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. 1980 Feb;77(2):1044–1048. doi: 10.1073/pnas.77.2.1044

A role for cyclic AMP in expression of developmentally regulated genes in Dictyostelium discoideum.

S M Landfear, H F Lodish
PMCID: PMC348420  PMID: 6244577

Abstract

Starved cells of Dictyostelium discoideum begin to synthesize a new class of developmentally regulated proteins at about 13 hr of the 24-hr developmental program, concomitant with the formation of tips on the tight cell aggregates [Alton, T. H. & Lodish, H. F. (1977) Dev. Biol. 60, 180--206]. Continued synthesis of these proteins is normally dependent upon the integrity of the multicellular aggregates, because cells that have been disaggregated at 13 hr and shaken in suspension for 5 hr do not make these proteins. We show here that addition of 20 microM cyclic AMP to suspension cultures of disaggregated 13-hr cells caused synthesis of most of these late proteins to be maintained. Translation in an in vitro wheat germ system of total cellular RNA isolated from these cyclic AMP-stimulated suspension cells, or from normal aggregates, generated several proteins that were not encoded by the RNA isolated from equivalent suspension cells which had not been treated with cyclic AMP or from preaggregation cells. We conclude that cyclic AMP has a direct role in maintaining the synthesis of aggregation-dependent Dictyostelium proteins and in maintaining the level of the corresponding mRNAs.

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Selected References

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

  1. Alcantara F., Monk M. Signal propagation during aggregation in the slime mould Dictyostelium discoideum. J Gen Microbiol. 1974 Dec;85(2):321–334. doi: 10.1099/00221287-85-2-321. [DOI] [PubMed] [Google Scholar]
  2. Alton T. H., Lodish H. F. Developmental changes in messenger RNAs and protein synthesis in Dictyostelium discoideum. Dev Biol. 1977 Oct 1;60(1):180–206. doi: 10.1016/0012-1606(77)90118-x. [DOI] [PubMed] [Google Scholar]
  3. Alton T. H., Lodish H. F. Synthesis of developmentally regulated proteins in Dictyostelium discoideum which are dependent on continued cell-cell interaction. Dev Biol. 1977 Oct 1;60(1):207–216. doi: 10.1016/0012-1606(77)90119-1. [DOI] [PubMed] [Google Scholar]
  4. Beug H., Katz F. E., Gerisch G. Dynamics of antigenic membrane sites relating to cell aggregation in Dictyostelium discoideum. J Cell Biol. 1973 Mar;56(3):647–658. doi: 10.1083/jcb.56.3.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bonner J. T. Induction of stalk cell differentiation by cyclic AMP in the cellular slime mold Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1970 Jan;65(1):110–113. doi: 10.1073/pnas.65.1.110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brenner M. Cyclic AMP gradient in migrating pseudoplasmodia of the cellular slime mold Dictyostelium discoideum. J Biol Chem. 1977 Jun 25;252(12):4073–4077. [PubMed] [Google Scholar]
  7. Brenner M. Cyclic AMP levels and turnover during development of the cellular slime mold Dictyostelium discoideum. Dev Biol. 1978 Jun;64(2):210–223. doi: 10.1016/0012-1606(78)90073-8. [DOI] [PubMed] [Google Scholar]
  8. Darmon M., Brachet P., Da Silva L. H. Chemotactic signals induce cell differentiation in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3163–3166. doi: 10.1073/pnas.72.8.3163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Devreotes P. N., Derstine P. L., Steck T. L. Cyclic 3',5' AMP relay in Dictyostelium discoideum. I. A technique to monitor responses to controlled stimuli. J Cell Biol. 1979 Feb;80(2):291–299. doi: 10.1083/jcb.80.2.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Devreotes P. N., Steck T. L. Cyclic 3',5' AMP relay in Dictyostelium discoideum. II. Requirements for the initiation and termination of the response. J Cell Biol. 1979 Feb;80(2):300–309. doi: 10.1083/jcb.80.2.300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Durston A. J., Vork F. A cinematographical study of the development of vitally stained Dictyostelium discoideum. J Cell Sci. 1979 Apr;36:261–279. doi: 10.1242/jcs.36.1.261. [DOI] [PubMed] [Google Scholar]
  12. Feit I. N., Fournier G. A., Needleman R. D., Underwood M. Z. Induction of stalk and spore cell differentiation by cyclic AMP in slugs of Dictyostelium discoideum. Science. 1978 Apr 28;200(4340):439–441. doi: 10.1126/science.205945. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Gerisch G., Hess B. Cyclic-AMP-controlled oscillations in suspended Dictyostelium cells: their relation to morphogenetic cell interactions. Proc Natl Acad Sci U S A. 1974 May;71(5):2118–2122. doi: 10.1073/pnas.71.5.2118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gerisch G., Wick U. Intracellular oscillations and release of cyclic AMP from Dictyostelium cells. Biochem Biophys Res Commun. 1975 Jul 8;65(1):364–370. doi: 10.1016/s0006-291x(75)80102-1. [DOI] [PubMed] [Google Scholar]
  16. Gilman A. G. A protein binding assay for adenosine 3':5'-cyclic monophosphate. Proc Natl Acad Sci U S A. 1970 Sep;67(1):305–312. doi: 10.1073/pnas.67.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Jacobson A., Lodish H. F. Genetic control of development of the cellular slime mold, Dictyostelium discoideum. Annu Rev Genet. 1975;9:145–185. doi: 10.1146/annurev.ge.09.120175.001045. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Klein C., Juliani M. H. cAMP,-induced changes in cAMP-binding sites on D; discoideum amebae. Cell. 1977 Feb;10(2):329–335. doi: 10.1016/0092-8674(77)90227-6. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Matsukuma S., Durston A. J. Chemotactic cell sorting in Dictyostelium discoideum. J Embryol Exp Morphol. 1979 Apr;50:243–251. [PubMed] [Google Scholar]
  23. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  24. Robertson A., Drage D. J., Cohen M. H. Control of Aggregation in Dictyostelium discoideum by an External Periodic Pulse of Cyclic Adenosine Monophosphate. Science. 1972 Jan 21;175(4019):333–335. doi: 10.1126/science.175.4019.333. [DOI] [PubMed] [Google Scholar]
  25. Rosen S. D., Kafka J. A., Simpson D. L., Barondes S. H. Developmentally regulated, carbohydrate-binding protein in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1973 Sep;70(9):2554–2557. doi: 10.1073/pnas.70.9.2554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Rubin J. The signal from fruiting body and conus tips of Dictyostelium discoideum. J Embryol Exp Morphol. 1976 Oct;36(2):261–271. [PubMed] [Google Scholar]
  28. Shaffer B. M. Secretion of cyclic AMP induced by cyclic AMP in the cellular slime mould Dictyostelium discoideum. Nature. 1975 Jun 12;255(5509):549–552. doi: 10.1038/255549a0. [DOI] [PubMed] [Google Scholar]
  29. Takemoto S., Okamoto K., Takeuchi I. The effects of cyclic AMP on disaggregation-induced changes in activities of developmentally regulated enzymes in Dictyostelium discoideum. Biochem Biophys Res Commun. 1978 Feb 28;80(4):858–865. doi: 10.1016/0006-291x(78)91323-2. [DOI] [PubMed] [Google Scholar]
  30. Town C., Gross J. The role of cyclic nucleotides and cell agglomeration in postaggregative enzyme synthesis in Dictyostelium discoideum. Dev Biol. 1978 Apr;63(2):412–420. doi: 10.1016/0012-1606(78)90145-8. [DOI] [PubMed] [Google Scholar]
  31. Wurster B., Schubiger K., Wick U., Gerisch G. Cyclic GMP in Dictyostelium discoideum, Oscillations and pulses in response to folic acid and cyclic AMP signals. FEBS Lett. 1977 Apr 15;76(2):141–144. doi: 10.1016/0014-5793(77)80139-7. [DOI] [PubMed] [Google Scholar]

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