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Dual role of cAMP duringDictyostelium development

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Abstract

cAMP plays an essential role duringDictyostelium development both outside and inside the cell. Membrane-bound receptors and adenylyl cyclase are responsible for sensing and producing extracellular cAMP, whereas a phosphodiesterase is responsible for maintaining a low basal level. The molecular events underlying this type of hormone like signalling, which are now beginning to be deciphered, will be presented, in the light of cAMP analogue studies. The importance of intracellular cAMP for cell differentiation has been demonstrated by the central role of the cAMP dependent protein kinase. Mutants as well as strains obtained by reverse genetics will be reviewed which lead to our current understanding of the role of intracellular cAMP in the differentiation of both stalk and spore cells.

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References

  1. Abe, K., and Yanagisawa, K., A new class of rapid developing mutants inDictyostelium discoideum: Implications for cyclic AMP metabolism and cell differentiation. Devl Biol.95 (1983) 200–210.

    Article  CAS  Google Scholar 

  2. Abe, T., Early, A., Siegert, F., Weijer, C., and Williams, J., Patterns of cell movement within theDictyostelium slug revealed by cell type-specific, surface labeling of living cells. Cell77 (1994) 687–699.

    Article  PubMed  Google Scholar 

  3. Aeckerle, S., Wurster, B., and Malchow, D., Oscillations and cyclic AMP induced changes of the K+ concentration inDictyostelium discoideum. EMBO J.4 (1985) 39–43.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Anjard, C., Etchebehere, L., Pinaud, S., Véron, M., and Reymond, C. D., An unusual catalytic subunit for the cAMP-dependent protein kinase ofDictyostelium discoideum. Biochemistry32 (1993) 9532–9538.

    Article  CAS  PubMed  Google Scholar 

  5. Anjard, C., Pinaud, S., Kay, R. R., and Reymond, C. D., Overexpression of Dd. PK2 protein kinase causes rapid development and affects intracellular cAMP pathway ofDictyostelium discoideum. Development115 (1992) 785–790.

    Article  CAS  PubMed  Google Scholar 

  6. Berks, M., and Kay, R. R., Combinatorial control of cell differentiation by cAMP and DIF-1 during development ofDictyostelium discoideum. Development110 (1990) 977–984.

    Article  CAS  PubMed  Google Scholar 

  7. Blusch, J. H., and Nellen, W., Folate responsiveness during growth and development ofDictyostelium: separate but related pathways control chemotaxis and gene regulation. Molec. Microbiol.11 (1994) 331–335.

    Article  CAS  Google Scholar 

  8. Bominaar, A. A., and Van Haastert, P. J. M., Chemotactic antagonists of cAMP inhibitDictyostelium phospholipase C. J. Cell Sci.104 (1993) 181–185.

    Article  CAS  PubMed  Google Scholar 

  9. Brachet, P., Dicou, E. L., and Klein, C., Inhibition of cell differentiation in a phosphodiesterase defective mutant ofDictyostelium discoideum. Cell Differ.8 (1979) 255–265.

    Article  CAS  PubMed  Google Scholar 

  10. Caterina, M. J., Milne, J. L., and Devreotes, P. N., Mutation of the third intracellular loop of the cAMP receptor, cAR1, ofDictyostelium yields mutants impaired in multiple signaling pathways. J. biol. Chem.269 (1994) 1523–1532.

    Article  CAS  PubMed  Google Scholar 

  11. Darmon, M., Brachet, P., and Pereira da Silva, L. H., Chemotactic signals induce cell differentiation inDictyostelium discoideum. Proc. natl Acad. Sci. USA72 (1975) 3163–3166.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. De Gunzburg, J., Part, D., Guiso, N., and Veron, M., An unusual adenosine 3′,5′-phosphate dependent protein kinase fromDictyostelium discoideum. Biochemistry23 (1984) 3805–3812.

    Article  PubMed  Google Scholar 

  13. Devreotes, P. N., Chemotaxis, in: Development ofDictyostelium discoideum, pp. 117–168. Ed. W. F. Loomis. Academic Press Inc., New York 1982.

    Chapter  Google Scholar 

  14. Early, A. E., Gaskell, M. J., Traynor, D., and Williams, J. G., Two distinct populations of prestalk cells within the tip of the migratoryDictyostelium slug with differing fates at culmination. Development118 (1993) 353–362.

    Article  CAS  PubMed  Google Scholar 

  15. Europe-Finner, G. N., and Newell, P. C., Cyclic AMP stimulates accumulation of inositol triphosphate inDictyostelium. J. Cell Sci.87 (1987) 221–229.

    Article  CAS  PubMed  Google Scholar 

  16. Faure, M., Franke, J., Hall, A. L., Podgorski, G. J., and Kessin, R. H., The cyclic nucleotide phosphodiesterase gene ofDictyostelium discoideum contains 3 promoters specific for growth, aggregation, and late development. Molec. cell. Biol.10 (1990) 1921–1930.

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Faure, M., Podgorski, G. J., Franke, J., and Kessin, R. H., Disruption ofDictyostelium discoideum morphogenesis by overproduction of cAMP phosphodiesterase. Proc. natl Acad. Sci. USA85 (1988) 8076–8080.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Faure, M., Podgorski, G. J., Franke, J., and Kessin, R. H., Rescue of aDictyostelium discoideum mutant defective in cyclic nucleotide phosphodiesterase. Devl Biol.131 (1989) 366–372.

    Article  CAS  Google Scholar 

  19. Franke, J., Podgorski, G. J., and Kessin, R. H., The expression of two transcripts of the phosphodiesterase gene during the development ofDictyostelium discoideum. Devl Biol.124 (1987) 504–511.

    Article  CAS  Google Scholar 

  20. Gee, K., Russell, F., and Gross, J. D., Ammonia hypersensitivity of slugger mutants of D.discoideum. J. Cell Sci.107 (1994) 701–708.

    Article  CAS  PubMed  Google Scholar 

  21. Gerisch, G., Fromm, H., Huesgen, A., and Wick, U., Control of cell-contact sites by cyclic AMP pulses in differentiatingDictyostelium cells. Nature, Lond.255 (1975) 547–549.

    Article  CAS  PubMed  Google Scholar 

  22. Gross, J. D., Bradbury, J., Kay, R. R., and Peacey, M. J., Intracellular pH and the control of cell differentiation inDictyostelium discoideum. Nature, Lond.303 (1983) 244–245.

    Article  CAS  PubMed  Google Scholar 

  23. Hadwiger, J. A., Wilkie, T. M., Strathmann, M., and Firtel, R. A., Identification ofDictyostelium G alpha genes expressed during multicellular development. Proc. natl Acad. Sci. USA88 (1991) 8213–8217.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Harwood, A. J., Hopper, N. A., Simon, M. N., Bouzid, S., Véron, M., and Williams, J. G., Multiple roles for cAMP-dependent protein kinase duringDictyostelium development. Devl Biol.149 (1992) 90–99.

    Article  CAS  Google Scholar 

  25. Harwood, A. J., Hopper, N. A., Simon, M. N., Driscoll, D. M., Véron, M., and Williams, J. G., Culmination inDictyostelium is regulated by the cAMP-dependent protein kinase. Cell69 (1992) 615–624.

    Article  CAS  PubMed  Google Scholar 

  26. Hassanain, H. H., and Kopachik, W., Regulatory signals affecting a selective loss of messenger RNA inDictyostelium discoideum. J. Cell Sci.94 (1989) 501–509.

    Article  CAS  PubMed  Google Scholar 

  27. Hereld, D., and Devreotes, P. N., The cAMP receptor family ofDictyostelium. Int. Rev. Cytol.137 (1993) 35–47.

    Article  Google Scholar 

  28. Hopper, N. A., Anjard, C., Reymond, C. D., and Williams, J. G., Induction of terminal differentiation ofDictyostelium by cAMP dependent protein kinase and opposing effects of intracellular and extracellular cAMP on stalk cell diferentiation. Development119 (1993) 147–154.

    Article  CAS  PubMed  Google Scholar 

  29. Hopper, N. A., Harwood, A. J., Bouzid, S., Véron, M., and Williams, J. G., Activation of the prespore and spore cell pathway ofDictyostelium differentiation by cAMP-dependent protein kinase and evidence for its upstream regulation by ammonia. EMBO J.12 (1993) 2459–2466.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Inouye, K. and Gross, J. D., In vitro stalk cell differentiation in wild-type and slugger mutants ofDictyostelium discoideum. Development118 (1993) 523–526.

    Article  CAS  Google Scholar 

  31. Insall, R. H., Soede, R. D. M., Schaap, P., and Devreotes, P. N., Two cAMP receptors activate common signalling pathways inDictyostelium. Molec. Biol. Cell5 (1994) 703–711.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Jermyn, K. A., and Williams, J. G., An analysis of culmination inDictyostelium using prestalk and stalk-specific cell autonomous markers. Development111 (1991) 779–787.

    Article  CAS  PubMed  Google Scholar 

  33. Johnson, R. L., Saxe, C. L., Gollop, R., Kimmel, A. R., and Devreotes, P. N., Identification and targeted gene disruption of cAR3, a cAMP receptor subtype expressed during multicellular stages ofDictyostelium development. Genes Dev.7 (1993) 273–282.

    Article  CAS  PubMed  Google Scholar 

  34. Johnson, R. L., Van Haastert, P. J. M., Kimmel, A. R., Saxe, C. L., Jastorff, B., and Devreotes, P. N., The cyclic nucleotide specificity of three cAMP receptors inDictyostelium. J. biol. Chem.267 (1992) 4600–4607.

    Article  CAS  PubMed  Google Scholar 

  35. Kay, R. R., cAMP and spore differentiation inDictyostelium discoideum. Proc. natl Acad. Sci. USA79 (1982) 3228–3231.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Kay, R. R., Evidence that elevated intracellular cyclic AMP triggers spore maturation inDictyostelium. Development105 (1989) 753–759.

    Article  CAS  Google Scholar 

  37. Kimmel, A. R., and Carlisle, B., A gene expressed in undifferentiated vegetativeDictyostelium is repressed by developmental pulses of cAMP and reinduced during dedifferentiation. Proc. natl Acad. Sci. USA83 (1986) 2506–2510.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Klein, C., and Juliani, M. H., c-AMP induced changes in c-AMP-binding sites onDictyostelium discoideum amoebae. Cell10 (1977) 329–335.

    Article  CAS  PubMed  Google Scholar 

  39. Klein, P. S., Sun, T. J., Saxe, C. L., Kimmel, A. R., Johnson, R. L., and Devreotes, P. N., A chemoattractant receptor controls development inDictyostelium discoideum. Science241 (1988) 1467–1472.

    Article  CAS  PubMed  Google Scholar 

  40. Kubohara, Y., Maeda, M., and Okamoto, K., Analysis of the maturation process of prestalk cells inDictyostelium discoideum. Expl Cell Res.207 (1993) 107–114.

    Article  CAS  Google Scholar 

  41. Kumagai, A., Pupillo, M., Gundersen, R., Miake-Lye, R., Devreotes, P. N., and Firtel, R. A., Regulation and function of Gα protein subunits inDictyostelium. Cell57 (1989) 265–275.

    Article  CAS  PubMed  Google Scholar 

  42. Lilly, P., Wu, L., Welker, D. L., and Devreotes, P. N., A G-protein beta-subunit is essential forDictyostelium development. Genes Dev.7 (1993) 986–995.

    Article  CAS  PubMed  Google Scholar 

  43. Lilly, P. J., and Devreotes, P. N., Identification of CRAC, a cytosolic regulator required for guanine nucleotide stimulation of adenylyl cyclase inDictyostelium. J. biol. Chem.269 (1994) 14123–14129.

    Article  CAS  PubMed  Google Scholar 

  44. Louis, J. M., Ginsburg, G. T., and Kimmel, A. R., The cAMP receptor cAR4 regulates axial patterning and cellular differentiation during late development ofDictyostelium. Genes Dev.8 (1994) 2086–2096.

    Article  CAS  PubMed  Google Scholar 

  45. Louvion, J. F., Scholder, J. C., Pinaud, S., and Reymond, C. D., Two independent promoters as well as 5′ untranslated regions regulateDd ras expression inDictyostelium. Nucleic Acids Res.19 (1991) 6133–6138.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Malchow, D., Nanjundiah, V., Wurster, B., Eckstein, F., and Gerisch, G., Cyclic AMP-induced pH changes inDictyostelium discoideum and their control by calcium. Biochim. biophys. Acta538 (1978) 473–480.

    Article  CAS  PubMed  Google Scholar 

  47. Mann, S. K. and Firtel, R. A., Two-phase regulatory pathway controls cAMP receptor-mediated expression of early genes inDictyostelium. Proc. natl Acad. Sci. USA 86 (1989) 1924–1928.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Mann, S. K., Yonemoto, W. M., Taylor, S. S., and Firtel, R. A., DdPK3, which plays essential roles duringDictyostelium development, encodes the catalytic subunit of cAMP-dependent protein kinase. Proc. natl Acad. Sci. USA89 (1992) 10701–10705.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Martiel, J.-L., and Goldbeter, A., A model based on receptor desensitization for cyclic AMP signaling inDictyostelium cells. Biophys. J.52 (1987) 807–828.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Mato, J. M., Krens, F. A., Van Haastert, P. J. M., and Konijn, T. M., 3′:5′-Cyclic AMP-dependent 3′:5′-cyclic GMP accumulation inDictyostelium discoideum. Proc. natl Acad. Sci. USA74 (1977) 2348–2351.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Mehdy, M. C., and Firtel, R. A., A secreted factor and cyclic AMP jointly regulate cell-type-specific gene expression inDictyostelium discoideum. Molec. cell. Biol.5 (1985) 705–713.

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Milne, J. L., and Coukell, M. B., A Ca2+ transport system associated with the plasma membrane ofDictyostelium discoideum is activated by different chemoattractant receptors. J. Cell Biol.112 (1991) 103–110.

    Article  CAS  PubMed  Google Scholar 

  53. Mutzel, R., Lacombe, M. L., Simon, M. N., De Gunzburg, J., and Véron, M., Cloning and cDNA sequence of the regulatory subunit of cAMP-dependent protein kinase fromDictyostelium discoideum. Proc. natl Acad. Sci. USA84 (1987) 6–10.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Oyama, M., and Blumberg, D. D., Interaction of cAMP with the cell-surface receptor induces cell-type-specific mRNA accumulation inDictyostelium discoideum. Proc. natl Acad. Sci. USA83 (1986) 4819–4823.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Peters, D. J. M., Bominaar, A. A., Snaar-Jagalska, B. E., Brandt, R., Van Haastert, P. J. M., Ceccarelli, A., Williams, J. G., and Schaap, P., Selective induction of gene expression and second-messenger accumulation inDictyostelium discoideum by the partial chemotactic antagonist 8-para-chlorophenylthioadenosine 3′,5′-cyclic monophosphate. Proc. natl Acad. Sci. USA88 (1991) 9219–9223.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Pitt, G. S., Milona, N., Borleis, J., Lin, K. C., Reed, R. R., and Devreotes, P. N., Structurally distinct and stage-specific adenylyl cyclase genes play different roles inDictyostelium development. Cell69 (1992) 305–315.

    Article  CAS  PubMed  Google Scholar 

  57. Podgorski, G. J., Franke, J., Faure, M., and Kessin, R. H., The cyclic nucleotide phosphodiesterase gene ofDictyostelium discoideum utilizes alternate promotors and splicing for the synthesis of multiple mRNAs. Molec. cell. Biol.9 (1989) 3938–3950.

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Franke, J., Faure, M., Wu, L., Hall, A. L., Podgorski, G. J., and Kessin, R. H., Cyclic nucleotide phosphodiesterase ofDictyostelium discoideum and its glycoprotein inhibitor-structure and expression of their genes. Devl Genet.12 (1991) 104–112.

    Article  CAS  Google Scholar 

  59. Pupillo, M., Insall, R., Pitt, G. S., and Devreotes, P. N., Multiple cyclic AMP receptors are linked to adenylyl cyclase inDictyostelium. Molec. Biol. Cell3 (1992) 1229–1234.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Pupillo, M., Kumagai, A., Pitt, G. S., Firtel, R. A., and Devreotes, P. N., Multiple alpha subunits of guanine nucleotide-binding proteins inDictyostelium. Proc. natl Acad. Sci. USA86 (1989) 4892–4896.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Reymond, C. D., Gomer, R. H., Mehdy, M. C., and Firtel, R. A., Developmental regulation of aDictyostelium gene encoding a protein homologous to mammalianras protein. Cell39 (1984) 141–148.

    Article  CAS  PubMed  Google Scholar 

  62. Riley, B. B. and Barclay, S. L., Ammonia promotes accumulation of intracellular cAMP in differentiating amoebae ofDictyostelium discoideum. Development109 (1990) 715–722.

    Article  CAS  PubMed  Google Scholar 

  63. Roos, W., Nanjundiah, V., Malchow, D., and Gerisch, G., Amplification of cyclic-AMP signals in aggregating cells ofDictyostelium discoideum. FEBS Lett.53 (1975) 139–142.

    Article  CAS  PubMed  Google Scholar 

  64. Saxe, C. L., Ginsburg, G. T., Louis, J. M., Johnson, R., Devreotes, P. N., and Kimmel, A. R., cAR2, a prestalk cAMP receptor required for normal tip formation and late development ofDictyostelium discoideum. Genes Dev.7 (1993) 262–272.

    Article  CAS  PubMed  Google Scholar 

  65. Schaap, P., and Van Driel, R., Induction of post-aggregative differentiation inDictyostelium discoideum by cAMP. Evidence for the involvement of the cell surface cAMP receptor. Expl Cell Res.159 (1985) 388–398.

    Article  CAS  Google Scholar 

  66. Schaap, P., Van Ments Cohen, M., Soede, R. D., Brandt, R., Firtel, R. A., Dostmann, W., Genieser, H. G., Jastorff, B., and Van Haastert, P. J. M., Cell-permeable non-hydrolyzable cAMP derivatives as tools for analysis of signaling pathways controlling gene regulation inDictyostelium. J. biol. Chem.268 (1993) 6323–6331.

    Article  CAS  PubMed  Google Scholar 

  67. Shaffer, B. M., Secretion of cyclic AMP induced by cyclic AMP in the cellular slime mouldDictyostelium discoideum. Nature255 (1975) 549–552.

    Article  CAS  PubMed  Google Scholar 

  68. Simon, M. N., Driscoll, D., Mutzel, R., Part, D., Williams, J., and Véron, M., Overproduction of the regulatory subunit of the cAMP-dependent protein kinase blocks the differentiation ofDictyostelium discoideum. EMBO J.8 (1989) 2039–2044.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Simon, M. N., Pelegrini, O., Véron, M., and Kay, R. R., Mutation of protein kinase-A causes heterochronic development ofDictyostelium. Nature356 (1992) 171–172.

    Article  CAS  PubMed  Google Scholar 

  70. Snaar-Jagalska, B. E. and Van Haastert, P. J. M., Pertussis toxin inhibits cAMP-induced desensitization of adenylate cyclase inDictyostelium discoideum. Molec. cell. Biochem.92 (1990) 177–189.

    Article  CAS  PubMed  Google Scholar 

  71. Snaar-Jagalska, B. E., Vanes, S., Kesbeke, F., and Van Haastert, P. J. M., Activation of a pertussis-toxin-sensitive guanine-nucleotide-binding regulatory protein during desensitization ofDictyostelium discoideum cells to chemotactic signals. Eur. J. Biochem.195 (1991) 715–721.

    Article  CAS  PubMed  Google Scholar 

  72. Sternfeld, J., and David, C. N., Cell sorting during pattern formation inDictyostelium. Differentiation20 (1981) 10–21.

    Article  CAS  Google Scholar 

  73. Tang, Y., and Othmer, H. G., A G-protein-based model of adaptation inDictyostelium discoideum. Mathl Biosci.120 (1994) 25–76.

    Article  CAS  Google Scholar 

  74. Theibert, A., and Devreotes, P. N., Surface receptor-mediated activation of adenylate cyclase inDictyostelium Regulation by guanine nucleotides in wild-type cells and aggregation deficient mutants. J. biol. Chem.261 (1986) 15,121–15,125.

    Article  CAS  Google Scholar 

  75. Theibert, A., Palmisano, M., Jastorff, B., and Devreotes, P.N., The specificity of the cAMP receptor mediating activation of adenylate cyclase inDictyostelium discoideum. Devl Biol.114 (1986) 529–533.

    Article  CAS  Google Scholar 

  76. Van Haastert, P. J. M., Guanine nucleotides modulate cell surface cAMP-binding sites in membranes fromDictyostelium discoideum. Biochem. biophys. Res. Commun.124 (1984) 597–604.

    Article  PubMed  Google Scholar 

  77. Van Haastert, P. J. M., De Vries, M. J., Penning, L. C., Roovers, F., Van der Kaay, J., Erneux, C., and Van Lookeren Campagne, M. M., Chemoattractant and guanosine 5′-[γ-thio]triphosphate induce the accumulation of inositol 1,4,5-trisphophate inDictyostelium cells that are labelled with [3H]inositol by electroporation. Biochem. J.258 (1989) 577–586.

    Article  PubMed Central  PubMed  Google Scholar 

  78. Van Haastert, P.J.M., and Kien, E., Binding of cAMP derivatives toDictyostelium discoideum cells. J. biol. Chem.258 (1983) 9636–9642.

    Article  PubMed  Google Scholar 

  79. Van Haastert, P. J. M., Van Driel, R., Jastorff, B., Baraniak, J., Stec, W. J., and De Wit, R. J. W., Competitive cAMP antagonists for cAMP-receptor proteins. J. biol. Chem.259 (1984) 10020–10024.

    Article  PubMed  Google Scholar 

  80. Van Haastert, P. J. M., Wang, M., Bominaar, A. A., Devreotes, P. N., and Schaap, P., cAMP-induced desensitization of surface cAMP receptors inDictyostelium—different second messengers mediate receptor phosphorylation, loss of ligand binding, degradation of receptor, and reduction of receptor messenger RNA levels. Molec. Biol. Cell3 (1992) 603–612.

    Article  PubMed Central  PubMed  Google Scholar 

  81. Véron, M., Radzio Andzelm, E., Tsigelny, I., Ten Eyck, L. F., and Taylor, S. S., A conserved helix motif complements the protein kinase core. Proc. natl Acad. Sci. USA90 (1993) 10,618–10,622.

    Article  Google Scholar 

  82. Wang, M., Van Driel, R., and Schaap, P., Cyclic AMP-phosphodiesterase induces dedifferentiation of prespore cells inDictyostelium discoideum slugs: evidence that cyclic AMP is the morphogenetic signal for prespore differentiation. Development103 (1988) 611–618.

    Article  CAS  Google Scholar 

  83. Wang, M., Van Haastert, P. J. M., Devreotes, P. N., and Schaap, P., Localization of chemoattractant receptors onDictyostelium discoideum cells during aggregation and down-regulation. Devl Biol.128 (1988) 72–77.

    Article  CAS  Google Scholar 

  84. Williams, G. B., Elders, E. M., and Sussman, M., Modulation of the cAMP relay inDictyostelium discoideum by ammonia and other metabolites: Possible morphogenetic consequences. Devl Biol.105 (1984) 377–388.

    Article  CAS  Google Scholar 

  85. Wu, L., and Franke, J., A developmentally regulated and cAMP-repressible gene ofDictyostelium discoideum—cloning and expression of the gene encoding cyclic nucleotide phosphodiesterase inhibitor. Gene91 (1990) 51–56.

    Article  CAS  PubMed  Google Scholar 

  86. Wu, L. J., and Devreotes, P. N.,Dictyostelium transiently expresses eight distinct G-protein alpha-subunits during its developmental program. Biochem. biophys. Res. Commun.179 (1991) 1141–1147.

    Article  CAS  PubMed  Google Scholar 

  87. Wurster, B., Schubiger, K., Wick, U., and Gerisch, G., Cyclic GMP inDictyostelium discoideum: Oscillations and pulses in response to folic acid and cyclic AMP signals. FEBS Lett.76 (1977) 141–144.

    Article  CAS  PubMed  Google Scholar 

  88. Yeh, R. P., Chan, F. K., and Coukell, M. B., Independent regulation of the extracellular cyclic AMP phosphodiesterase-inhibitor system and membrane differentiation by exogenous cyclic AMP. Devl Biol.66 (1978) 361–374.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institut d'Histologie et d'Embryologie, University of Lausanne, Rue du Bugnon 9, CH-1005, Lausanne, Switzerland

    C. D. Reymond

  2. Clusius Laboratory, Institute of Molecular Plant Sciences, Leiden University, Wassenaarseweg 64, NL-2333 AL, Leiden, The Netherlands

    P. Schaap

  3. Unité de Biochimie Cellulaire, Institut Pasteur, 28 Rue du Dr. Roux, F-75724, Paris, Cedex 15, France

    M. Véron

  4. MRC Laboratory for Cell Biology, University College London, Gower Street, WC1E 6BT, London, UK

    J. G. Williams

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Reymond, C.D., Schaap, P., Véron, M. et al. Dual role of cAMP duringDictyostelium development. Experientia 51, 1166–1174 (1995). https://doi.org/10.1007/BF01944734

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