Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1983 Jun 1;96(6):1559–1565. doi: 10.1083/jcb.96.6.1559

Sensory adaptation of Dictyostelium discoideum cells to chemotactic signals

PMCID: PMC2112430  PMID: 6304109

Abstract

Postvegetative Dictyostelium discoideum cells react chemotactically to gradients of cAMP, folic acid, and pterin. In the presence of a constant concentration of 10(-5) M cAMP cells move at random. They still are able to respond to superimposed gradients of cAMP, although the response is less efficient than without the high background level of cAMP. Cells which are accommodated to 10(-5) M cAMP do not react to a gradient of cAMP if the mean cAMP concentration is decreasing with time. This indicates the involvement of adaptation in the detection of chemotactic gradients: cells adapt to the mean concentration of chemoattractant and respond to positive deviations from the mean concentration. Cells adapted to high cAMP concentrations react normally to gradients of folic acid or pterin. Adaptation to one of these compounds does not affect the response to the other attractants. This suggests that cAMP, folic acid, and pterin are detected by different receptors, and that adaptation is localized at a step in the transduction process before the signals from these receptors coincide into one pathway. I discuss the implications of adaptation for chemotaxis and cell aggregation.

Full Text

The Full Text of this article is available as a PDF (900.2 KB).

Selected References

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

  1. Bonner J. T., Barkley D. S., Hall E. M., Konijn T. M., Mason J. W., O'Keefe G., 3rd, Wolfe P. B. Acrasin, Acrasinase, and the sensitivity to acrasin in Dictyostelium discoideum. Dev Biol. 1969 Jul;20(1):72–87. doi: 10.1016/0012-1606(69)90005-0. [DOI] [PubMed] [Google Scholar]
  2. Bonner J. T., Kelso A. P., Gillmor R. G. A new approach to the problem of aggregation in the cellular slime molds. Biol Bull. 1966 Feb;130(1):28–42. doi: 10.2307/1539950. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Dinauer M. C., Steck T. L., Devreotes P. N. Cyclic 3',5'-AMP relay in Dictyostelium discoideum IV. Recovery of the cAMP signaling response after adaptation to cAMP. J Cell Biol. 1980 Aug;86(2):545–553. doi: 10.1083/jcb.86.2.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dinauer M. C., Steck T. L., Devreotes P. N. Cyclic 3',5'-AMP relay in Dictyostelium discoideum V. Adaptation of the cAMP signaling response during cAMP stimulation. J Cell Biol. 1980 Aug;86(2):554–561. doi: 10.1083/jcb.86.2.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Futrelle R. P. Dictyostelium chemotactic response to spatial and temporal gradients. Theories of the limits of chemotactic sensitivity and of pseudochemotaxis. J Cell Biochem. 1982;18(2):197–212. doi: 10.1002/jcb.1982.240180207. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Gerisch G., Hülser D., Malchow D., Wick U. Cell communication by periodic cyclic-AMP pulses. Philos Trans R Soc Lond B Biol Sci. 1975 Nov 6;272(915):181–192. doi: 10.1098/rstb.1975.0080. [DOI] [PubMed] [Google Scholar]
  10. Green A. A., Newell P. C. Evidence for the existence of two types of cAMP binding sites in aggregating cells of Dictyostelium discoideum. Cell. 1975 Oct;6(2):129–136. doi: 10.1016/0092-8674(75)90003-3. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Macnab R. M., Koshland D. E., Jr The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2509–2512. doi: 10.1073/pnas.69.9.2509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Malchow D., Gerisch G. Short-term binding and hydrolysis of cyclic 3':5'-adenosine monophosphate by aggregating Dictyostelium cells. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2423–2427. doi: 10.1073/pnas.71.6.2423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Malchow D., Nägele B., Schwarz H., Gerisch G. Membrane-bound cyclic AMP phosphodiesterase in chemotactically responding cells of Dictyostelium discoideum. Eur J Biochem. 1972 Jun 23;28(1):136–142. doi: 10.1111/j.1432-1033.1972.tb01894.x. [DOI] [PubMed] [Google Scholar]
  15. Mato J. M., Krens F. A., van Haastert P. J., Konijn T. M. 3':5'-cyclic AMP-dependent 3':5'-cyclic GMP accumulation in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2348–2351. doi: 10.1073/pnas.74.6.2348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mato J. M., Krens F. A., van Haastert P. J., Konijn T. M. Unified control of chemotaxis and cAMP mediated cGMP accumulation by cAMP in Dictyostelium discoideum. Biochem Biophys Res Commun. 1977 Jul 11;77(1):399–402. doi: 10.1016/s0006-291x(77)80211-8. [DOI] [PubMed] [Google Scholar]
  17. Mato J. M., Van Haastert P. J., Krens F. A., Rhijnsburger E. H., Dobbe F. C., Konijn T. M. Cyclic AMP and folic acid mediated cyclic GMP accumulation in Dictyostelium discoideum. FEBS Lett. 1977 Jul 15;79(2):331–336. doi: 10.1016/0014-5793(77)80814-4. [DOI] [PubMed] [Google Scholar]
  18. Nandini-Kishore S. G., Frazier W. A. [3H]Methotrexate as a ligand for the folate receptor of Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7299–7303. doi: 10.1073/pnas.78.12.7299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pan P., Hall E. M., Bonner J. T. Determination of the active portion of the folic acid molecule in cellular slime mold chemotaxis. J Bacteriol. 1975 Apr;122(1):185–191. doi: 10.1128/jb.122.1.185-191.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pan P., Hall E. M., Bonner J. T. Folic acid as second chemotactic substance in the cellular slime moulds. Nat New Biol. 1972 Jun 7;237(75):181–182. doi: 10.1038/newbio237181a0. [DOI] [PubMed] [Google Scholar]
  21. Pannbacker R. G., Bravard L. J. Phosphodiesterase in Dictyostelium discoideum and the chemotactic response to cyclic adenosine monophosphate. Science. 1972 Mar 3;175(4025):1014–1015. doi: 10.1126/science.175.4025.1014. [DOI] [PubMed] [Google Scholar]
  22. Roos W., Nanjundiah V., Malchow D., Gerisch G. Amplification of cyclic-AMP signals in aggregating cells of Dictyostelium discoideum. FEBS Lett. 1975 May 1;53(2):139–142. doi: 10.1016/0014-5793(75)80005-6. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Swanson J. A., Taylor D. L. Local and spatially coordinated movements in Dictyostelium discoideum amoebae during chemotaxis. Cell. 1982 Feb;28(2):225–232. doi: 10.1016/0092-8674(82)90340-3. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Van Haastert P. J., Van Walsum H., Pasveer F. J. Nonequilibrium kinetics of a cyclic GMP-binding protein in Dictyostelium discoideum. J Cell Biol. 1982 Aug;94(2):271–278. doi: 10.1083/jcb.94.2.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Van Haastert P. J., Van der Heijden P. R. Excitation, adaptation, and deadaptation of the cAMP-mediated cGMP response in Dictyostelium discoideum. J Cell Biol. 1983 Feb;96(2):347–353. doi: 10.1083/jcb.96.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wurster B., Bozzaro S., Gerisch G. Cyclic GMP regulation and responses of Polysphondylium violaceum to chemoattractants. Cell Biol Int Rep. 1978 Jan;2(1):61–69. doi: 10.1016/0309-1651(78)90085-1. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Zigmond S. H. Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J Cell Biol. 1977 Nov;75(2 Pt 1):606–616. doi: 10.1083/jcb.75.2.606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zigmond S. H. Mechanisms of sensing chemical gradients by polymorphonuclear leukocytes. Nature. 1974 May 31;249(456):450–452. doi: 10.1038/249450a0. [DOI] [PubMed] [Google Scholar]
  32. Zigmond S. H., Sullivan S. J. Sensory adaptation of leukocytes to chemotactic peptides. J Cell Biol. 1979 Aug;82(2):517–527. doi: 10.1083/jcb.82.2.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. van Haastert P. J., De Wit R. J., Konijn T. M. Antagonists of chemoattractants reveal separate receptors for cAMP, folic acid and pterin in Dictyostelium. Exp Cell Res. 1982 Aug;140(2):453–456. doi: 10.1016/0014-4827(82)90139-2. [DOI] [PubMed] [Google Scholar]
  34. van Haastert P. J., van Lookeren Campagne M. M., Ross F. M. Altered cGMP-phosphodiesterase activity in chemotactic mutants of Dictyostelium discoideum. FEBS Lett. 1982 Oct 18;147(2):149–152. doi: 10.1016/0014-5793(82)81029-6. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES