The adenylyl and guanylyl cyclase superfamily

Current Opinion in Structural Biology

Volumn 8, Issue 6, 1998, Pages 770-777

  Hurley, James H ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; DNA POLYMERASE; FORSKOLIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANYLATE CYCLASE; PYROPHOSPHATE;

ALLOSTERISM; BINDING SITE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STRUCTURE; HUMAN; METAL BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; REVIEW;

MAMMALIA;

EID: 0032425454     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(98)80097-3     Document Type: Article

References (41)

1. 1. Sunahara RK, Dessauer CW, Gilman AG: Complexity and diversity of mammalian adenylyl cyclases. Annu Rev Pharmacol Toxicol 1996, 36:461-480.
2. 2. Xia ZG, Storm DR: Calmodulin-regulated adenylyl cyclases and neuromodulation. Curr Opin Neurobiol 1997, 7:391-396.
3. 3. Houslay MD, Milligan G: Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem Sci 1997, 22:217-224.
4. 4. Cooper DMF (Ed): Adenylyl cyclases. Adv Second Messenger Phosphoprotein Res 1997, 32.
5. 5. Hanoune J, Rouille Y, Tzavara E, Shen TS, Lipskaya L, Miyamoto N, Suzuki Y, Defer N: Adenylyl cyclases: structure, regulation and function in an enzyme superfamily. Mol Cell Endocrinol 1997, 128:179-194.
6. 6. Tang WJ, Hurley JH: Catalytic mechanism and regulation of mammalian adenylyl cyclases. Mol Pharmacol 1998, 54:231-240.
7. 7. Krupinski J, Coussen F, Bakalyar H, Tang WJ, Feinstein PG, Orth K, Slaughter C, Reed RR, Gilman AG: Adenylyl cyclase amino acid sequence: possible channel or transporter-like structure. Science 1989, 244:1558-1564.
8. sα and forskolin. Science 1995, 268:1769-1772.
9. sα-and forskolin-activated enzyme in vitro. J Biol Chem 1996, 271:10941-10945.
10. 10. Whisnant RE, Gilman AG, Dessauer CW: Interaction of the two cytosolic domains of mammalian adenylyl cyclase. Proc Natl Acad Sci USA 1996, 93:6621-6625.
11. 2+ ion binding.
12. 12. Garbers DL, Lowe DG: Guanylyl cyclase receptors. J Biol Chem 1994, 269:30741-30744.
13. 13. Zhang G, Liu Y, Qin J, Vo B, Tang WJ, Ruoho AE, Hurley JH: Characterization and crystallization of a minimal catalytic core domain from mammalian type II adenylyl cyclase. Protein Sci 1997, 6:903-908.
14. 2 homodimer. The structure reveals the details of forskolin binding and suggests a mechanism for forskolin activation.
15. 15. Scholich K, Barbier AJ, Mullenix JB, Patel TB: Characterization of soluble forms of nonchimeric type V adenylyl cyclases. Proc Natl Acad Sci USA 1997, 94:2915-2920.
16. sα with the cytosolic domains of mammalian adenylyl cyclase. J Biol Chem 1997, 272:22265-22271.
17. sα activation.
18. 18. Dessauer CW, Scully TT, Gilman AG: Interactions of forskolin and ATP with the cytosolic domains of mammalian adenylyl cyclase. J Biol Chem 1997, 272:22272-22277.
19. 19. Tucker CL, Hurley JH, Miller TR, Hurley JB: Two amino acid substitutions convert a guanylyl cyclase, retGC-1, into an adenylyl cyclase. Proc Natl Acad Sci USA 1998, 95:5993-5997. A homodimeric membrane guanylyl cyclase was converted into an adenylyl cyclase by replacing the cysteine and glutamate that interact with the guanine ring of GTP with an aspartate and a lysine, as suggested by homology modeling [11•]. A third change (arginine to glutamine) leads to an unregulated ATP-specific enzyme, but regulation was rescued in a quintuple mutant incorporating two hydrophobic packing changes at the dimer interface. This suggests connections between the specificity pocket, dimer interface and regulatory mechanisms.
20. 20. Sunahara RK, Beuve A, Tesmer JJG, Sprang SR, Garbers DL, Gilman AG: Exchange of substrate and inhibitor specificities between adenylyl and guanylyl cyclases. J Biol Chem 1998, 273:16332-16338. A soluble adenylyl cyclase (AC) heterodimer was made partly GTP-specific and soluble guanylyl cyclase (GC) was completely converted into an AC using the same three mutations described in [19••], starting from the heterodimer structure [17••]. The key arginine/glutamine is provided by the AC C, domain or the GC α subunit in the heterodimers. The specificity swaps also work on adenine and guanine-containing P-site inhibitors, thereby extending the P-site inhibition concept to the GCs.
21. 21. Desaubry L, Shoshani I, Johnson RA: 2′, 5′-dideoxyadenosine 3′-polyphosphates are potent inhibitors of adenylyl cyclases. J Biol Chem 1996, 271:14028-14034.
22. 22. Dessauer CW, Gilman AG: The catalytic mechanism of mammalian adenylyl cyclase. Equilibrium binding and kinetic analysis of P-site inhibition. J Biol Chem 1997, 272:27787-27795. This paper shows that P-site inhibitors compete kinetically with cAMP in the reverse reaction and helps underpin the interpretation of the P-site inhibitor complex structure [17••].
23. 23. Artymiuk PJ, Poirrett AR, Rice DW, Willett PA: A polymerase I palm in adenylyl cyclase? Nature 1997, 388:33-34.
24. 24. Bryant SH, Madej T, Janin J, Liu Y, Ruoho AE, Zhang G, Hurley JH: A polymerase I palm in adenylyl cyclase: reply. Nature 1997, 388:34.
25. 25. Tang WJ, Stanzel M, Gilman AG: Truncation and alanine-scanning mutants of type I adenylyl cyclase. Biochemistry 1995, 34:14563-14572.
26. 26. Koch KW, Eckstein F, Stryer L: Stereochemical course of the reaction catalyzed by guanylate cyclase from bovine retinal rod outer segments. J Biol Chem 1990, 265:9659-9663.
27. 27. Garbers DL, Johnson RA: Metal and metal-ATP interaction with brain and cardiac adenylate cyclase. J Biol Chem 1975, 250:8449-8456.
28. 28. Doublie S, Tabor S, Long AM, Richardson CC, Ellenberger T: Crystal structure of bacteriophage T7 DNA polymerase complexed to a primer-template, a nucleoside triphosphate, and its processivity factor thioredoxin. Nature 1998, 391:251-258. This structure reveals in high-resolution detail how two metal ions bind to the polymerase I family palm domain. This provides the best available model of the coordination chemistry of the adenylyl cyclase (AC) catalytic complex. The same metal-nucleotide interactions were first seen in DNA polymerase β [29], although its β-sheet topology differs from both polymerase I and AC.
29. 29. Sawaya MR, Prasad R, Wilson SH, Kraut J, Pelletier H: Crystal structure of human DNA polymerase β complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry 1997, 36:11205-11215.
30. 2 domain of adenylyl cyclase were identified from genetic screens.
31. 31. Van SZ, Huang ZH, Andrews RK, Tang WJ: Conversion of forskolin-insensitive to forskolin-sensitive (mouse-type IX) adenylyl cyclase. Mol Pharmacol 1998, 53:182-187. An elegant application of protein engineering both to help identify two key determinants of forskolin sensitivity and to create a forskolin-sensitive AC9.
32. 32. Laurenza A, Sutkowski EM, Seamon KB: Forskolin: a specific stimulator of adenylyl cyclase or a diterpene with multiple sites of action? Trends Pharmacol Sci 1989, 10:442-447.
33. 33. Stone JR, Marietta MA: Synergistic activation of soluble guanylate cyclase by YC-1 and carbon monoxide: implications for the role of cleavage of the iron-histidine bond during activation by nitric oxide. Chem Biol 1998, 5:255-261.
34. sα complex [17••] and by a purely genetic approach [36].
35. sα activates adenylyl cyclase. Nat Struct Biol 1998, 5:88-92.
36. sα. J Biol Chem 1998, 273:6968-6975.
37. 37. Parent CA, Devreotes PN: Constitutively active adenylyl cyclase mutant requires neither G proteins nor cytosolic regulators. J Biol Chem 1996, 271:18333-18336.
38. 38. Chen JQ, Devivo M, Dingus J, Harry A, Li JR, Sui JL, Carty DJ, Blank JL, Exton JH, Stoffel RH et al.: A region of adenylyl Cyclase 2 critical for regulation by G-protein βγ subunits. Science 1995, 268:1166-1169.
39. 39. Vorherr T, Knopfel L, Hofmann F, Mollner S, Pfeuffer T, Carafoli E: The calmodulin binding domain of nitric oxide synthase and adenylyl cyclase. Biochemistry 1993, 32:6081-6088.
40. 40. Wu Z, Wong ST, Storm DR: Modification of the calcium and calmodulin sensitivity of the type I adenylyl cyclase by mutagenesis of its calmodulin binding domain. J Biol Chem 1993, 268:23766-23768.
41. 41. Coudart-Cavalli MP, Sismeiro O, Danchin A: Bifunctional structure of two adenylyl cyclases from the myxobacterium Stigmatella aurantiaca. Biochimie 1997, 79:757-767. The authors describe the cloning of a bacterial adenylyl cyclase (AC) that has six transmembrane segments and a single catalytic domain. It presumably functions as a homodimer of 12 transmembrane segments. It suggests a missing link in the probable evolution of the complex mammalian AC from a simpler soluble or single transmembrane homodimeric ancestor and perhaps opens a new avenue for genetic analysis of the function of the transmembrane regions.