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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1997 Mar 29;352(1351):391–417. doi: 10.1098/rstb.1997.0029

A discrete cell model with adaptive signalling for aggregation of Dictyostelium discoideum.

J C Dallon 1, H G Othmer 1
PMCID: PMC1691935  PMID: 9134569

Abstract

Dictyostelium discoideum (Dd) is a widely studied model system from which fundamental insights into cell movement, chemotaxis, aggregation and pattern formation can be gained. In this system aggregation results from the chemotactic response by dispersed amoebae to a travelling wave of the chemoattractant cAMP. We have developed a model in which the cells are treated as discrete points in a continuum field of the chemoattractant, and transduction of the extracellular cAMP signal into the intracellular signal is based on the G protein model developed by Tang & Othmer. The model reproduces a number of experimental observations and gives further insight into the aggregation process. We investigate different rules for cell movement the factors that influence stream formation the effect on aggregation of noise in the choice of the direction of movement and when spiral waves of chemoattractant and cell density are likely to occur. Our results give new insight into the origin of spiral waves and suggest that streaming is due to a finite amplitude instability.

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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. Claviez M., Brink M., Gerisch G. Cytoskeletons from a mutant of Dictyostelium discoideum with flattened cells. J Cell Sci. 1986 Dec;86:69–82. doi: 10.1242/jcs.86.1.69. [DOI] [PubMed] [Google Scholar]
  3. DeYoung G., Monk P. B., Othmer H. G. Pacemakers in aggregation fields of Dictyostelium discoideum: does a single cell suffice? J Math Biol. 1988;26(5):487–517. doi: 10.1007/BF00276057. [DOI] [PubMed] [Google Scholar]
  4. Durston A. J. Pacemaker activity during aggregation in Dictyostelium discoideum. Dev Biol. 1974 Apr;37(2):225–235. doi: 10.1016/0012-1606(74)90144-4. [DOI] [PubMed] [Google Scholar]
  5. Fisher P. R. Pseudopodium activation and inhibition signals in chemotaxis by Dictyostelium discoideum amoebae. Semin Cell Biol. 1990 Apr;1(2):87–97. [PubMed] [Google Scholar]
  6. Futrelle R. P., Traut J., McKee W. G. Cell behavior in Dictyostelium discoideum: preaggregation response to localized cyclic AMP pulses. J Cell Biol. 1982 Mar;92(3):807–821. doi: 10.1083/jcb.92.3.807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gingle A. R., Robertson A. The development of the relaying competence in Dictyostelium discoideum. J Cell Sci. 1976 Jan;20(1):21–27. doi: 10.1242/jcs.20.1.21. [DOI] [PubMed] [Google Scholar]
  8. Höfer T., Sherratt J. A., Maini P. K. Dictyostelium discoideum: cellular self-organization in an excitable biological medium. Proc Biol Sci. 1995 Mar 22;259(1356):249–257. doi: 10.1098/rspb.1995.0037. [DOI] [PubMed] [Google Scholar]
  9. Kuwayama H., Ishida S., Van Haastert P. J. Non-chemotactic Dictyostelium discoideum mutants with altered cGMP signal transduction. J Cell Biol. 1993 Dec;123(6 Pt 1):1453–1462. doi: 10.1083/jcb.123.6.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Levine H, Reynolds W. Streaming instability of aggregating slime mold amoebae. Phys Rev Lett. 1991 May 6;66(18):2400–2403. doi: 10.1103/PhysRevLett.66.2400. [DOI] [PubMed] [Google Scholar]
  11. Lilly P. J., Devreotes P. N. Chemoattractant and GTP gamma S-mediated stimulation of adenylyl cyclase in Dictyostelium requires translocation of CRAC to membranes. J Cell Biol. 1995 Jun;129(6):1659–1665. doi: 10.1083/jcb.129.6.1659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. MacKay S. A. Computer simulation of aggregation in Dictyostelium discoideum. J Cell Sci. 1978 Oct;33:1–16. doi: 10.1242/jcs.33.1.1. [DOI] [PubMed] [Google Scholar]
  13. McRobbie S. J. Chemotaxis and cell motility in the cellular slime molds. Crit Rev Microbiol. 1986;13(4):335–375. doi: 10.3109/10408418609108742. [DOI] [PubMed] [Google Scholar]
  14. Monk P. B., Othmer H. G. Cyclic AMP oscillations in suspensions of Dictyostelium discoideum. Philos Trans R Soc Lond B Biol Sci. 1989 Mar 15;323(1215):185–224. doi: 10.1098/rstb.1989.0005. [DOI] [PubMed] [Google Scholar]
  15. Parnas H., Segel L. A. Computer evidence concerning the chemotactic signal in Dictyostelium discoideum. J Cell Sci. 1977 Jun;25:191–204. doi: 10.1242/jcs.25.1.191. [DOI] [PubMed] [Google Scholar]
  16. Pitt G. S., Brandt R., Lin K. C., Devreotes P. N., Schaap P. Extracellular cAMP is sufficient to restore developmental gene expression and morphogenesis in Dictyostelium cells lacking the aggregation adenylyl cyclase (ACA). Genes Dev. 1993 Nov;7(11):2172–2180. doi: 10.1101/gad.7.11.2172. [DOI] [PubMed] [Google Scholar]
  17. Raman R. K., Hashimoto Y., Cohen M. H., Robertson A. Differentiation for aggregation in the cellular slime moulds: the emergence of autonomously signalling cells in Dictyostelium discoideum. J Cell Sci. 1976 Jul;21(2):243–259. doi: 10.1242/jcs.21.2.243. [DOI] [PubMed] [Google Scholar]
  18. Ross F. M., Newell P. C. Streamers: chemotactic mutants of Dictyostelium discoideum with altered cyclic GMP metabolism. J Gen Microbiol. 1981 Dec;127(2):339–350. doi: 10.1099/00221287-127-2-339. [DOI] [PubMed] [Google Scholar]
  19. Siu C. H., Kamboj R. K. Cell-cell adhesion and morphogenesis in Dictyostelium discoideum. Dev Genet. 1990;11(5-6):377–387. doi: 10.1002/dvg.1020110509. [DOI] [PubMed] [Google Scholar]
  20. Snaar-Jagalska B. E., Van Haastert P. J. Pertussis toxin inhibits cAMP-induced desensitization of adenylate cyclase in Dictyostelium discoideum. Mol Cell Biochem. 1990 Feb 9;92(2):177–189. doi: 10.1007/BF00218135. [DOI] [PubMed] [Google Scholar]
  21. Tang Y., Othmer H. G. A G protein-based model of adaptation in Dictyostelium discoideum. Math Biosci. 1994 Mar;120(1):25–76. doi: 10.1016/0025-5564(94)90037-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tang Y., Othmer H. G. Excitation, oscillations and wave propagation in a G-protein-based model of signal transduction in Dictyostelium discoideum. Philos Trans R Soc Lond B Biol Sci. 1995 Aug 29;349(1328):179–195. doi: 10.1098/rstb.1995.0102. [DOI] [PubMed] [Google Scholar]
  23. Theibert A., Devreotes P. N. Surface receptor-mediated activation of adenylate cyclase in Dictyostelium. Regulation by guanine nucleotides in wild-type cells and aggregation deficient mutants. J Biol Chem. 1986 Nov 15;261(32):15121–15125. [PubMed] [Google Scholar]
  24. 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]
  25. Valkema R., Van Haastert P. J. A model for cAMP-mediated cGMP response in Dictyostelium discoideum. Mol Biol Cell. 1994 May;5(5):575–585. doi: 10.1091/mbc.5.5.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Varnum-Finney B. J., Voss E., Soll D. R. Frequency and orientation of pseudopod formation of Dictyostelium discoideum amebae chemotaxing in a spatial gradient: further evidence for a temporal mechanism. Cell Motil Cytoskeleton. 1987;8(1):18–26. doi: 10.1002/cm.970080104. [DOI] [PubMed] [Google Scholar]
  27. Varnum B., Edwards K. B., Soll D. R. Dictyostelium amebae alter motility differently in response to increasing versus decreasing temporal gradients of cAMP. J Cell Biol. 1985 Jul;101(1):1–5. doi: 10.1083/jcb.101.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Vasiev BN, Hogeweg P, Panfilov AV. Simulation of dictyostelium discoideum aggregation via reaction-diffusion model. Phys Rev Lett. 1994 Dec 5;73(23):3173–3176. doi: 10.1103/PhysRevLett.73.3173. [DOI] [PubMed] [Google Scholar]
  29. Wessels D., Soll D. R., Knecht D., Loomis W. F., De Lozanne A., Spudich J. Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Dev Biol. 1988 Jul;128(1):164–177. doi: 10.1016/0012-1606(88)90279-5. [DOI] [PubMed] [Google Scholar]

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