Pharmacological distinction between soluble and transmembrane adenylyl cyclases

Journal of Pharmacology and Experimental Therapeutics

Volumn 347, Issue 3, 2013, Pages 589-598

  Bitterman, Jacob L ^a   Ramos Espiritu, Lavoisier ^a   Diaz, Ana ^a   Levin, Lonny R ^a   Buck, Jochen ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (1H BENZO[D]IMIDAZOL 2 YLTHIO) N' (5 BROMO 2 HYDROXYBENZYLIDENE)PROPANEHYDRAZIDE; 2 AMINO 7 (2 FURANYL) 7,8 DIHYDRO 5(6H) QUINAZOLINE; 2 HYDROXYESTRADIOL; 2',5' DIDEOXYADENOSINE; 3' TRIPHOSPHATE 3' TRIPHOSPHATE; 4 HYDROXYESTRADIOL; 9 (TETRAHYDRO 2 FURYL)ADENINE; ADENYLATE CYCLASE; ADENYLATE CYCLASE INHIBITOR; CALCIUM ION; GUANINE NUCLEOTIDE BINDING PROTEIN; KH 7; N (2 PHENYLCYCLOPENTYL)AZACYCLOTRIDECAN 2 IMINE; UNCLASSIFIED DRUG; VIDARABINE;

ARTICLE; CONTROLLED STUDY; DRUG POTENCY; DRUG SPECIFICITY; EMBRYO; ENZYME REGULATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FAMILY; SIGNAL TRANSDUCTION;

ADENYLATE CYCLASE; CELLS, CULTURED; CYCLIC AMP; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; SUBSTRATE SPECIFICITY;

EID: 84887845806     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.113.208496     Document Type: Article

References (74)

1. Abdel-Majid R.M., Leong WL, Schalkwyk L.C., Smallman DS, Wong ST, Storm DR, Fine A, Dobson M.J., Guernsey DL, and Neumann PE (1998) Loss of adenylyl cyclase I activity disrupts patterning of mouse somatosensory cortex. Nat Genet 19: 289-291. (Pubitemid 28309346)
2. Acin-Perez R., Salazar E, Kamenetsky M., Buck J, Levin LR, and Manfredi G (2009) Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab 9:265-276.
3. Braeunig JH, Schweda F, Han P-L, and Seifert R (2013) Similarly potent inhibition of adenylyl cyclase by P-site inhibitors in hearts from wild type and AC5 knockout mice. PLoS ONE 8:e68009.
4. Braun T and Dods RF (1975) Development of a Mn-2+-sensitive, "soluble" adenylate cyclase in rat testis. Proc Natl Acad Sci USA 72:1097-1101.
5. Buck J, Sinclair ML, Schapal L, Cann M.J., and Levin LR (1999) Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc Natl Acad Sci USA 96:79-84. (Pubitemid 29036056)
6. Bundey RA and Insel PA (2004) Discrete intracellular signaling domains of soluble adenylyl cyclase: camps of cAMP? Sci STKE 2004:pe19.
7. Buxton IL and Brunton LL (1983) Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes. J Biol Chem 258:10233-10239. (Pubitemid 14241179)
8. Calebiro D, Nikolaev VO, Gagliani M.C., de Filippis T, Dees C, Tacchetti C., Persani L, and Lohse MJ (2009) Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol 7:e1000172.
9. Chen J, Martinez J, Milner T.A., Buck J., and Levin LR (2013) Neuronal expression of soluble adenylyl cyclase in the mammalian brain. Brain Res 1518:1-8.
10. Chen Y, Cann MJ, Litvin T.N., Iourgenko V., Sinclair ML, Levin LR, and Buck J (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289:625-628. (Pubitemid 30622067)
11. Chien CL, Wu YS, Lai H.L., Chen YH, Jiang ST, Shih CM, Lin S.S., Chang C., and Chern Y (2010) Impaired water reabsorption in mice deficient in the type VI adenylyl cyclase (AC6). FEBS Lett 584:2883-2890.
12. Choi HB, Gordon GR, Zhou N, Tai C., Rungta RL, Martinez J, Milner TA, Ryu J.K., McLarnon JG, and Tresguerres M, et al (2012) Metabolic communication between astrocytes and neurons via bicarbonate-responsive soluble adenylyl cyclase. Neuron 75:1094-1104.
13. Corredor RG, Trakhtenberg EF, Pita-Thomas W, Jin X., Hu Y, and Goldberg JL (2012) Soluble adenylyl cyclase activity is necessary for retinal ganglion cell survival and axon growth. J Neurosci 32:7734-7744.
14. 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.
15. Désaubry L., Shoshani I, and Johnson RA (1996a) 2',5'-Dideoxyadenosine 3'-poly-phosphates are potent inhibitors of adenylyl cyclases. J Biol Chem 271:2380-2382.
16. Désaubry L., Shoshani I, and Johnson RA (1996b) Inhibition of adenylyl cyclase by a family of newly synthesized adenine nucleoside 3'-polyphosphates. J Biol Chem 271:14028-14034.
17. Dessauer CW (2009) Adenylyl cyclase: A-kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol Pharmacol 76:935-941.
18. Dessauer CW and Gilman AG (1997) The catalytic mechanism of mammalian adenylyl cyclase: equilibrium binding and kinetic analysis of P-site inhibition. J Biol Chem 272:27787-27795. (Pubitemid 27473578)
19. 2+ uptake induces cyclic AMP generation in the matrix and modulates organelle ATP levels. Cell Metab 17:965-975.
20. Dunn TA, Storm DR, and Feller MB (2009) Calcium-dependent increases in protein kinase-A activity in mouse retinal ganglion cells are mediated by multiple adenylate cyclases. PLoS ONE 4:e7877.
21. Emery AC, Eiden MV, and Eiden LE (2013) A new site and mechanism of action for the widely used adenylate cyclase inhibitor SQ22, 536. Mol Pharmacol 83: 95-105.
22. Esposito G, Jaiswal BS, Xie F, Krajnc-Franken MA, Robben T.J., Strik AM, Kuil C, Philipsen RL, van Duin M, and Conti M, et al. (2004) Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc Natl Acad Sci USA 101:2993-2998. (Pubitemid 38332002)
23. Ferrandon S, Feinstein TN, Castro M, Wang B., Bouley R, Potts JT, Gardella T.J., and Vilardaga JP (2009) Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat Chem Biol 5:734-742.
24. Forte LR, Bylund DB, and Zahler WL (1983) Forskolin does not activate sperm adenylate cyclase. Mol Pharmacol 24:42-47. (Pubitemid 13075103)
25. Gadea A, López E, and López-Colomé AM (1999) The adenylate cyclase inhibitor MDL-12330Ahas a non-specific effect on glycine transport in Müller cells from the retina. Brain Res 838:200-204. (Pubitemid 29389835)
26. Geng W, Wang Z, Zhang J., Reed BY, Pak CY, and Moe OW (2005) Cloning and characterization of the human soluble adenylyl cyclase. Am J Physiol Cell Physiol 288:C1305-C1316. (Pubitemid 40991068)
27. Gille A, Lushington GH, Mou T.C., Doughty MB, Johnson RA, and Seifert R (2004) Differential inhibition of adenylyl cyclase isoforms and soluble guanylyl cyclase by purine and pyrimidine nucleotides. J Biol Chem 279:19955-19969. (Pubitemid 38623438)
28. Grupp G, Grupp IL, Johnson C.L., Matlib MA, Rouslin W, Schwartz A, Wallick E.T., Wang T., and Wisler P (1980) Effects of RMI 12330A, a new inhibitor of adenylate cyclase on myocardial function and subcellular activity. Br J Pharmacol 70: 429-442. (Pubitemid 11241414)
29. Halm ST, Zhang J, and Halm DR (2010) Beta-adrenergic activation of electrogenic K+ and Cl-secretion in guinea pig distal colonic epithelium proceeds via separate cAMP signaling pathways. Am J Physiol Gastrointest Liver Physiol 299:G81-G95.
30. Hayes JS and Brunton LL (1982) Functional compartments in cyclic nucleotide action. J Cyclic Nucleotide Res 8:1-16. (Pubitemid 12047342)
31. Hayes JS, Brunton LL, and Mayer SE (1980) Selective activation of particulate cAMP-dependent protein kinase by isoproterenol and prostaglandin E1. J Biol Chem 255:5113-5119. (Pubitemid 10015830)
32. Hess KC, Jones BH, Marquez B, Chen Y., Ord TS, Kamenetsky M, Miyamoto C, Zippin J.H., Kopf GS, and Suarez SS, et al (2005) The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Dev Cell 9: 249-259. (Pubitemid 41051743)
33. Hollenhorst MI, Lips KS, Kummer W, and Fronius M (2012) Nicotine-induced activation of soluble adenylyl cyclase participates in ion transport regulation in mouse tracheal epithelium. Life Sci 91:1009-1012.
34. Houslay MD (2010) Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem Sci 35:91-100.
35. Iwatsubo K, Minamisawa S, Tsunematsu T., Nakagome M, Toya Y, Tomlinson J.E., Umemura S., Scarborough RM, Levy DE, and Ishikawa Y (2004) Direct inhibition of type 5 adenylyl cyclase prevents myocardial apoptosis without functional deterioration. J Biol Chem 279:40938-40945. (Pubitemid 39287693)
36. Iwatsubo K, Tsunematsu T, and Ishikawa Y (2003) Isoform-specific regulation of adenylyl cyclase: a potential target in future pharmacotherapy. Expert Opin Ther Targets 7:441-451. (Pubitemid 36722228)
37. Jaiswal BS and Conti M (2001) Identification and functional analysis of splice variants of the germ cell soluble adenylyl cyclase. J Biol Chem 276:31698-31708.
38. Jaiswal BS and Conti M (2003) Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa. Proc Natl Acad Sci USA 100:10676-10681. (Pubitemid 37140087)
39. Johnson RA, Désaubry L, Bianchi G., Shoshani I, Lyons E, Jr, Taussig R, Watson PA, Cali JJ, Krupinski J, and Pieroni JP, et al. (1997) Isozyme-dependent sensitivity of adenylyl cyclases to P-site-mediated inhibition by adenine nucleosides and nucleoside 3'-polyphosphates. J Biol Chem 272:8962-8966. (Pubitemid 27154894)
40. Kamenetsky M, Middelhaufe S, Bank E.M., Levin LR, Buck J, and Steegborn C (2006) Molecular details of cAMP generation in mammalian cells: a tale of two systems. J Mol Biol 362:623-639. (Pubitemid 44332423)
41. Lee YS, Tresguerres M, Hess K., Marmorstein LY, Levin LR, Buck J, and Marmorstein AD (2011) Regulation of anterior chamber drainage by bicarbonate-sensitive soluble adenylyl cyclase in the ciliary body. J Biol Chem 286: 41353-41358.
42. Lefkimmiatis K, Leronni D, and Hofer AM (2013) Distinct cAMP/PKA signaling dynamics visualized in the inner and outer compartments of mitochondria. J Cell Biol 202:453-462.
43. Litvin TN, Kamenetsky M, Zarifyan A., Buck J, and Levin LR (2003) Kinetic properties of "soluble" adenylyl cyclase. Synergism between calcium and bicarbonate. J Biol Chem 278:15922-15926. (Pubitemid 36799709)
44. Onda T, Hashimoto Y, Nagai M., Kuramochi H, Saito S, Yamazaki H., Toya Y, Sakai I, Homcy C.J., and Nishikawa K, et al. (2001) Type-specific regulation of adenylyl cyclase. Selective pharmacological stimulation and inhibition of adenylyl cyclase isoforms. J Biol Chem 276:47785-47793.
45. Pastor-Soler N., Beaulieu V, Litvin T.N., Da Silva N, Chen Y, Brown D., Buck J, Levin LR, and Breton S (2003) Bicarbonate-regulated adenylyl cyclase (sAC) is a sensor that regulates pH-dependent V-ATPase recycling. J Biol Chem 278: 49523-49529.
46. Patel TB, Du Z, Pierre S., Cartin L, and Scholich K (2001) Molecular biological approaches to unravel adenylyl cyclase signaling and function. Gene 269:13-25. (Pubitemid 32488902)
47. Rall TW and Sutherland EW (1958) Formation of a cyclic adenine ribonucleotide by tissue particles. J Biol Chem 232:1065-1076.
48. Ramos LS, Zippin JH, Kamenetsky M, Buck J., and Levin LR (2008) Glucose and GLP-1 stimulate cAMP production via distinct adenylyl cyclases in INS-1E insulinoma cells. J Gen Physiol 132:329-338.
49. Rich TC, Fagan KA, Nakata H, Schaack J., Cooper DM, and Karpen JW (2000) Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J Gen Physiol 116:147-161. (Pubitemid 30637001)
50. Rusinova R, Herold KF, Sanford R.L., Greathouse DV, Hemmings HC, Jr, and Andersen OS (2011) Thiazolidinedione insulin sensitizers alter lipid bilayer properties and voltage-dependent sodium channel function: implications for drug discovery. J Gen Physiol 138:249-270.
51. Sadana R and Dessauer CW (2009) Physiological roles for G protein-regulated adenylyl cyclase isoforms: insights from knockout and overexpression studies. Neu-rosignals 17:5-22.
52. Salomon Y (1979) Adenylate cyclase assay. Adv Cyclic Nucleotide Res 10:35-55.
53. Sample V, DiPilato LM, Yang J.H., Ni Q., Saucerman JJ, and Zhang J (2012) Regulation of nuclear PKA revealed by spatiotemporal manipulation of cyclic AMP. Nat Chem Biol 8:375-382.
54. Seifert R, Lushington GH, Mou T.C., Gille A., and Sprang SR (2012) Inhibitors of membranous adenylyl cyclases. Trends Pharmacol Sci 33:64-78.
55. Steegborn C, Litvin TN, Hess K.C., Capper AB, Taussig R, Buck J, Levin L.R., and Wu H (2005) A novel mechanism for adenylyl cyclase inhibition from the crystal structure of its complex with catechol estrogen. J Biol Chem 280:31754-31759. (Pubitemid 41291924)
56. Stessin AM, Zippin JH, Kamenetsky M, Hess K.C., Buck J., and Levin LR (2006) Soluble adenylyl cyclase mediates nerve growth factor-induced activation of Rap1. J Biol Chem 281:17253-17258.
57. Storm DR, Hansel C, Hacker B., Parent A, and Linden DJ (1998) Impaired cerebellar long-term potentiation in type I adenylyl cyclase mutant mice. Neuron 20: 1199-1210. (Pubitemid 28293136)
58. Strazzabosco M, Fiorotto R, Melero S., Glaser S, Francis H, Spirli C., and Alpini G (2009) Differentially expressed adenylyl cyclase isoforms mediate secretory functions in cholangiocyte subpopulation. Hepatology 50:244-252.
59. Sutherland EW and Rall TW (1958) Fractionation and characterization of a cyclic adenine ribonucleotide formed by tissue particles. J Biol Chem 232: 1077-1091.
60. Tesmer JJ, Dessauer CW, Sunahara R.K., Murray LD, Johnson RA, Gilman AG, and Sprang SR (2000) Molecular basis for P-site inhibition of adenylyl cyclase. Biochemistry 39:14464-14471.
61. Tian G, Sandler S, Gylfe E., and Tengholm A (2011) Glucose- and hormone-induced cAMP oscillations in a- and b-cells within intact pancreatic islets. Diabetes 60: 1535-1543.
62. Tresguerres M, Buck J and Levin LR (2010) Physiological carbon dioxide, bicarbonate, and pH sensing. Pflugers Arch European J Physiol 460:953-964.
63. Tresguerres M, Levin LR, and Buck J (2011) Intracellular cAMP signaling by soluble adenylyl cyclase. Kidney Int 79:1277-1288.
64. Wachten S, Masada N, Ayling L.J., Ciruela A., Nikolaev VO, Lohse MJ, and Cooper DM (2010) Distinct pools of cAMP centre on different isoforms of adenylyl cyclase in pituitary-derived GH3B6 cells. J Cell Sci 123:95-106.
65. Willoughby D, Wachten S, Masada N., and Cooper DM (2010) Direct demonstration of discrete Ca2+ microdomains associated with different isoforms of adenylyl cyclase. J Cell Sci 123:107-117.
66. Wu KY, Zippin JH, Huron D.R., Kamenetsky M., Hengst U, Buck J, Levin L.R., and Jaffrey SR (2006) Soluble adenylyl cyclase is required for netrin-1 signaling in nerve growth cones. Nat Neurosci 9:1257-1264. (Pubitemid 44454267)
67. Wu ZL, Thomas SA, Villacres E.C., Xia Z., Simmons ML, Chavkin C, Palmiter RD, and Storm DR (1995) Altered behavior and long-term potentiation in type I ade-nylyl cyclase mutant mice. Proc Natl Acad Sci USA 92:220-224.
68. Yan L, Vatner DE, O'Connor JP, Ivessa A, Ge H., Chen W, Hirotani S, Ishikawa Y., Sadoshima J, and Vatner SF (2007) Type 5 adenylyl cyclase disruption increases longevity and protects against stress. Cell 130:247-258. (Pubitemid 47081133)
69. Zaccolo M (2011) Spatial control of cAMP signalling in health and disease. Curr Opin Pharmacol 11:649-655.
70. Zippin JH, Chadwick PA, Levin L.R., Buck J., and Magro CM (2010) Soluble adenylyl cyclase defines a nuclear cAMP microdomain in keratinocyte hyperproliferative skin diseases. J Invest Dermatol 130:1279-1287.
71. Zippin JH, Chen Y, Nahirney P., Kamenetsky M, Wuttke MS, Fischman D.A., Levin LR, and Buck J (2003) Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains. FASEB J 17:82-84.
72. Zippin JH, Chen Y, Straub S.G., Hess KC, Diaz A, Lee D, Tso P., Holz GG, Sharp GW, and Levin LR, et al (2013) CO2/HCO3- and calcium regulated soluble adenylyl cyclase as a physiological ATP sensor. J Biol Chem doi:10.1074/jbc. M113.510073.
73. Zippin JH, Farrell J, Huron D., Kamenetsky M, Hess KC, Fischman D.A., Levin LR, and Buck J (2004) Bicarbonate-responsive "soluble" adenylyl cyclase defines a nuclear cAMP microdomain. J Cell Biol 164:527-534. (Pubitemid 38233314)
74. Zippin JH, Levin LR, and Buck J (2001) CO(2)/HCO(3)(-)-responsive soluble adenylyl cyclase as a putative metabolic sensor. Trends Endocrinol Metab 12:366-370. (Pubitemid 33714231)