. A spatial gradient of expression of a cAMP-regulated prespore cell-type-specific gene in Dictyostelium. Genes Dev. 1990 Apr;4(4):596–612. doi: 10.1101/gad.4.4.596. [DOI] [PubMed] [Google Scholar]
  13. Henderson E. J. The cyclic adenosine 3':5'-monophosphate receptor of Dictyostelium discoideum. Binding characteristics of aggregation-competent cells and variation of binding levels during the life cycle. J Biol Chem. 1975 Jun 25;250(12):4730–4736. [PubMed] [Google Scholar]
  14. Houle J., Balthazar J., West C. M. A glycosylation mutation affects cell fate in chimeras of Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1989 May;86(10):3679–3683. doi: 10.1073/pnas.86.10.3679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Inouye K., Takeuchi I. Correlations between prestalk-prespore tendencies and cAMP-related activities in Dictyostelium discoideum. Exp Cell Res. 1982 Apr;138(2):311–318. doi: 10.1016/0014-4827(82)90180-x. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. 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]
  19. Kessin R. H., Orlow S. J., Shapiro R. I., Franke J. Binding of inhibitor alters kinetic and physical properties of extracellular cyclic AMP phosphodiesterase from Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5450–5454. doi: 10.1073/pnas.76.11.5450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kimmel A. R., Firtel R. A. cAMP signal transduction pathways regulating development of Dictyostelium discoideum. Curr Opin Genet Dev. 1991 Oct;1(3):383–390. doi: 10.1016/s0959-437x(05)80304-1. [DOI] [PubMed] [Google Scholar]
  21. Klein C. Induction of phosphodiesterase by cyclic adenosine 3':5'-monophosphate in differentiating Dictyostelium discoideum amoebae. J Biol Chem. 1975 Sep 25;250(18):7134–7138. [PubMed] [Google Scholar]
  22. Konijn T. M., Van De Meene J. G., Bonner J. T., Barkley D. S. The acrasin activity of adenosine-3',5'-cyclic phosphate. Proc Natl Acad Sci U S A. 1967 Sep;58(3):1152–1154. doi: 10.1073/pnas.58.3.1152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Krefft M., Voet L., Mairhofer H., Williams K. L. Analysis of proportion regulation in slugs of Dictyostelium discoideum using a monoclonal antibody and a FACS-IV. Exp Cell Res. 1983 Aug;147(1):235–239. doi: 10.1016/0014-4827(83)90291-4. [DOI] [PubMed] [Google Scholar]
  24. Matsukuma S., Durston A. J. Chemotactic cell sorting in Dictyostelium discoideum. J Embryol Exp Morphol. 1979 Apr;50:243–251. [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. 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]
  27. 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]
  28. Podgorski G. J., Franke J., Faure M., Kessin R. H. The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum utilizes alternate promoters and splicing for the synthesis of multiple mRNAs. Mol Cell Biol. 1989 Sep;9(9):3938–3950. doi: 10.1128/mcb.9.9.3938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rossier C., Franke J., Mullens I. A., Kelley K. J., Kessin R. H. Detection and regulation of the mRNA for the inhibitor of extracellular cAMP phosphodiesterase of Dictyostelium discoideum. Eur J Biochem. 1983 Jun 15;133(2):383–391. doi: 10.1111/j.1432-1033.1983.tb07474.x. [DOI] [PubMed] [Google Scholar]
  30. Rubin J., Robertson A. The tip of the Dictyostelium discoideum pseudoplasmodium as an organizer. J Embryol Exp Morphol. 1975 Feb;33(1):227–241. [PubMed] [Google Scholar]
  31. Schaap P., Van Lookeren Campagne M. M., Van Driel R., Spek W., Van Haastert P. J., Pinas J. Postaggregative differentiation induction by cyclic AMP in Dictyostelium: intracellular transduction pathway and requirement for additional stimuli. Dev Biol. 1986 Nov;118(1):52–63. doi: 10.1016/0012-1606(86)90072-2. [DOI] [PubMed] [Google Scholar]
  32. Siu C. H., Des Roches B., Lam T. Y. Involvement of a cell-surface glycoprotein in the cell-sorting process of Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1983 Nov;80(21):6596–6600. doi: 10.1073/pnas.80.21.6596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. TAKEUCHI I. IMMUNOCHEMICAL AND IMMUNOHISTOCHEMICAL STUDIES ON THE DEVELOPMENT OF THE CELLULAR SLIME MOLD DICTYOSTELIUM MUCOROIDES. Dev Biol. 1963 Aug;8:1–26. doi: 10.1016/0012-1606(63)90023-x. [DOI] [PubMed] [Google Scholar]
  34. Tsang A., Bradbury J. M. Separation and properties of prestalk and prespore cells of Dictyostelium discoideum. Exp Cell Res. 1981 Apr;132(2):433–441. doi: 10.1016/0014-4827(81)90118-x. [DOI] [PubMed] [Google Scholar]
  35. Wallace J. S., Morrissey J. H., Newell P. C. Monoclonal antibodies specific for stalk differentiation in Dictyostelium discoideum. Cell Differ. 1984 Aug;14(3):205–211. doi: 10.1016/0045-6039(84)90047-2. [DOI] [PubMed] [Google Scholar]
  36. Williams J. G., Duffy K. T., Lane D. P., McRobbie S. J., Harwood A. J., Traynor D., Kay R. R., Jermyn K. A. Origins of the prestalk-prespore pattern in Dictyostelium development. Cell. 1989 Dec 22;59(6):1157–1163. doi: 10.1016/0092-8674(89)90771-x. [DOI] [PubMed] [Google Scholar]
  37. Williams J. G., Jermyn K. A., Duffy K. T. Formation and anatomy of the prestalk zone of Dictyostelium. Development. 1989;107 (Suppl):91–97. doi: 10.1242/dev.107.Supplement.91. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES