The Dictyostelium discoideum genome uncovers seven cyclic nucleotide PDEs (phosphodiesterases), of which six have been characterized previously and the seventh is characterized in the present paper. Three enzymes belong to the ubiquitous class I PDEs, common in all eukaryotes, whereas four enzymes belong to the rare class II PDEs that are present in bacteria and lower eukaryotes. Since all D. discoideum PDEs are now characterized we have calculated the contribution of each enzyme in the degradation of the three important pools of cyclic nucleotides: (i) extracellular cAMP that induces chemotaxis during aggregation and differentiation in slugs; (ii) intracellular cAMP that mediates development; and (iii) intracellular cGMP that mediates chemotaxis. It appears that each cyclic nucleotide pool is degraded by a combination of enzymes that have different affinities, allowing a broad range of substrate concentrations to be degraded with first-order kinetics. Extracellular cAMP is degraded predominantly by the class II high-affinity enzyme DdPDE1 and its close homologue DdPDE7, and in the multicellular stage also by the low-affinity transmembrane class I enzyme DdPDE4. Intracellular cAMP is degraded by the DdPDE2, a class I enzyme regulated by histidine kinase/phospho-relay, and by the cAMP-/cGMP-stimulated class II DdPDE6. Finally, basal intracellular cGMP is degraded predominantly by the high-affinity class I DdPDE3, while the elevated cGMP levels that arise after receptor stimulation are degraded predominantly by a cGMP-stimulated cGMP-specific class II DdPDE5. The analysis shows that the combination of enzymes is tuned to keep the concentration and lifetime of the substrate within a functional range.
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February 2007
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Research Article|
January 25 2007
Seven Dictyostelium discoideum phosphodiesterases degrade three pools of cAMP and cGMP
Sonya Bader;
Sonya Bader
1
1Department of Molecular Cell Biology, University of Groningen, Kerklaan 30, 9751NN, Haren, The Netherlands
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Arjan Kortholt;
Arjan Kortholt
1
1Department of Molecular Cell Biology, University of Groningen, Kerklaan 30, 9751NN, Haren, The Netherlands
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Peter J. M. Van Haastert
Peter J. M. Van Haastert
2
1Department of Molecular Cell Biology, University of Groningen, Kerklaan 30, 9751NN, Haren, The Netherlands
2To whom correspondence should be addressed (email P.J.M.van.Haastert@rug.nl).
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Publisher: Portland Press Ltd
Received:
July 28 2006
Revision Received:
October 05 2006
Accepted:
October 16 2006
Accepted Manuscript online:
October 16 2006
Online ISSN: 1470-8728
Print ISSN: 0264-6021
The Biochemical Society, London
2007
Biochem J (2007) 402 (1): 153–161.
Article history
Received:
July 28 2006
Revision Received:
October 05 2006
Accepted:
October 16 2006
Accepted Manuscript online:
October 16 2006
Citation
Sonya Bader, Arjan Kortholt, Peter J. M. Van Haastert; Seven Dictyostelium discoideum phosphodiesterases degrade three pools of cAMP and cGMP. Biochem J 15 February 2007; 402 (1): 153–161. doi: https://doi.org/10.1042/BJ20061153
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