Skip to content
1887

Microbiology Society logo Microbiology

Volume 139, Issue 12

Developmental and cAMP-mediated regulation of glycogen phosphorylase 1 in Free

Abstract

The glycogen phosphorylase-1 (gp-1) exhibits a complex pattern of developmental expression in which differential temporal regulation of enzyme activity, protein levels and mRNA levels is observed. This pattern of expression implies that gp-1 regulation occurs at multiple levels, probably involving both transcriptional and post-transcriptional events. Post-translational control of gp-1 activity, in effect, actually regulates the protein from a developmental perspective. In this report we have examined several facets of this regulation. We show that addition of exogenous cAMP to cells in suspension culture caused changes in gp-1 enzyme activity and mRNA levels that are identical to those observed during normal development, suggesting that cAMP is involved in the regulation of gp-1. Exogenous cAMP could regulate gp-1 mRNA expression at concentrations as low as 1·0 μ. cAMP regulation of gp-1 mRNA appeared to occur through a mechanism that required intracellular cAMP signalling. We identified regions of the promoter necessary for gp-1 expression by using gp-1 promoter deletions to drive the expression of a luciferase reporter gene. Results of these experiments suggested that developmental and cAMP-mediated changes in gp-1 mRNA levels were the result of alterations in transcription. The promoter analysis also suggested that a vegetative specific element is located between −785 and −1894 nucleotides from the transcriptional start site. Elements necessary for maximal developmental and cAMP-mediated expression appear to be located between −1153 and −1894 nucleotides from the cap site. Sequence elements located between −180 and −1153 appear to be required for a basal level of late developmental expression.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Society for General Microbiology, 1993
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-139-12-3043
1993-12-01
2025-01-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/139/12/mic-139-12-3043.html?itemId=/content/journal/micro/10.1099/00221287-139-12-3043&mimeType=html&fmt=ahah

References

  1. Bradford M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248–254
     [Google Scholar]
  2. Brenner M., Thoms S.D. 1984; Caffeine blocks activation of cyclic AMP synthesis in Dictyostelium discoideum. Developmental Biology 101:136–146
     [Google Scholar]
  3. Brickey D.A., Naranan V., Sucic J.F., Rutherford C.L. 1990; Regulation of the two forms of glycogen phosphorylase by cAMP and its analogs in Dictyostelium discoideum. Molecular and Cellular Biochemistry 97:17–33
     [Google Scholar]
  4. Datta S., Firtel R.A. 1988; An 80-bp cis-acting regulatory region controls cAMP and development regulation of a prestalk gene in Dictyostelium. Genes and Development 2:294–304
     [Google Scholar]
  5. Early A., Williams J.G. 1989; Identification of sequences regulating the transcription of a Dictyostelium gene selectively expressed in pre-spore cells. Nucleic Acids Research 17:6473–6484
     [Google Scholar]
  6. Europe-Finner G.N., Newell P.C. 1986; Inositol 1,4,5,-trisphosphate induces calcium release from a non-mitochondrial pool in amoebae of Dictyostelium. Biochimica et Biophysica Acta 887:335–340
     [Google Scholar]
  7. Europe-Finner G.N., Newell P.C. 1987; Cyclic AMP stimulates accumulation of inositol trisphosphate in Dictyostelium. Journal of Cell Science 87:221–229
     [Google Scholar]
  8. Faix I., Gerisch G., Noegel A.A. 1992; Overexpression of the csA cell adhesion molecule under its own cAMP-regulated promoter impairs morphogenesis in Dictyostelium. Journal of Cell Science 102:203–214
     [Google Scholar]
  9. Feinberg A.P., Vogelstein B. 1983; A technique for radiolabeling restriction endonuclease fragments to high specific activity. Ana-lytical Biochemistry 132:6–13
     [Google Scholar]
  10. Fosnaugh K.L., Loomis W.F. 1991; Coordinate regulation of the spore coat genes in Dictyostelium. Developmental Genetics 12:123–132
     [Google Scholar]
  11. Gerisch G. 1987; Cyclic AMP and other signals controlling cell differentiation in Dictyostelium. Annual Review of Biochemistry 56:853–879
     [Google Scholar]
  12. Ginsburg G., Kimmel A.R. 1989; Inositol trisphosphate and diacylglycerol can differentially modulate gene expression in Dictyostelium. Proceedings of the National Academy of Sciences of the United States of America 869332–9336
     [Google Scholar]
  13. Gustafson G.L., Wright B.E. 1972; Analysis of approaches used in studying differentiation of the cellular slime mold. Critical Reviews in Microbiology 1:453–478
     [Google Scholar]
  14. Haberstroh L., Firtel R.A. 1990; A spatial gradient of expression of a cAMP-regulated prespore cell-type-specific gene in Dictyostelium. Genes and Development 4:596–612
     [Google Scholar]
  15. Haberstroh L., Galindo J., Firtel R.A. 1991; Developmental and spatial regulation of a Dictyostelium prespore gene: cis-acting elements and a cAMP induced, developmentally regulated DNA binding activity. Development 113:947–958
     [Google Scholar]
  16. Haribabu B., Dottin R.P. 1986; Pharmacological characterization of cyclic AMP receptors mediating gene regulation in Dictyostelium discoideum. Molecular and Cellular Biology 6:2402–2408
     [Google Scholar]
  17. Janssens P.M.W., Van Haastert P.J.M. 1987; Molecular basis of transmembrane signal transduction in Dictyostelium. Microbiological Reviews 51:396–418
     [Google Scholar]
  18. Khoury G., Gruss P. 1983; Enhancer elements. Cell 33:313–314
     [Google Scholar]
  19. Kimmel A.R. 1987; Different molecular mechanisms for cAMP regulation of gene expression during Dictyostelium development. Developmental Biology 122:163–171
     [Google Scholar]
  20. Loomis W.F. 1982 The Development of Dictyostelium discoideum. New York: Academic Press;
     [Google Scholar]
  21. Mann S.K.O., Firtel R.A. 1987; Cyclic AMP regulation of early gene expression in Dictyostelium discoideum: mediation via the cell surface cyclic AMP receptor. Molecular and Cellular Biology 7:458–169
     [Google Scholar]
  22. Marshall R., Sargent D., Wright B.E. 1970; Glycogen turnover in Dictyostelium discoideum. Biochemistry 9:3087–3094
     [Google Scholar]
  23. Naranan V., Sucic J.F., Brickey D.A., Rutherford C.L. 1988; The relationship between the two forms of glycogen phosphorylase in Dictyostelium discoideum. Differentiation 38:1–10
     [Google Scholar]
  24. Nellen W., Silan C., Firtel R.A. 1984; DNA-mediated transformation in Dictyostelium discoideum: regulated expression of an actin gene fusion. Molecular and Cellular Biology 4:2890–2898
     [Google Scholar]
  25. Nellen W., Datta S., Reymond C., Sivertsen A., Mann S., Crowley T., Firtel R.A. 1987; Molecular biology in Dictyostelium: tools and applications. Methods in Cell Biology 28:67–108
     [Google Scholar]
  26. Oyama M., Blumberg D.D. 1986; Interaction of cAMP with the cell surface receptor induces cell-type-specific mRNA accumulation in Dictyostelium discoideum. Proceedings of the National Academy of Sciences of the United States of America 834819–4823
     [Google Scholar]
  27. Pahlic M., Rutherford C.L. 1979; Adenylate cyclase activity and cyclic AMP levels during the development of Dictyostelium discoideum. Journal of Biological Chemistry 254:9703–9707
     [Google Scholar]
  28. Pavlovic J., Haribabu B., Dottin R.P. 1989; Identification of a signal transduction response sequence element necessary for induction of a Dictyostelium discoideum gene by extracellular cAMP. Molecular and Cellular Biology 9:4660–4669
     [Google Scholar]
  29. Pears C.J., Williams J.G. 1987; Identification of a DNA sequence element required for efficient expression of a developmentally regulated and cAMP-inducible gene of Dictyostelium discoideum. EMBO Journal 6:195–200
     [Google Scholar]
  30. Pears C.J., Williams J.G. 1988; Multiple copies of a G-rich element upstream of a cAMP inducible Dictyostelium gene are necessary but not sufficient for efficient gene expression. Nucleic Acids Research 16:8467–8486
     [Google Scholar]
  31. Rogers P.V., Luo S., Sucic J.F., Rutherford C.L. 1992; Characterization and cloning of glycogen phosphorylase 1 from Dictyostelium discoideum. Biochimica et Biophysica Acta 1129:262–272
     [Google Scholar]
  32. Rutherford C.L., Cloutier M.J. 1986; Identification of two forms of glycogen phosphorylase in Dictyostelium. Archives of Biochemistry and Biophysics 250:435–439
     [Google Scholar]
  33. Rutherford C.L., Peery R.B., Sucic J.F., Yin Y., Rogers P.V., Luo S., Selmin O. 1992; Cloning, structural analysis, and expression of the glycogen phosphorylase 2 gene in Dictyostelium. Journal of Biological Chemistry 267:2294–2302
     [Google Scholar]
  34. Schaap P., Van lookeren Campagne M.M., Van Driel R., Spek W., Van Haastert P.J.M., Pinas J. 1986; Postaggregative differentiation induction by cyclic AMP in Dictyostelium-. intra-cellular transduction pathway and requirement for additional stimuli. Developmental Biology 118:52–63
     [Google Scholar]
  35. Schaffner W., Serfling E., Jasin M. 1985; Enhancers and eukaryotic gene transcription. Trends in Genetics 1:224–230
     [Google Scholar]
  36. Sussman M., Brackenbury R. 1976; Biochemical and molecular genetic aspects of cellular slime mold development. Annual Review of Plant Physiology 27:229–265
     [Google Scholar]
  37. Tasaka M., Hasegawa M., Nakata M., Orii H., Ozaki T., Takeuchi I. 1992; Protein binding and DNase-I-hypersensitive sites in the cis-acting regulatory region of the spore-coat SP96 gene of Dictyostelium. Mechanisms of Development 36:105–115
     [Google Scholar]
  38. Wright B.E., Simon W., Walsh B.T. 1968; A kinetic model of metabolism essential to differentiation in Dictyostelium discoideum. Proceedings of the National Academy of Sciences of the United States of America 60644–651
     [Google Scholar]
/content/journal/micro/10.1099/00221287-139-12-3043
Loading
Developmental and cAMP-mediated regulation of glycogen phosphorylase 1 in Dictyostelium discoideum
Microbiology 139, 3043 (1993); https://doi.org/10.1099/00221287-139-12-3043
/content/journal/micro/10.1099/00221287-139-12-3043
/content/journal/micro/10.1099/00221287-139-12-3043
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error