Binding of cyclic nucleotides to phosphodiesterase 10A and 11A GAF domains does not stimulate catalytic activity

Biochemical Journal

Volumn 423, Issue 3, 2009, Pages 401-409

  Matthiesen, Karina ^a   Nielsen, Jacob ^a  

^a H LUNDBECK A S   (Denmark)

Author keywords

Anabena adenylate cyclases and Escherichia coli Fh1A (GAF) domain; cAMP; cGMP; cGMP specific and stimulated phosphodiesterases; Phosphodiesterase 10A (PDE10A); Phosphodiesterase 11A (PDE11A); Scintillation proximity assay

Indexed keywords

ANABENA ADENYLATE CYCLASES AND ESCHERICHIA COLI FH1A (GAF) DOMAIN; CAMP; CGMP; CGMP-SPECIFIC AND -STIMULATED PHOSPHODIESTERASES; PHOSPHODIESTERASE 10A (PDE10A); PHOSPHODIESTERASE 11A (PDE11A);

AIRCRAFT ENGINES; BIOCHEMISTRY; BIOLOGICAL MEMBRANES; CATALYST ACTIVITY; ELECTROCHEMICAL SENSORS; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYMES; ESCHERICHIA COLI; FETAL MONITORING; LIGANDS; LUMINESCENCE; NUCLEIC ACIDS; SCINTILLATION;

NUCLEOTIDES;

3',5' CYCLIC NUCLEOTIDE PHOSPHODIESTERASE; 3',5' CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 10A; 3',5' CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 11A; 3',5' CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 2A; 3',5' CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 5A; 3',5' CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 6; CYCLIC GMP SPECIFIC AND STIMULATED PHOSPHODIESTERASE; UNCLASSIFIED DRUG;

ANABAENA; ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME LOCALIZATION; ESCHERICHIA COLI; HUMAN; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SCINTILLATION;

CATALYSIS; CYCLIC AMP; CYCLIC GMP; HUMANS; PHOSPHORIC DIESTER HYDROLASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

ANABAENA; ESCHERICHIA COLI;

EID: 70350124064     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20090982     Document Type: Article

References (37)

1. Beavo, J. A. and Brunton, L. L. (2002) Cyclic nucleotide research - still expanding after half a century. Nat. Rev. Mol. Cell. Biol. 3, 710-718
2. Defer, N., Best-Belpomme, M. and Hanoune, J. (2000) Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. Am. J. Physiol. Renal Physiol. 279, F400-F416
3. Koesling, D., Bohme, E. and Schultz, G. (1991) Guanylyl cyclases, a growing family of signal-transducing enzymes. FASEB J. 5, 2785-2791
4. Terrin, A., Di, B. G., Pertegato, V., Cheung, Y. F., Baillie, G., Lynch, M. J., Elvassore, N., Prinz, A., Herberg, F. W., Houslay, M. D. and Zaccolo, M. (2006) PGE(1) stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: role of compartmentalized phosphodiesterases. J. Cell. Biol. 175, 441-451
5. Beavo, J. A. (1995) Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol. Rev. 75, 725-748
6. Soderling, S. H. and Beavo, J. A. (2000) Regulation of cAMP and cGMP signaling: new phosphodiesterases and new functions. Curr. Opin. Cell Biol. 12, 174-179
7. Fawcett, L., Baxendale, R., Stacey, P., McGrouther, C., Harrow, I., Soderling, S., Hetman, J., Beavo, J. A. and Phillips, S. C. (2000) Molecular cloning and characterization of a distinct human phosphodiesterase gene family: PDE11A. Proc. Natl. Acad. Sci. U.S.A. 97, 3702-3707
8. Bender, A. T. and Beavo, J. A. (2006) Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol. Rev. 58, 488-520
9. Lugnier, C. (2006) Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol. Ther. 109, 366-398
10. Soderling, S. H., Bayuga, S. J. and Beavo, J. A. (1999) Isolation and characterization of a dual-substrate phosphodiesterase gene family: PDE10A. Proc. Natl. Acad. Sci. U.S.A. 96, 7071-7076
11. Fujishige, K., Kotera, J., Michibata, H., Yuasa, K., Takebayashi, S., Okumura, K. and Omori, K. (1999) Cloning and characterization of a novel human phosphodiesterase that hydrolyzes both cAMP and cGMP (PDE10A). J. Biol. Chem. 274, 18438-18445
12. Seeger, T. F., Bartlett, B., Coskran, T. M., Culp, J. S., James, L. C., Krull, D. L., Lanfear, J., Ryan, A. M., Schmidt, C. J., Strick, C. A. et al. (2003) Immunohistochemical localization of PDE10A in the rat brain. Brain Res. 985, 113-126
13. Siuciak, J. A., Chapin, D. S., Harms, J. F., Lebel, L. A., McCarthy, S. A., Chambers, L., Shrikhande, A., Wong, S., Menniti, F. S. and Schmidt, C. J. (2006) Inhibition of the striatum-enriched phosphodiesterase PDE10A: a novel approach to the treatment of psychosis. Neuropharmacology 51, 386-396
14. Wayman, C., Phillips, S., Lunny, C., Webb, T., Fawcett, L., Baxendale, R. and Burgess, G. (2005) Phosphodiesterase 11 (PDE11) regulation of spermatozoa physiology. Int. J. Impot. Res. 17, 216-223
15. Aravind, L. and Ponting, C. P. (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem. Sci. 22, 458-459
16. Martinez, S. E., Beavo, J. A. and Hol, W. G. (2002) GAF domains: two-billion-year-old molecular switches that bind cyclic nucleotides. Mol. Interv. 2, 317-323
17. Wu, A. Y., Tang, X. B., Martinez, S. E., Ikeda, K. and Beavo, J. A. (2004) Molecular determinants for cyclic nucleotide binding to the regulatory domains of phosphodiesterase 2A. J. Biol. Chem. 279, 37928-37938
18. Zoraghi, R., Bessay, E. P., Corbin, J. D. and Francis, S. H. (2005) Structural and functional features in human PDE5A1 regulatory domain that provide for allosteric cGMP binding, dimerization, and regulation. J. Biol. Chem. 280, 12051-12063
19. Martins, T. J., Mumby, M. C. and Beavo, J. A. (1982) Purification and characterization of a cyclic GMP-stimulated cyclic nucleotide phosphodiesterase from bovine tissues. J. Biol. Chem. 257, 1973-1979
20. Francis, S. H., Bessay, E. P., Kotera, J., Grimes, K. A., Liu, L., Thompson, W. J. and Corbin, J. D. (2002) Phosphorylation of isolated human phosphodiesterase-5 regulatory domain induces an apparent conformational change and increases cGMP binding affinity. J. Biol. Chem. 277, 47581-47587
21. Gillespie, P. G. and Beavo, J. A. (1988) Characterization of a bovine cone photoreceptor phosphodiesterase purified by cyclic GMP-sepharose chromatography. J. Biol. Chem. 263, 8133-8141
22. Cote, R. H. and Brunnock, M. A. (1993) Intracellular cGMP concentration in rod photoreceptors is regulated by binding to high and moderate affinity cGMP binding sites. J. Biol. Chem. 268, 17190-17198
23. Erneux, C., Couchie, D., Dumont, J. E., Baraniak, J., Stec, W. J., Abbad, E. G., Petridis, G. and Jastorff, B. (1981) Specificity of cyclic GMP activation of a multi-substrate cyclic nucleotide phosphodiesterase from rat liver. Eur. J. Biochem. 115, 503-510
24. Martinez, S. E., Wu, A. Y., Glavas, N. A., Tang, X. B., Turley, S., Hol, W. G. and Beavo, J. A. (2002) The two GAF domains in phosphodiesterase 2A have distinct roles in dimerization and in cGMP binding. Proc. Natl. Acad. Sci. U.S.A. 99, 13260-13265
25. Rybalkin, S. D., Rybalkina, I. G., Shimizu-Albergine, M., Tang, X. B. and Beavo, J. A. (2003) PDE5 is converted to an activated state upon cGMP binding to the GAFa domain. EMBO J. 22, 469-478
26. Arshavsky, V. Y., Dumke, C. L. and Bownds, M. D. (1992) Noncatalytic cGMP-binding sites of amphibian rod cGMP phosphodiesterase control interaction with its inhibitory gamma-subunits. A putative regulatory mechanism of the rod photoresponse. J. Biol. Chem. 267, 24501-24507
27. Gross-Langenhoff, M., Hofbauer, K., Weber, J., Schultz, A. and Schultz, J. E. (2006) cAMP is a ligand for the tandem GAF domain of human phosphodiesterase 10 and cGMP for the tandem GAF domain of phosphodiesterase 11. J. Biol. Chem. 281, 2841-2846
28. Gross-Langenhoff, M., Stenzl, A., Altenberend, F., Schultz, A. and Schultz, J. E. (2008) The properties of phosphodiesterase 11A4 GAF domains are regulated by modifications in its N-terminal domain. FEBS J. 275, 1643-1650
29. Huang, D., Hinds, T. R., Martinez, S. E., Doneanu, C. and Beavo, J. A. (2004) Molecular determinants of cGMP binding to chicken cone photoreceptor phosphodiesterase. J. Biol. Chem. 279, 48143-48151
30. Hebert, M. C., Schwede, F., Jastorff, B. and Cote, R. H. (1998) Structural features of the noncatalytic cGMP binding sites of frog photoreceptor phosphodiesterase using cGMP analogs. J. Biol. Chem. 273, 5557-5565
31. Sopory, S., Balaji, S., Srinivasan, N. and Visweswariah, S. S. (2003) Modeling and mutational analysis of the GAF domain of the cGMP-binding, cGMP-specific phosphodiesterase, PDE5. FEBS Lett. 539, 161-166
32. Yamazaki, A., Sen, I., Bitensky, M. W., Casnellie, J. E. and Greengard, P. (1980) Cyclic GMP-specific, high affinity, noncatalytic binding sites on light-activated phosphodiesterase. J. Biol. Chem. 255, 11619-11624
33. Handa, N., Mizohata, E., Kishishita, S., Toyama, M., Morita, S., Uchikubo-Kamo, T., Akasaka, R., Omori, K., Kotera, J., Terada, T. et al. (2008) Crystal structure of the GAF-B domain from human phosphodiesterase 10A complexed with its ligand, cAMP. J. Biol. Chem. 283, 19657-19664
34. Yuasa, K., Kanoh, Y., Okumura, K. and Omori, K. (2001) Genomic organization of the human phosphodiesterase PDE11A gene. Evolutionary relatedness with other PDEs containing GAF domains. Eur. J. Biochem. 268, 168-178
35. Yuasa, K., Kotera, J., Fujishige, K., Michibata, H., Sasaki, T. and Omori, K. (2000) Isolation and characterization of two novel phosphodiesterase PDE11A variants showing unique structure and tissue-specific expression. J. Biol. Chem. 275, 31469-31479
36. Zoraghi, R., Corbin, J. D. and Francis, S. H. (2004) Properties and functions of GAF domains in cyclic nucleotide phosphodiesterases and other proteins. Mol. Pharmacol. 65, 267-278.
37. Weeks, J. L., Zoraghi, R., Francis, S. H. and Corbin, J. D. (2007) N-Terminal domain of phosphodiesterase-11A4 (PDE11A4) decreases affinity of the catalytic site for substrates and tadalafil, and is involved in oligomerization. Biochemistry 46, 10353-10364