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. 1984 Apr;81(7):2127–2131. doi: 10.1073/pnas.81.7.2127

Differential cellular distribution of cAMP-dependent protein kinase during development of Dictyostelium discoideum

Kristin L Schaller *,, Ben H Leichtling *, Irene H Majerfeld *, Clive Woffendin *, Eva Spitz *, Shizuko Kakinuma *, Howard V Rickenberg *,†,
PMCID: PMC345450  PMID: 16593449

Abstract

It was shown previously by us that cAMP-dependent protein kinase activity in the cellular slime mold Dictyostelium discoideum increased during the early stages of development. Results from other laboratories showed that during the subsequent stage of cell differentiation and positioning, the accumulation of a number of prespore mRNAs and proteins (but not prestalk mRNAs and proteins) was dependent upon cAMP. The present communication describes the cellular distribution of the cAMP-dependent protein kinase at that stage of development. Pseudoplasmodia were disrupted, and prespore cells were separated from prestalk cells by sedimentation through a Percoll gradient. Prespore cells had approximately 4-5 times as much of both the catalytic and regulatory subunits of the cAMP-dependent protein kinase as did the prestalk cells. That the increase of cAMP-dependent protein kinase during development reflected de novo synthesis of the enzyme in both prespore and prestalk cells was demonstrated on the basis of [3H]leucine incorporation into the regulatory subunit. The findings are consistent with a role of the cAMP-dependent protein kinase in mediating the effects of cAMP on the synthesis of prespore-specific mRNAs and proteins at the stage at which cAMP appears to be required for the cell type-specific syntheses.

Keywords: prespore, prestalk, pattern formation, cell-cell contact

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Selected References

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  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. Blumberg D. D., Lodish H. F. Changes in the messenger RNA population during differentiation of dictyostelium discoideum. Dev Biol. 1980 Aug;78(2):285–300. doi: 10.1016/0012-1606(80)90337-1. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Garrod D. R., Ashworth I. M. Effect of growth conditions on development of the cellular slime mould, Dictyostelium discoideum. J Embryol Exp Morphol. 1972 Oct;28(2):463–479. [PubMed] [Google Scholar]
  5. Gunzburg J., Veron M. A cAMP-dependent protein kinase is present in differentiating Dictyostelium discoideum cells. EMBO J. 1982;1(9):1063–1068. doi: 10.1002/j.1460-2075.1982.tb01297.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Juliani M. H., Brochetto M. R., Da Costa Maia J. C. Changes in cyclic AMP binding and protein kinase activities during growth and differentiation of Blastocladiella emersonii. Cell Differ. 1979 Dec;8(6):421–430. doi: 10.1016/0045-6039(79)90038-1. [DOI] [PubMed] [Google Scholar]
  7. Kay R. R. Gene expression in Dictyostelium discoidium: mutually antagonistic roles of cyclic-AMP and ammonia. J Embryol Exp Morphol. 1979 Aug;52:171–182. [PubMed] [Google Scholar]
  8. Landfear S. M., Lodish H. F. A role for cyclic AMP in expression of developmentally regulated genes in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1980 Feb;77(2):1044–1048. doi: 10.1073/pnas.77.2.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Leichtling B. H., Majerfeld I. H., Coffman D. S., Rickenberg H. V. Identification of the regulatory subunit of a cAMP-dependent protein kinase in Dictyostelium discoideum. Biochem Biophys Res Commun. 1982 Apr 14;105(3):949–955. doi: 10.1016/0006-291x(82)91062-2. [DOI] [PubMed] [Google Scholar]
  10. Leichtling B. H., Majerfeld I. H., Spitz E., Schaller K. L., Woffendin C., Kakinuma S., Rickenberg H. V. A cytosolic cyclic AMP-dependent protein kinase in Dictyostelium discoideum. II. Developmental regulation. J Biol Chem. 1984 Jan 10;259(1):662–668. [PubMed] [Google Scholar]
  11. Leichtling B. H., Spitz E., Rickenberg H. V. A cAMP-binding protein from Dictyostelium discoideum regulates mammalian protein kinase. Biochem Biophys Res Commun. 1981 May 29;100(2):515–522. doi: 10.1016/s0006-291x(81)80207-0. [DOI] [PubMed] [Google Scholar]
  12. Liu A. Y. Differentiation-specific increase of cAMP-dependent protein kinase in the 3T3-L1 cells. J Biol Chem. 1982 Jan 10;257(1):298–306. [PubMed] [Google Scholar]
  13. Loomis W. F. The spatial pattern of cell-type differentiation in Dictyostelium. Dev Biol. 1982 Oct;93(2):279–284. doi: 10.1016/0012-1606(82)90117-8. [DOI] [PubMed] [Google Scholar]
  14. Majerfeld I. H., Leichtling B. H., Meligeni J. A., Spitz E., Rickenberg H. V. A cytosolic cyclic AMP-dependent protein kinase in Dictyostelium discoideum. I. Properties. J Biol Chem. 1984 Jan 10;259(1):654–661. [PubMed] [Google Scholar]
  15. Mangiarotti G., Ceccarelli A., Lodish H. F. Cyclic AMP stabilizes a class of developmentally regulated Dictyostelium discoideum mRNAs. Nature. 1983 Feb 17;301(5901):616–618. doi: 10.1038/301616a0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Ratner D., Borth W. Comparison of differentiating Dictyostelium discoideum cell types separated by an improved method of density gradient centrifugation. Exp Cell Res. 1983 Jan;143(1):1–13. doi: 10.1016/0014-4827(83)90103-9. [DOI] [PubMed] [Google Scholar]
  19. Rutherford C. L., Taylor R. D., Frame L. T., Auck R. L. A cyclic AMP dependent protein kinase in Dictyostelium discoideum. Biochem Biophys Res Commun. 1982 Oct 15;108(3):1210–1220. doi: 10.1016/0006-291x(82)92129-5. [DOI] [PubMed] [Google Scholar]
  20. SUSSMAN M., OSBORN M. J. UDP-GALACTOSE POLYSACCHARIDE TRANSFERASE IN THE CELLULAR SLIME MOLD, DICTYOSTELIUM DISCOIDEUM: APPEARANCE AND DISAPPEARANCE OF ACTIVITY DURING CELL DIFFERENTIATION. Proc Natl Acad Sci U S A. 1964 Jul;52:81–87. doi: 10.1073/pnas.52.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Tasaka M., Noce T., Takeuchi I. Prestalk and prespore differentiation in Dictyostelium as detected by cell type-specific monoclonal antibodies. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5340–5344. doi: 10.1073/pnas.80.17.5340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Watts D. J., Ashworth J. M. Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J. 1970 Sep;119(2):171–174. doi: 10.1042/bj1190171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. de Gunzburg J., Veron M. Intracellular adenosine 3',5'-phosphate binding proteins in Dictyostelium discoideum: partial purification and characterization in aggregation competent cells. Biochemistry. 1981 Aug 4;20(16):4547–4554. doi: 10.1021/bi00519a006. [DOI] [PubMed] [Google Scholar]

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