Isoform-specific regulation of adenylyl cyclase: A potential target in future pharmacotherapy

Expert Opinion on Therapeutic Targets

Volumn 7, Issue 3, 2003, Pages 441-451

  Iwatsubo, Kousaku ^a   Tsunematsu, Takashi ^a   Ishikawa, Yoshihiro ^a,b  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Adenylyl cyclase (AC); cAMP; Forskolin; Isoform specific; P site inhibitor

Indexed keywords

2 AMINO 7 (2 FURANYL) 7,8 DEHYDRO 5(6H)QUINAZOLINE; 5,6 DEHYDROXY 7 DEACTYL 7 NICOTINOYLFORSKOLIN; 6 (3 DIMETHYLAMINOPROPIONYL)FORSKOLIN; 6 [3 (DIMETHYLAMINO)PROPIONYL] 14,15 DIHYDROFORSKOLIN; 6 [N (2 ISOTHIOCYNATOETHYL)AMINOCARBONYL]FORSKOLIN; ACETYLSALICYLIC ACID; ADENYLATE CYCLASE; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALMODULIN; CAVEOLIN; DITERPENE; ENZYME INHIBITOR; FORSKOLIN; FORSKOLIN DERIVATIVE; G PROTEIN COUPLED RECEPTOR; ISOENZYME; METOPROLOL; NEUROHORMONE; NKY 80; PROPRANOLOL; PROTEIN KINASE C; QUINAZOLINE DERIVATIVE; SILDENAFIL; UNCLASSIFIED DRUG;

DRUG SELECTIVITY; DRUG STRUCTURE; DRUG SYNTHESIS; DRUG TARGETING; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME MODIFICATION; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; HEART FAILURE; HORMONAL REGULATION; HUMAN; MOLECULAR CLONING; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; TISSUE SPECIFICITY;

ADENYLATE CYCLASE; ANIMALS; BIOLOGICAL AVAILABILITY; ENZYME INHIBITORS; FORECASTING; FORSKOLIN; HUMANS; MICE; MICE, TRANSGENIC; PROTEIN ISOFORMS; RATS;

EID: 0038717215     PISSN: 14728222     EISSN: None     Source Type: Journal    
DOI: 10.1517/14728222.7.3.441     Document Type: Review

References (96)

1. HOUSLAY MD, KOLCH W: Cell-type specific integration of cross-talk between extracellular signal-regulated kinase and cAMP signaling. Mol. Pharmacol. (2000) 58(4):659-668.
2. HANOUNE J, DEFER N: Regulation and role of adenylyl cyclase isoforms.Ann. Rev. Pharmacol. Toxicol. (2001) 41:45-174.
3. ISHIKAWA Y, HOMCY CJ: The adenylyl cyclases: as integrators of transmembrane signal transduction. Circ. Res. (1997) 80(3):297-304.
4. TANG WJ, HURLEY JH: Catalytic mechanism and regulation of mammalian adenylyl cyclases. Mol. Pharmacol. (1998) 54(2):231-240.
5. STORM DR, HANSEL C, HACKER B, PARENT A, LINDEN DJ: Impaired cerebellar long-term potentiation in Type I adenylyl cyclase mutant mice. Neuron (1998) 20(6):1199-1210.
6. WONG ST, TRINH K, HACKER B et al.: Disruption of the Type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron (2000) 27(3):487-497.
7. LEE KW, HONG JH, CHOI IY et al.: Impaired d2 dopamine receptor function in mice lacking Type 5 adenylyl cyclase. J. Neurosci. (2002) 22(18):7931-7940.
8. SCHAEFER ML, WONG ST, WOZNIAK DF et al.: Altered stress-induced anxiety in adenylyl cyclase Type VIII-deficient mice. J. Neurosci. (2000) 20(13):4809-4820.
9. HOSONO M, TAKAHIRA T, FUJITA A et al.: Cardiovascular and adenylate cyclase stimulant properties of NKH477, a novel water-soluble forskolin derivative. J. Cardiovasc. Pharmacol. (1992) 19(4):625-634.
10. SHAFIQ J, SUZUKI S, ITOH T, KURIYAMA H: Mechanisms of vasodilation induced by NKH477 a water-soluble forskolin derivative, in smooth muscle of the porcine coronary artery. Circ. Res. (1992) 71(1):70-81.
11. HIRASAWA A, AWAJIT, HOSONO M et al.: Effects of a new forskolin derivative, NKH477, on canine ventricular arrhythmia models. J. Cardiovasc. Pharmacol. (1993) 22(6):847-851.
12. MORI M, TAKEUCHI M, TAKAOKA H, HARUNO A, HASHIMOTO K: Effect of NKH477, a new water-soluble forskolin derivative, on arterial-ventricular coupling and mechanical energy transduction in patients with left ventricular systolic dysfunction: comparison with dobutamine. J. Cardiovasc. Pharmacol. (1994) 24(2):310-316.
13. SANBE A, TAKEO S: Effects of NKH477, a water-soluble forskolin derivative, on cardiac function in rats with chronic heart failure after myocardial infarction. J. Pharmacol. Exp. Ther. (1995) 274(1):120-126.
14. TESMER JJ, SUNAHARA RK, GILMAN AG, SPRANG SR: Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsα.GTPγS. Science (1997) 278(5345):1907-1916.
15. YAN SZ, HUANG ZH, RAO VD, HURLEY JH, TANG WJ: Three discrete regions of mammalian adenylyl cyclase form a site for Gsα activation. J. Biol Chem. (1997) 272(30):18849-18854.
16. ITOH H, GILMAN AG: Expression and analysis of Gsα mutants with decreased ability to activate adenylylcyclase. J. Biol. Chem. (1991) 266(24):16226-16231.
17. BERLOT CH, BOURNE HR: Identification of effector-activating residues of Gsα. Cell (1992) 68(5):911-922.
18. TANG WJ, GILMAN AG: Type-specific regulation of adenylyl cyclase by G protein βγ subunits. Science (1991) 254(5037 ):1500-1503.
19. BAYEWITCH ML, AVIDOR-REISS T, LEVY R et al.: Differential modulation of adenylyl cyclases I and II by various Gβ subunits. J. Biol. Chem. (1998) 273(4):2273-2276.
20. GAO BN, GILMAN AG: Cloning and expression of a widely distributed (Type IV) adenylyl cyclase. Proc. Natl. Acad. Sci. USA (1991) 88(22):10178-10182.
21. YOSHIMURA M, IKEDA H, TABAKOFF B: μ-Opioid receptors inhibit dopamine-stimulated activity of Type V adenylyl cyclase but enhance dopamine-stimulated activity of Type VII adenylyl cyclase. Mol. Pharmacol. (1996) 50(1):43-51.
22. BAYEWITCH ML, AVIDOR-REISS T, LEVY R et al.: Inhibition of adenylyl cyclase isoforms V and VI by various Gβγ subunits. FASEB J. (1998) 12(11):1019-1025.
23. TAUSSIG R, INIGUEZ-LLUHI JA, GILMAN AG: Inhibition of adenylyl cyclase by Giα. Science (1993) 261(5118):218-221.
24. TAUSSIG R, TANG WJ, HEPLER JR, GILMAN AG: Distinct patterns of bidirectional regulation of mammalian adenylyl cyclases. J. Biol. Chem. (1994) 269(8):6093-6100.
25. MEANS AR: Regulatory cascades involving calmodulin-dependent protein kinases. Mol. Endocrinol. (2000) 14(1):4-13.
26. KRUPINSKI J, COUSSEN F, BAKALYAR HA et al.: Adenylyl cyclase amino acid sequence: possible channelor transporter-like structure. Science (1989) 244(4912):1558-1564.
27. 2+/calmodulin-stimulated enzyme expressed in discrete regions of rat brain. J. Biol. Chem. (1994) 269(16 ):12190-12195.
28. 2+/calmodulin. J. Biol. Chem. (1996) 271(2):1089-1095.
29. 2+/calmodulin-insensitive adenylyl cyclase from rat brain. Proc. Natl. Acad. Sci. USA (1991) 88(22):10173-10177.
30. HELLEVUO K, YOSHIMURA M, MONS N, HOFFMAN PL, COOPER DN, TABAKOFF B: The characterization of a novel human adenylyl cyclase which is present in brain and other tissues. J. Biol. Chem. (1995) 270(19):11581-11589.
31. CHOI EJ, XIA Z, STORM DR: Stimulation of the Type III olfactory adenylyl cyclase by calcium and calmodulin. Biochemistry (1992) 31(28):6492-6498.
32. WEI J, WAYMAN G, STORM DR: Phosphorylation and inhibition of Type III adenylyl cyclase by calmodulin-dependent protein kinase II in vivo. J. Biol. Chem. (1996) 271(39):24231-24235.
33. (2+)-inhibitable adenylyl cyclase from NCB-20 cells. Proc. Natl. Acad. Sci. USA (1992) 89(15):6716-6720.
34. 2+/calcineurin-inhibited adenylyl cyclase, highly abundant in forebrain regions, is important for learning and memory. J. Neurosci. (1998) 18(23):9650-9661.
35. JACOBOWITZ O, CHEN J, PREMONT RT, IYENGAR R: Stimulation of specific types of Gs-stimulated adenylyl cyclases by phorbol ester treatment. J. Biol. Chem. (1993) 268(6):3829-3832.
36. JACOBOWITZ O, IYENGAR R: Phorbol ester-induced stimulation and phosphorylation of adenylyl cyclase 2. Proc. Natl. Acad. Sci. USA (1994) 91(22):10630-10634.
37. WATSON PA, KRUPINSKI J, KEMPINSKI AM, FRANKENFIELD CD: Molecular cloning and characterization of the Type VII isoform of mammalian adenylyl cyclase expressed widely in mouse tissues and in S49 mouse lymphoma cells. J. Biol. Chem. (1994) 269(46):28893-28898.
38. ZIMMERMANN G, TAUSSIG R: Protein kinase C alters the responsiveness of adenylyl cyclases to G protein α and βγ subunits. J. Biol. Chem. (1996) 271(43):27161-27166.
39. LAI HL, LIN TH, KAO YY, LIN WJ, HWANG MJ, CHEM Y: The N terminus domain of Type VI adenylyl cyclase mediates its inhibition by protein kinase C. Mol. Pharmacol. (1999) 56(3):644-650.
40. LIN TH, LAI HL, KAO YY, SUN CN, HWANG MJ, CHEM Y: Protein kinase C inhibits Type VI adenylyl cyclase by phosphorylating the regulatory N domain and two catalytic C1 and C2 domains. J. Biol. Chem. (2002) 277(18):15721-15728.
41. KAWABE J, EBINA T, ISMAIL S, KITCHEN DB, HOMCY DJ, ISHIKAWA Y: A novel peptide inhibitor of adenylyl cyclase (AC). A peptide from Type V AC directly inhibits AC catalytic activity. J. Biol. Chem. (1994) 269(40):24906-24911.
42. KAWABE J, EBINA T, TOYA Y et al.: Regulation of Type V adenylyl cyclase by PMA-sensitive and -insensitive protein kinase C isoenzymes in intact cells. FEBS Lett. (1996) 384(3):273-276.
43. IWAMI G, KAWABE J, EBINA T, CANNON PJ, HOMCY DJ, ISHIKAWA Y: Regulation of adenylyl cyclase by protein kinase A. J. Biol. Chem. (1995) 270(21):12481-12484.
44. CHEN Y, HARRY A, LI J et al.: Adenylyl cyclase 6 is selectively regulated by protein kinase A phosphorylation in a region involved in Gσ stimulation. Proc. Natl. Acad. Sci. USA (1997) 94(25):14100-14104.
45. WAYMAN GA, WEI J, WONG S, STORM DR: Regulation of Type I adenylyl cyclase by calmodulin kinase IV in vivo. Mol. Cell. Biol. (1996) 16(11):6075-6082.
46. KURZCHALIA TV, PARTON RG: Membrane microdomains and caveolae. Curr. Opin. Cell Biol. (1999) 11(4):424-431.
47. RAZANI B, LISANTI MP: Caveolin-deficient mice: insights into caveolar function human disease. J. Clin. Invest. (2001) 108(11):1553-1561.
48. SCHWENCKE C, OKUMURA S, YAMAMOTO M, GENG YJ, ISHIKAWA Y: Colocalization of β-adrenergic receptors and caveolin within the plasma membrane. J. Cell. Biochem. (1999) 75(1):64-72.
49. SCHWENCKE C, YAMAMOTO M, OKUMURA S, TOYA Y, KIM SJ, ISHIKAWA Y: Compartmentation of cyclic adenosine 3′,5′-monophosphate signaling in caveolae. Mol. Endocrinol. (1999) 13(7):1061-1070.
50. OSTROM RS, GREGORIAN C, DRENAN RM, XIANG Y, REGAN JW, INSEL PA: Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J. Biol. Chem. (2001) 276(45):42063-42069.
51. (2+) entry. J. Biol. Chem. (2002) 277(8):6025-6031.
52. TOYA Y, SCHWENCKE C, COUET J, LISANTI MP, ISHIKAWA Y: Inhibition of adenylyl cyclase by caveolin peptides. Endocrinology (1998) 139(4):2025-2031.
53. ZHEN M, HUANG X, BAMBER B, JIN Y: Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron (2000) 26(2):331-343.
54. YAN SZ, BEELER JA, CHEN Y, SHELTON RJ, WANG WJ: The regulation of Type 7 adenylyl cyclase by its C1b region and Escherichia coli peptidylprolyl isomerase, SlyD. J. Biol. Chem. (2001) 276(11):8500-8506.
55. HEPLER JR: Emerging roles for RGS proteins in cell signalling. Trends Pharmacol. Sci. (1999) 20(9):376-382.
56. SINNARAJAH S, DESSAUER CW, SRIKUMAR D et al.: RGS2 regulates signal transduction in olfactory neurons by attenuating activation of adenylyl cyclase III, Nature (2001) 409(6823):1051-1055.
57. SEAMON KB, PADGETT W, DALY JW: Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc. Natl. Acad. Sci. USA (1981) 78(6):3363-3367.
58. LINDNER E, DOHADWALLA AN, BHATTACHARYA BK: Positive inotropic and blood pressure lowering activity of a diterpene derivative isolated from Coleus forskohli: forskolin. Arzneimittelforschung (1978) 28(2):284-289.
59. BRISTOW MR, GINSBURG R, STROSBERG A, MONTGOMERY W, MINOBE W: Pharmacology and inotropic potential of forskolin in the human heart. J. Clin. Invest. (1984) 74(1):212-223.
60. TOYA Y, SCHWENCKE C, ISHIKAWA Y: Forskolin derivatives with increased selectivity for cardiac adenylyl cyclase. J. Mol. Cell. Cardiol. (1998) 30(1):97-108.
61. TOBISE K, ISHIKAWA Y, HOLMER SR et al.: Changes in Type VI adenylyl cyclase isoform expression correlate with a decreased capacity for cAMP generation in the aging ventricle. Circ. Res. (1994) 74(4):596-603.
62. ISHIKAWA Y, SOROTA S, KIUCHI K et al.: Downregulation of adenylylcyclase types V and VI mRNA levels in pacing-induced heart failure in dogs: J. Clin. Invest. (1994) 93(5):2224-2229.
63. ZHANG G, LIU Y, RUOHO AE, HURLEY JH: Structure of the adenylyl cyclase catalytic core. Nature (1997) 386(6622):247-253.
64. ONDA T, HASHIMOTO Y, NAGAI M et al.: Type-specific regulation of adenylyl cyclase. Selective pharmacological stimulation and inhibition of adenylyl cyclase isoforms. J. Biol. Chem. (2001) 276(51):47785-47793.
65. SUTKOWSKI EM, ROBBINS JD, TANG WJ, SEAMON KB: Irreversible inhibition of forskolin interactions with Type I adenylyl cyclase by a 6-isothiocyanate derivative of forskolin. Mol. Pharmacol. (1996) 50(2):299-305.
66. LONDOS C, WOLFF J: Two distinct adenosine-sensitive sites on adenylate cyclase. Proc. Natl. Acad. Sci. USA (1977) 74(12):5482-5486.
67. 2+ and adenosine sites involved in a bireactant mechanism for adenylate cyclase inhibition and their probable localization on this enzyme's catalytic component. Biochem. Biophys. Res. Commun. (1979) 90(2):513-519.
68. FLORIO VA, ROSS EM: Regulation of the catalytic component of adenylate cyclase. Potentiative interaction of stimulatory ligands and 2′,5′-dideoxyadenosine. Mol. Pharmacol. (1983) 24(2):195-202.
69. JOHNSON RA, DESAUBRY L, BIANCHI G et al.: Isozyme-dependent sensitivity of adenylyl cyclases to P-site-mediated inhibition by adenine nucleosides and nucleoside 3′-polyphosphates. J. Biol. Chem. (1997) 272(14):8962-8966.
70. 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(44):27787-27795.
71. TESMER JJ, DESSAUER CW, SUNAHARA RK et al.: Molecular basis for P-site inhibition of adenylyl cyclase. Biochemistry (2000) 39(47):14464-14471.
72. DESAUBRY L, SHOSHANI I, JOHNSON RA: 2′,5′-Dideoxyadenosine 3′-polyphosphates are potent inhibitors of adenylyl cyclases. J. Biol. Chem. (1996) 271(5):2380-2382.
73. DESAUBRY L, SHOSHANI I, JOHNSON RA: Inhibition of adenylyl cyclase by a family of newly synthesized adenine nucleoside 3′-polyphosphates. J. Biol. Chem. (1996) 271(24):14028-14034.
74. DESAUBRY L, JOHNSON RA: Adenine nucleoside 3′-tetraphosphates are novel and potent inhibitors of adenylyl cyclases. J. Biol. Chem. (1998) 273(38):24972-24977.
75. JOHNSON RA, YEUNG SM, STUBNER D, BUSHFIELD M, SHOSHANI I: Cation and structural requirements for P-site-mediated inhibition of adenylate cyclase. Mol. Pharmacol. (1989) 35(5):681-688.
76. ARTYMIUK PJ, POIRRETTE AR, RICE DW, WILLETT P: A polymerase I palm in adenylyl cyclase? Nature (1997) 388(6637):33-34.
77. HUANG H, CHOPRA R, VERDINE GL, HARRISON SC: Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science (1998) 282(5394):1669-1675.
78. ENGLUND PT, HUBERMAN JA, JOVIN TM, KORNBERG A: Enzymatic synthesis of deoxyribonucleic acid. XXX. Binding of triphosphates to deoxyribonucleic acid polymerase. J. Biol. Chem. (1969) 244(11):3038-3044.
79. IWATSUBO K, MINAMIZAWA S, TOYA Y et al.: Pharmacological inhibition of cardiac adenylyl cyclase in an isoform-specific manner. American Heart Association's Scientific Sessions in 2002 Chicago, USA (2002).
80. HANOUNE J, STENGEL D, LACOMBE ML et al.: Proteolytic activation of rat liver adenylate cyclase by a contaminant of crude collagenase from Clostridium histolyticum. J. Biol. Chem. (1977) 252(6):2039-2045.
81. LACOMBE ML, STENGEL D, HANOUNE J: Proteolytic activation of adenylate cyclase from rat-liver plasma membranes. FEBS Lett. (1977) 77(2):159-163.
82. RICHERT ND, RYAN RJ: Proteolytic enzyme activation of rat ovarian adenylate cyclase. Proc. Natl. Acad. Sci. USA (1977) 74(11):4857-4861.
83. STENGEL D, LAD PM, NIELSEN TB, RODBELL M, HANOUNE J: Proteolysis activates adenylate cyclase in rat liver and AC-lymphoma cell independently of the guanine nucleotide regulatory site. FEBS Lett. (1980) 115(2):260-264.
84. HEIDEMAN W, CASPERSON GF, BOURNE HR: Adenylyl cyclase in yeast. Hydrodynamic properties and activation by trypsin. J. Biol. Chem. (1987) 262(15):7087-7091.
85. EBINA T, TOYA Y, OKA N, KAWABE J, SCHWENCKE C, ISHIKAWA Y: Isoform-dependent activation of adenylyl cyclase by proteolysis. FEBS Lett. (1997) 401(2-3):223-226.
86. SAITO T, LEE JM, TABAKOFF B: Ethanol's effects on cortical adenylate cyclase activity. J. Neurochem. (1985) 44(4):1037-1044.
87. BODE DC, MOLINOFF PB: Effects of ethanol in vitro on the β adrenergic receptor-coupled adenylate cyclase system. J. Pharmacol. Exp. Ther. (1988) 246(3):1040-1047.
88. YOSHIMURA M, TABAKOFF B: Selective effects of ethanol on the generation of cAMP by particular members of the adenylyl cyclase family. Alcohol. Clin. Exp. Res. (1995) 19(6):1435-1440.
89. YOSHIMURA M, TABAKOFF B: Ethanol's actions on cAMP-mediated signaling in cells transfected with Type VII adenylyl cyclase. Alcohol. Clin. Exp. Res. (1999) 23(9):1457-1461.
90. NELSON EJ, HELLEVUO K, YOSHIMURA M, TABAKOFF B: Ethanol-induced phosphorylation and potentiation of the activity of Type 7 adenylyl cyclase: involvement of PKCδ. J. Biol. Chem. (2003) 278(7):4552-4560.
91. EBINA T, TOYA Y, KAWABE J, ISHIKAWA Y: Regulation of adenylyl cyclase isoforms by N-alkanols. J. Cell. Biochem. (1997) 66(4):450-456.
92. EBINA T, TOYA Y, OKA N, SCHWENCKE C, KAWABE J, ISHIKAWA Y: Isoform-specific regulation of adenylyl cyclase by oxidized catecholamines. J. Mol. Cell. Cardiol. (1997)29(4):1247-1254.
93. BOOLELL M, ALLEN MJ, BALLARD SA et al.: Sildenafil: an orally active Type 5 cyclic GMP-specific phosphodiesterase inhibitor for the treatment of penile erectile dysfunction. Int. J. Impot. Res. (1996) 8(2):47-52.
94. GOLDSTEIN I, LUE TF, PADMA-NATHAN H, ROSEN RC, STEERS WD, WICKER PA: Oral sildenafil in the treatment of erectile dysfunction. Sildenafil Study Group. N. Engl. J. Med. (1998) 338(20):1397-1404.
95. IWASE M, ISHIKAWA Y, SHEN YT et al.: Neurally mediated cardiac effects of forskolin in conscious dogs. Am. J. Physiol. (1996) 271(4 Pt 2):H1473-H1482.
96. KREEK MJ: Opiate and cocaine addictions: challenge for pharmacotherapies. Pharmacol. Biochem. Behav. (1997) 57(3):551-569.