Properties and Functions of GAF Domains in Cyclic Nucleotide Phosphodiesterases and Other Proteins

Molecular Pharmacology

Volumn 65, Issue 2, 2004, Pages 267-278

  Zoraghi, Roya ^a   Corbin, Jackie D ^a   Francis, Sharron H ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; ADENYLATE CYCLASE; CYCLIC NUCLEOTIDE; CYCLIC NUCLEOTIDE PHOSPHODIESTERASE; GAF PROTEIN; MEMBRANE PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHROMOSOME 7Q; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SHORT SURVEY;

2',3'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASES; AMINO ACID SEQUENCE; ANIMALS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEOTIDES, CYCLIC;

EID: 1642457208     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: 10.1124/mol.65.2.267     Document Type: Short Survey

References (108)

1. Akamine P, Madhusudan WJ, Xuoung NH, Ten Eyck LF, and Taylor SS (2003) Dynamic features of cAMP-dependent protein kinase revealed by apoenzyme crystal structure. J Mol Biol 327:159-171.
2. Anantharaman V, Koonin EV, and Aravind L (2001) Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains. J Mol Biol 307:1271-1292.
3. Aquirre G, Farber D, Lolley R, Fletcher RT, and Chader GJ (1978) Rod-cone dysplasia in Irish setters: a defect in cyclic GMP metabolism in visual cells. Science (Wash DC) 201:1133-1134.
4. Aravind L and Ponting CP (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22:458-459.
5. Biel M, Zong X, Ludwig A, Sautter A, and Hofmann F (1999) Structure and function of cyclic nucleotide-gated channels. Rev Physiol Biochem Pharmacol 135:151-171.
6. Boekhoff I, Michel WC, Breer H, and Ache BW (1994) Single odors differentially stimulate dual second messenger pathways in lobster olfactory receptor cells. J Neurosci 14:3304-3309.
7. Bosgraaf L, Russcher H, Snippe H, Bader S, Wind J, and Van Hasstert PJ (2002) Identification and characterization of two unusual cGMP-stimulated phoshodiesterases in Dictyostelium. Mol Biol Cell 13:3878-3889.
8. Burns F, Zhao AZ, and Beavo JA (1996) Cyclic nucleotide phosphodiesterases: gene complexity, regulation by phosphorylation and physiological implications. Adv Pharmacol 36:29-48.
9. Charbonneau H, Prusti RK, LeTrong H, Sonnenburg WK, Mullaney PJ, Walsh KA, and Beavo JA (1990) Identification of a noncatalytic cGMP-binding domain conserved in both the cGMP-stimulated and photoreceptor cyclic nucleotide phosphodiesterases. Proc Natl Acad Sci USA 87:288-292.
10. Cheung PP, Xu H, McLaughlin MM, Ghazaleh FA, Livi GP, and Colman RW (1996) Human platelet cGI-PDE: expression in yeast and localization of the catalytic domain by deletion mutagenesis. Blood 88:1321-1329.
11. Corbin JD, Blount MA, Weeks JL 2nd, Beasley A, Kuhn KP, Ho YS, Saidi LF, Hurley JH, Kotera J, and Francis SH (2003) [3H]Sildenafil binding to phosphodiesterase-5 is specific, kinetically heterogeneous and stimulated by cGMP. Mol Pharmacol 63:1364-1372.
12. Corbin JD, Turko IV, Beasley A, and Francis SH (2000) Phosphorylation of phosphodiesterase-5 by cyclic nucleotide-dependent protein kinase alters its catalytic and allosteric cGMP-binding activities. Eur J Biochem 267:2760-2767.
13. Cote RH, Bownds MD, and Arshavsky VY (1994) cGMP binding sites on photoreceptor phosphodiesterase: role in feedback regulation of visual transduction. Proc Natl Acad Sci USA 91:4845-4849.
14. D'Amours MR and Cote RH (1999) Regulation of photoreceptor phosphodiesterase catalysis by its non-catalytic cGMP-binding sites. Biochem J 340:863-869.
15. Danciger M, Blaney J, Gao YQ, Zhao DY, Heckenlively JR, Jacobson SG, and Farber DB (1995) Mutations in the PDE6B gene in autosomal recessive retinitis pigmentosa. Genomics 30:1-7.
16. Dryja TP, Rucinski DE, Chen SH, and Berson EL (1999) Frequency of mutations in the gene encoding the alpha subunit of rod cGMP-phosphodiesterase in autosomal recessive retinitis pigmentosa. Investig Ophthalmol Vis Sci 40:1859-1865.
17. Erneux C, Couchie D, Dumont JE, Baraniak J, Stec WJ, Abbad EG, 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.
18. Erneux C, Miot F, Van Haastert PJ, and Jastorff B (1985) The binding of cyclic nucleotide analogs to a purified cyclic GMP-stimulated phosphodiesterase from bovine adrenal tissue. J Cyclic Nucleotide Protein Phosphor Res 10:463-472.
19. Fawcett L, Baxendale R, Stacey P, McGrouther C, Harrow I, Soderling S, Hetman J, Beavo JA, and Phillips SC (2000) Molecular cloning and characterization of a distinct human phosphodiesterase gene family: PDE11A. Proc Natl Acad Sci USA 97:3702-3707.
20. Fink TL, Francis SH, Beasley A, Grimes KA, and Corbin JD (1999) Expression of an active, monomeric catalytic domain of the cGMP-binding cGMP-specific phosphodiesterase (PDE5). J Biol Chem 274:34613-34620.
21. Francis SH, Bessay EP, Kotera J, Grimes KA, Liu L, Thompson WJ, and Corbin JD (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.
22. Francis SH, Chu DM, Thomas MK, Beasley A, Grimes K, Busch JL, Turko IV, Haik TL, and Corbin JD (1998) Ligand-induced conformational changes in cyclic nucleotide phosphodiesterases and cyclic nucleotide-dependent protein kinases. Methods 14:81-92.
23. Francis SH and Corbin JD (1999) Cyclic nucleotide-dependent protein kinases: intracellular receptors for cAMP and cGMP action. Crit Rev Clin Lab Sci 36:275-328.
24. Francis SH, Lincoln TM, Corbin JD (1980) Characterization of a novel cGMP binding protein from rat lung. J Biol Chem 255:620-626.
25. Francis SH, Thomas MK, and Corbin JD (1990) Cyclic GMP-specific phosphodiesterase from lung, in Cyclic Nucleotide Phosphodiesterases: Structure Regulation and Drug Action (Beavo J and Houslay MD eds) pp 117-140, Wiley, Chichester, New York.
26. Francis SH, Turko IV, and Corbin JD (2001) Cyclic nucleotide phosphodiesterases: relating structure and function. Progr Nucleic Acid Res Mol Biol 65:1-52.
27. 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.
28. Gal A, Orth U, Baehr W, Schwinger E, and Rosenberg T (1994) Heterozygous missense mutation in the rod cGMP phosphodiesterase beta-subunit gene in autosomal dominant stationary night blindness [erratum appears in Nat Genet 1994;7:551]. Nat Genet 7:64-68.
29. Gal A, Orth U, Baehr W, Schwinger E, and Rosenberg T (1994) Heterozygous missense mutation in the rod cGMP phosphodiesterase beta-subunit gene in autosomal dominant stationary night blindness [erratum appears in Nat Genet 1994;7:551]. Nat Genet 7:64-68.
30. Galperin MY, Nikolskaya AN, and Koonin EV (2001) Novel domains of the prokaryotic two-component signal transduction systems [erratum appears in FEMS Microbiol Lett 2001;204:213-214]. FEMS Microbiol Lett 203:11-21.
31. Galperin MY, Nikolskaya AN, and Koonin EV (2001) Novel domains of the prokaryotic two-component signal transduction systems [erratum appears in FEMS Microbiol Lett 2001;204:213-214]. FEMS Microbiol Lett 203:11-21.
32. Gillespie PG and Beavo JA (1988) Characterization of a bovine cone photoreceptor phosphodiesterase purified by cyclic GMP-sepharose chromatography. J Biol Chem 263:8133-8141.
33. Gillespie PG and Beavo JA (1989) cGMP is tightly bound to bovine retinal rod phosphodiesterase. Proc Natl Acad Sci USA 86:4311-4315.
34. Giltay R, Kostka G, and Timpl R (1997) Sequence and expression of a novel member (LTBP-4) of the family of latent transforming growth factor-beta binding proteins. FEBS Lett 411:164-168.
35. Granovsky AE, Natochin M, McEntaffer RL, Haik TL, Francis SH, Corbin JD, and Artemyev NO (1998) Probing domain functions of chimeric PDE6alpha′ /PDE5 cGMP-phosphodiesterase. J Biol Chem 273:24485-24490.
36. Hebert MC, Schwede F, Jastorff B, and Cote RH (1998) Structural features of the noncatalytic cGMP binding sites of frog photoreceptor phosphodiesterase using cGMP analogs. J Biol Chem 273:5557-5565.
37. Ho YS, Burden LM, and Hurley JH (2000) Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor [erratum appears in EMBO (Eur Mol Biol Organ) J 2001;20:1483]. EMBO (Eur Mol Biol Organ) J 19:5288-5299.
38. Ho YS, Burden LM, and Hurley JH (2000) Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor [erratum appears in EMBO (Eur Mol Biol Organ) J 2001;20:1483]. EMBO (Eur Mol Biol Organ) J 19:5288-5299.
39. Hopper S, Korsa I, and Bock A (1996) The nucleotide concentration determines the specificity of in vitro transcription activation by the sigma 54-dependent activator FhlA. J Bacteriol 178:199-203.
40. Hurley JH (2003) GAF domains: cyclic nucleotides come full circle. Sci STKE 164: PE1.
41. Jacobitz S, McLaughlin MM, Livi GP, Burman M, and Torphy TJ (1996) Mapping the functional domains of human recombinant phosphodiesterase 4A: structural requirements for catalytic activity and rolipram binding. Mol Pharmacol 50:891-899.
42. Joerger RD, Jacobson MR, and Bishop PE (1989) Two nifA-like genes required for expression of alternative nitrogenases by Azotobacter vinelandii. J Bacteriol 171: 3258-3267.
43. Juilfs DM, Fulle HJ, Zhao AZ, Houslay MD, Garbers DL, and Beavo JA (1997) A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway. Proc Natl Acad Sci USA 94:3388-3395.
44. Kader A, Frazzini VI, Solomon RA, and Trifiletti RR (1993) Nitric oxide production during focal cerebral ischemia in rats. Stroke 24:1709-1716.
45. Kajimura N, Yamazaki M, Morikawa K, Yamazaki A, and Mayanagi K (2002) Three-dimensional structure of non-activated cGMP phosphodiesterase 6 and comparison of its image with those of activated forms. J Struct Biol 139:27-38.
46. Kameni Tcheudji JF, Lebeau L, Virmaux N, Maftei CG, Cote RH, Lugnier C, and Schultz P (2001) Molecular organization of bovine rod cGMP-phosphodiesterase 6. J Mol Biol 310:781-791.
47. Kanacher T, Schultz A, Linder JU, and Schultz JE (2002) A GAF-domain-regulated adenylyl cyclase from Anabaena is a self-activating cAMP switch. EMBO (Eur Mol Biol Organ) J 21:3672-3680.
48. Kaneko T, Nakamura Y, Wolk CP, Kuritz T, Sasamoto S, Watanabe A, Iriguchi M, Ishikawa A, Kawashima K, Kimura T, et al. (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:205-213, 227-253.
49. Korsa I and Bock A (1997) Characterization of fhlA mutations resulting in ligand-independent transcriptional activation and ATP hydrolysis. J Bacteriol 179:41-45.
50. Kotera J, Fujishige K, Yuasa K, and Omori K (1999) Characterization and phosphorylation of PDE10A2, a novel alternative splice variant of human phosphodiesterase that hydrolyzes cAMP and cGMP. Biochem Biophys Res Commun 261:551-557.
51. Koyanagi M, Suga H, Hoshiyama D, Ono K, Iwabe N, Kuma K, and Miyata T (1998) Ancient gene duplication and domain shuffling in the animal cyclic nucleotide phosphodiesterase family. FEBS Lett 436:323-328.
52. Letunic I, Goodstadt L, Dickens NJ, Doerks T, Schultz J, Mott R, Ciccarelli F, Copley RR, Ponting CP, and Bork P (2002) Recent improvements to the SMART domain-based sequence annotation resource. Nucleic Acids Res 30:242-244.
53. Little R and Dixon R (2003) The amino-terminal GAF domain of azotobacter vinelandii NifA binds 2-oxoglutarate to resist inhibition by NifL under nitrogen-limiting conditions. J Biol Chem 278:28711-28718.
54. Lincoln TM, Hall CL, Park CR, Corbin JD (1976) Guanosine 3′:5′-cyclic monophosphate binding proteins in rat tissues. Proc Natl Acad Sci USA 73:2559-2563.
55. Liu L, Underwood T, Li H, Pamukcu R, and Thompson WJ (2002) Specific cGMP binding by the cGMP binding domains of cGMP-binding cGMP specific phosphodiesterase. Cell Signal 14:45-51.
56. Lolley RN, Farber DB, Rayborn ME, and Hollyfield JG (1977) Cyclic GMP accumulation causes degeneration of photoreceptor cells: simulation of an inherited disease. Science (Wash DC) 196:664-666.
57. MacFarland RT, Zelus BD, and Beavo JA (1991) High concentrations of a cGMP-stimulated phosphodiesterase mediate ANP-induced decreases in cAMP and steroidogenesis in adrenal glomerulosa cells. J Biol Chem 266:136-142.
58. Manganiello VC, Tanaka T, and Murashima S (1990) Cyclic GMP-stimulated cyclic nucleotide phosphodiesterases, in Cyclic Nucleotide Phosphodiesterases: Structure Regulation and Drug Action (Beavo J and Houslay MD eds) pp 61-85, Wiley, Chichester, New York.
59. Martinez SE, Beavo JA, and Hol WG (2002a) GAF domains: two billion year old molecular switches that bind cyclic nucleotides. Mol Intervent 2:317-323.
60. Martinez SE, Wu AY, Glavas NA, Tang XB, Turley S, Hol WG, and Beavo JA (2002b) The two GAF domains in phosphodiesterase 2A have distinct roles in dimerization and in cGMP binding. Proc Natl Acad Sci USA 99:13260-13265.
61. Martins TJ, Mumby MC, and Beavo JA (1982) Purification and characterization of a cyclic GMP-stimulated cyclic nucleotide phosphodiesterase from bovine tissues. J Biol Chem 257:1973-1979.
62. McAllister-Lucas LM, Haik TL, Colbran JL, Sonnenburg WK, Seger D, Turko IV, Beavo JA, Francis SH, and Corbin JD (1995) An essential aspartic acid at each of two allosteric cGMP-binding sites of a cGMP-specific phosphodiesterase. J Biol Chem 270:30671-30679.
63. McKay DB and Steitz TA (1981) Structure of catabolite gene activator protein at 2.9 A resolution suggests binding to left-handed B-DNA. Nature (Lond) 290:744-749.
64. McLaughlin ME, Ehrhart TL, Berson EL, and Dryja TP (1995) Mutation spectrum of the gene encoding the beta subunit of rod phosphodiesterase among patients with autosomal recessive retinitis pigmentosa. Proc Natl Acad Sci USA 92:3249-3253.
65. Montgomery BL and Lagarias JC (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci 7:357-366.
66. Moss J, Manganiello VC, and Vaughan M (1977) Substrate and effector specificity of a guanosine 3′:5′-monophosphate phosphodiesterase from rat liver. J Biol Chem 252:5211-5215.
67. Mou H and Cote RH (2001) The catalytic and GAF domains of the rod cGMP phosphodiesterase (PDE6) heterodimer are regulated by distinct regions of its inhibitory gamma subunit. J Biol Chem 276:27527-27534.
68. Mou H, Grazio HJ 3rd, Cook TA, Beavo JA, and Cote RH (1999) cGMP binding to noncatalytic sites on mammalian rod photoreceptor phosphodiesterase is regulated by binding of its gamma and delta subunits. J Biol Chem 274:18813-18820.
69. Mullershausen F, Friebe A, Feil R, Thompson WJ, Hofmann F, and Koesling D (2003) Direct activation of PDE5 by cGMP: long-term effects within NO/cGMP signaling. J Cell Biol 160:719-727.
70. Muradov KG, Boyd KK, Martinez SE, Beavo JA, and Artemyev NO (2003a) The GAFa domains of rod cGMP-phosphodiesterase 6 determine the selectivity of the enzyme dimerization. J Biol Chem 278:10594-601.
71. Muradov KG, Granovsky AE, and Artemyev NO (2003b) Mutation in rod PDE6 linked to congenital stationary night blindness impairs the enzyme inhibition by its gamma-subunit. Biochemistry 42:3305-3310.
72. Muradov KG, Granovsky AE, Schey KL, and Artemyev NO (2002) Direct interaction of the inhibitory gamma-subunit of rod cGMP phosphodiesterase (PDE6) with the PDE6 GAFa domains. Biochemistry 41:3884-3890.
73. Okada D and Asakawa S (2002) Allosteric activation of cGMP-specific, cGMP-binding phosphodiesterase (PDE5) by cGMP. Biochemistry 41:9672-9679.
74. Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, Nikaido I, Osato N, Saito R, Suzuki H, et al. (2002) Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature (Lond) 420:563-573.
75. Pai EF, Kabsch W, Krengel U, Holmes KC, John J, and Wittinghofer A (1989) Structure of the guanine-nucleotide-binding domain of the Ha-ras oncogene product p21 in the triphosphate conformation. Nature (Lond) 341:209-214.
76. Passner JM, Schultz SC, and Steitz TA (2000) Modeling the cAMP-induced allosteric transition using the crystal structure of CAP-cAMP at 2.1 A resolution. J Mol Biol 304:847-859.
77. Pfeifer A, Ruth P, Dostmann W, Sausbier M, Klatt P, and Hofmann F (1999) Structure and function of cGMP-dependent protein kinases. Rev Physiol Biochem Pharmacol 135:105-149.
78. Rascon A, Soderling SH, Schaefer JB, and Beavo JA (2002) Cloning and characterization of a cAMP-specific phosphodiesterase (TbPDE2B) from Trypanosoma brucei. Proc Natl Acad Sci USA 99:4714-4719.
79. Reyes-Ramirez F, Little R, and Dixon R (2002) Mutant forms of the Azotobacter vinelandii transcriptional activator NifA resistant to inhibition by the NifL regulatory protein. J Bacteriol 184:6777-6785.
80. Richter W (2002) 3′,5′Cyclic nucleotide phosphodiesterases class III: members, structure and catalytic mechanism. Proteins 46:278-286.
81. Richter W and Conti M (2002) Dimerization of the type 4 cAMP-specific phosphodiesterases is mediated by the upstream conserved regions (UCRs). J Biol Chem 277:40212-40221.
82. Rybalkin SD and Beavo JA (1996) Multiplicity within cyclic nucleotide phosphodiesterases. Biochem Soc Trans 24:1005-1009.
83. Rybalkin SD, Rybalkina IG, Shimizu-Albergine M, Tang XB, and Beavo JA (2003) PDE5 is converted to an activated state upon cGMP binding to the GAF A domain. EMBO (Eur Mol Biol Organ) J 22:469-478.
84. Sato-Nara K, Yuhashi KI, Higashi K, Hosoya K, Kubota M, and Ezura H (1999) Stage- and tissue-specific expression of ethylene receptor homolog genes during fruit development in muskmelon. Plant Physiol 120:321-330.
85. Schluter K, Jockusch BM, and Rothkegel M (1997) Profilins as regulators of actin dynamics. Biochim Biophys Acta 1359:97-109.
86. Schultz J, Milpetz F, Bork P, and Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857-5864.
87. Sebkhi A, Strange JW, Phillips SC, Wharton J, and Wilkins MR (2003) Phosphodiesterase type 5 as a target for the treatment of hypoxia-induced pulmonary hypertension. Circulation 107:3230-3235.
88. Seebeck T, Gong K, Kunz S, Schaub R, Shalaby T, and Zoraghi R (2001) cAMP signalling in Trypanosoma brucei. Int J Parasitol 31:491-498.
89. Shabb JB and Corbin JD (1992) Cyclic nucleotide-binding domains in proteins having diverse functions. J Biol Chem 267:5723-5726.
90. Sharrock RA and Quail PH (1989) Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution and differential expression of a plant regulatory photoreceptor family. Genes Dev 3:1745-1757.
91. Skiba NP, Artemyev NO, and Hamm HE (1995) The carboxyl terminus of the gamma-subunit of rod cGMP phosphodiesterase contains distinct sites of interaction with the enzyme catalytic subunits and the alpha-subunit of transducin. J Biol Chem 270:13210-13215.
92. Soderling SH, Bayuga SJ, and Beavo JA (1999) Isolation and characterization of a dual-substrate phosphodiesterase gene family: PDE10A. Proc Natl Acad Sci USA 96:7071-7076.
93. Sopory S, Balaji S, Srinivasan N, and Visweswariah SS (2003) Modeling and mutational analysis of the GAF domain of the cGMP-binding, cGMP-specific phosphodiesterase, PDE5. FEBS Lett 539:161-166.
94. Stroop SD and Beavo JA (1992) Sequence homology and structure-function studies of the bovine cyclic-GMP-stimulated and retinal phosphodiesterases. Adv Second Messenger Phosphoprotein Res 25:55-71.
95. Su Y, Dostmann WR, Herberg FW, Durick K, Xuong NH, Ten Eyck L, Taylor SS, and Varughese KI (1995) Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains. Science (Wash DC) 269:807-813.
96. Thomas MK, Francis SH, Beebe SJ, Gettys TW, and Corbin JD (1992) Partial mapping of cyclic nucleotide sites and studies of regulatory mechanisms of phosphodiesterases using cyclic nucleotide analogues. Adv Second Messenger Phosphoprotein Res 25:45-53.
97. Thomas MK, Francis SH, and Corbin JD (1990a) Characterization of a purified bovine lung cGMP-binding cGMP phosphodiesterase. J Biol Chem 265:14964-14970.
98. Thomas MK, Francis SH, and Corbin JD (1990b) Substrate- and kinase-directed regulation of phosphorylation of a cGMP-binding phosphodiesterase by cGMP. J Biol Chem 265:14971-14978.
99. Tsang SH, Gouras P, Yamashita CK, Kjeldbye H, Fisher J, Farber DB, and Goff SP (1996) Retinal degeneration in mice lacking the gamma subunit of the rod cGMP phosphodiesterase. Science (Wash DC) 272:1026-1029.
100. Turko IV, Francis SH, and Corbin JD (1998) Binding of cGMP to both allosteric sites of cGMP-binding cGMP-specific phosphodiesterase (PDE5) is required for its phosphorylation. Biochem J 329:505-510.
101. Turko IV, Haik TL, McAllister-Lucas LM, Burns F, Francis SH, and Corbin JD (1996) Identification of key amino acids in a conserved cGMP-binding site of cGMP-binding phosphodiesterases. A putative NKXnD motif for cGMP binding. J Biol Chem 271:22240-22244.
102. Urao T, Yamaguchi-Shinozaki K, and Shinozaki K (2001) Plant histidine kinases: an emerging picture of two-component signal transduction in hormone and environmental responses. Science STKE 2001:RE18.
103. Weber G (1975) Energetics of ligand binding to proteins. Adv Protein Chem 29:1-83.
104. Wyatt TA, Naftilan AJ, Francis SH, and Corbin JD (1998) ANF elicits phosphorylation of the cGMP phosphodiesterase in vascular smooth muscle cells. Am J Physiol 274:H448-H455.
105. 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 265:168-178.
106. 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.
107. Zhang R, Wang Y, Zhang L, Zhang Z, Tsang W, Lu M, and Chopp M (2002) Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 33:2675-2680.
108. Zoraghi R and Seebeck T (2002) The cAMP-specific phosphodiesterase TbPDE2C is an essential enzyme in bloodstream from Trypanosoma brucei. Proc Natl Acad Sci USA 99:4343-4348.