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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
. 1995 May 9;92(10):4387–4391. doi: 10.1073/pnas.92.10.4387

Three-dimensional scroll waves of cAMP could direct cell movement and gene expression in Dictyostelium slugs.

T Bretschneider 1, F Siegert 1, C J Weijer 1
PMCID: PMC41949  PMID: 7753816

Abstract

Complex three-dimensional waves of excitation can explain the observed cell movement pattern in Dictyostelium slugs. Here we show that these three-dimensional waves can be produced by a realistic model for the cAMP relay system [Martiel, J. L. & Goldbeter, A. (1987) Biophys J. 52, 807-828]. The conversion of scroll waves in the prestalk zone of the slug into planar wave fronts in the prespore zone can result from a smaller fraction of relaying cells in the prespore zone. Further, we show that the cAMP concentrations to which cells in a slug are exposed over time display a simple pattern, despite the complex spatial geometry of the waves. This cAMP distribution agrees well with observed patterns of cAMP-regulated cell type-specific gene expression. The core of the spiral, which is a region of low cAMP concentration, might direct expression of stalk-specific genes during culmination.

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Selected References

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  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. Berks M., Kay R. R. Combinatorial control of cell differentiation by cAMP and DIF-1 during development of Dictyostelium discoideum. Development. 1990 Nov;110(3):977–984. doi: 10.1242/dev.110.3.977. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. 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]
  6. Firtel R. A. Signal transduction pathways controlling multicellular development in Dictyostelium. Trends Genet. 1991 Nov-Dec;7(11-12):381–388. doi: 10.1016/0168-9525(91)90260-w. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Hopper N. A., Anjard C., Reymond C. D., Williams J. G. Induction of terminal differentiation of Dictyostelium by cAMP-dependent protein kinase and opposing effects of intracellulr and extracellular cAMP on stalk cell differentiation. Development. 1993 Sep;119(1):147–154. doi: 10.1242/dev.119.1.147. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Johnson R. L., Van Haastert P. J., Kimmel A. R., Saxe C. L., 3rd, Jastorff B., Devreotes P. N. The cyclic nucleotide specificity of three cAMP receptors in Dictyostelium. J Biol Chem. 1992 Mar 5;267(7):4600–4607. [PubMed] [Google Scholar]
  12. Martiel J. L., Goldbeter A. A Model Based on Receptor Desensitization for Cyclic AMP Signaling in Dictyostelium Cells. Biophys J. 1987 Nov;52(5):807–828. doi: 10.1016/S0006-3495(87)83275-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Matsukuma S., Durston A. J. Chemotactic cell sorting in Dictyostelium discoideum. J Embryol Exp Morphol. 1979 Apr;50:243–251. [PubMed] [Google Scholar]
  14. Otte A. P., Plomp M. J., Arents J. C., Janssens P. M., van Driel R. Production and turnover of cAMP signals by prestalk and prespore cells in Dictyostelium discoideum cell aggregates. Differentiation. 1986;32(3):185–191. doi: 10.1111/j.1432-0436.1986.tb00572.x. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Schaap P., van Driel R. V. Induction of post-aggregative differentiation in Dictyostelium discoideum by cAMP. Evidence of involvement of the cell surface cAMP receptor. Exp Cell Res. 1985 Aug;159(2):388–398. doi: 10.1016/s0014-4827(85)80012-4. [DOI] [PubMed] [Google Scholar]
  17. Siegert F., Weijer C. J. Three-dimensional scroll waves organize Dictyostelium slugs. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6433–6437. doi: 10.1073/pnas.89.14.6433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Steinbock O., Siegert F., Müller S. C., Weijer C. J. Three-dimensional waves of excitation during Dictyostelium morphogenesis. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7332–7335. doi: 10.1073/pnas.90.15.7332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Tomchik K. J., Devreotes P. N. Adenosine 3',5'-monophosphate waves in Dictyostelium discoideum: a demonstration by isotope dilution--fluorography. Science. 1981 Apr 24;212(4493):443–446. doi: 10.1126/science.6259734. [DOI] [PubMed] [Google Scholar]
  21. Tyson J. J., Murray J. D. Cyclic AMP waves during aggregation of Dictyostelium amoebae. Development. 1989 Jul;106(3):421–426. doi: 10.1242/dev.106.3.421. [DOI] [PubMed] [Google Scholar]
  22. Wessels D., Murray J., Soll D. R. Behavior of Dictyostelium amoebae is regulated primarily by the temporal dynamic of the natural cAMP wave. Cell Motil Cytoskeleton. 1992;23(2):145–156. doi: 10.1002/cm.970230207. [DOI] [PubMed] [Google Scholar]

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