Muscarinic receptors stimulate AC2 by novel phosphorylation sites, whereas Gβγ subunits exert opposing effects depending on the G-protein source

Biochemical Journal

Volumn 447, Issue 3, 2012, Pages 393-405

  Shen, Jia X ^a   Wachten, Sebastian ^a   Halls, Michelle L ^a   Everett, Katy L ^a   Cooper, Dermot M F ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Adenylyl cyclase 2 (AC2); Muscarinic receptor; Protein kinase C (PKC); Somatostatin receptor

Indexed keywords

ADENYLATE CYCLASE; ADENYLATE CYCLASE 2; CARBACHOL; CYCLIC AMP; FORSKOLIN; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; MUSCARINIC M3 RECEPTOR; MUSCARINIC RECEPTOR; MUTANT PROTEIN; MYRISTIC ACID DERIVATIVE; PHORBOL MYRISTIC ACID; PROSTAGLANDIN E1; PROTEIN KINASE C; SERINE; SOMATOSTATIN RECEPTOR; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ADENYLATE CYCLASE; ANIMALS; CARBACHOL; CYCLIC AMP; ENZYME ACTIVATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; HEK293 CELLS; HUMANS; MUTATION; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RECEPTOR, MUSCARINIC M3; RECEPTORS, SOMATOSTATIN; SINGLE-CELL ANALYSIS;

EID: 84867279636     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120279     Document Type: Article

References (49)

1. Robison, G. A., Butcher, R. W. and Sutherland, E. W. (1968) Cyclic AMP. Annu. Rev. Biochem. 37, 149-174
2. Butcher, R. W., Robison, G. A., Hardman, J. G. and Sutherland, E. W. (1968) The role of cyclic AMP in hormone actions. Adv. Enzyme Regul. 6, 357-389
3. 2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol. Rev. 87, 965-1010
4. Dessauer, C. W. (2009) Adenylyl cyclase-A-kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol. Pharmacol. 76, 935-941
5. Houslay, M. D. and Milligan, G. (1997) Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem. Sci. 22, 217-224 (Pubitemid 27246638)
6. Watts, V. J. and Neve, K. A. (2005) Sensitization of adenylate cyclase by Gαi/o-coupled receptors. Pharmacol. Ther. 106, 405-421 (Pubitemid 40726295)
7. Taussig, R. and Gilman, A. G. (1995) Mammalian membrane-bound adenylyl cyclases. J. Biol. Chem. 270, 1-4
8. Cooper, D. M. F. (2003) Regulation and organization of adenylyl cyclases and cAMP. Biochem. J. 375, 517-529
9. 2+-signaling pathways of adenylyl cyclases. Cold Spring Harbor Perspect. Biol. 3, a004143
10. Cooper, D. M. F., Mons, N. and Karpen, J. W. (1995) Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature 374, 421-424
11. Ehnert, C., Tegeder, I., Pierre, S., Birod, K., Nguyen, H. V., Schmidtko, A., Geisslinger, G. and Scholich, K. (2004) Protein associated with Myc (PAM) is involved in spinal nociceptive processing. J. Neurochem. 88, 948-957 (Pubitemid 38199316)
12. Iwasa, H., Kikuchi, S., Mine, S., Miyagishima, H., Sugita, K., Sato, T. and Hasegawa, S. (2000) Up-regulation of type II adenylyl cyclase mRNA in kindling model of epilepsy in rats. Neurosci. Lett. 282, 173-176 (Pubitemid 30136455)
13. Zimmermann, G. and Taussig, R. (1996) Protein kinase C alters the responsiveness of adenylyl cyclases to G protein α and βγ subunits. J. Biol. Chem. 271, 27161-27166 (Pubitemid 26359138)
14. Yoshimura, M. and Cooper, D. M. F. (1993) Type-specific stimulation of adenylylcyclase by protein kinase C. J. Biol. Chem. 268, 4604-4607 (Pubitemid 23081567)
15. Jacobowitz, O., Chen, J., Premont, R. T. and Iyengar, R. (1993) Stimulation of specific types of Gs-stimulated adenylyl cyclases by phorbol ester treatment. J. Biol. Chem. 268, 3829-3832 (Pubitemid 23072909)
16. Jacobowitz, O. and Iyengar, R. (1994) Phorbol ester-induced stimulation and phosphorylation of adenylyl cyclase 2. Proc. Natl. Acad. Sci. U.S.A. 91, 10630-10634 (Pubitemid 24329052)
17. Lustig, K. D., Conklin, B. R., Herzmark, P., Taussig, R. and Bourne, H. R. (1993) Type II adenylyl cyclase integrates coincident signals from Gs, Gi, and Gq. J. Biol. Chem. 268, 13900-13905 (Pubitemid 23195502)
18. Tsu, R. C. and Wong, Y. H. (1996) Gi-mediated stimulation of type II adenylyl cyclase is augmented by Gq-coupled receptor activation and phorbol ester treatment. J. Neurosci. 16, 1317-1323
19. Levin, L. R. and Reed, R. R. (1995) Identification of functional domains of adenylyl cyclase using in vivo chimeras. J. Biol. Chem. 270, 7573-7579
20. Bol, G. F., Gros, C., Hulster, A., Bosel, A. and Pfeuffer, T. (1997) Phorbol ester-induced sensitisation of adenylyl cyclase type II is related to phosphorylation of threonine 1057. Biochem. Biophys. Res. Comm. 237, 251-256 (Pubitemid 27406014)
21. Bol, G. F., Hulster, A. and Pfeuffer, T. (1997) Adenylyl cyclase type II is stimulated by PKC via C-terminal phosphorylation. Biochim. Biophys. Acta 1358, 307-313 (Pubitemid 27462656)
22. 2+-dependent cAMP synthesis in pancreatic and neuronal systems. J. Biol. Chem. 285, 20328-20342
23. Wachten, S., Masada, N., Ayling, L. J., Ciruela, A., Nikolaev, V. O., Lohse, M. J. and Cooper, D. M. F. (2010) Distinct pools of cAMP centre on different isoforms of adenylyl cyclase in pituitary-derived GH3 B6 cells. J. Cell Sci. 123, 95-106
24. Nikolaev, V. O., Bunemann, M., Hein, L., Hannawacker, A. and Lohse, M. J. (2004) Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Chem. 279, 37215-37218 (Pubitemid 39195424)
25. Blom, N., Gammeltoft, S. and Brunak, S. (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294, 1351-1362 (Pubitemid 30008805)
26. Xue, Y., Ren, J., Gao, X., Jin, C., Wen, L. and Yao, X. (2008) GPS 2.0, a tool to predict kinase-specific phosphorylation sites in hierarchy. Mol Cell Proteomics. 7, 1598-1608
27. Xue, Y., Li, A., Wang, L., Feng, H. and Yao, X. (2006) PPSP: prediction of PK-specific phosphorylation site with Bayesian decision theory. BMC Bioinformatics 7, 163
28. Li, T., Li, F. and Zhang, X. (2008) Prediction of kinase-specific phosphorylation sites with sequence features by a log-odds ratio approach. Proteins 70, 404-414
29. Evans, T., Smith, M. M., Tanner, L. I. and Harden, T. K. (1984) Muscarinic cholinergic receptors of two cell lines that regulate cyclic AMP metabolism by different molecular mechanisms. Mol. Pharmacol. 26, 395-404 (Pubitemid 15190701)
30. 2+/calmodulin of type 1 and 8 adenylyl cyclases support their different physiological roles. J. Biol. Chem. 284, 4451-4463
31. 2+ entry via Orai1 and stromal interacting molecule 1 (STIM1) regulates adenylyl cyclase type 8. Mol. Pharmacol. 75, 830-842
32. Federman, A. D., Conklin, B. R., Schrader, K. A., Reed, R. R. and Bourne, H. R. (1992) Hormonal stimulation of adenylyl cyclase through Gi-protein βγ subunits. Nature 356, 159-161
33. Tang, W. J. and Gilman, A. G. (1991) Type-specific regulation of adenylyl cyclase by G protein βγ subunits. Science 254, 1500-1503
34. el-Fakahany, E. E., Alger, B. E., Lai, W. S., Pitler, T. A., Worley, P. F. and Baraban, J. M. (1988) Neuronal muscarinic responses: role of protein kinase C. FASEB J. 2, 2575-2583
35. Iancu, R. V., Ramamurthy, G. and Harvey, R. D. (2008) Spatial and temporal aspects of cAMP signalling in cardiac myocytes. Clin. Exp. Pharmacol. Physiol. 35, 1343-1348
36. Herbert, J. M., Augereau, J. M., Gleye, J. and Maffrand, J. P. (1990) Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 172, 993-999
37. Taussig, R., Quarmby, L. M. and Gilman, A. G. (1993) Regulation of purified type I and type II adenylylcyclases by G protein βγ subunits. J. Biol. Chem. 268, 9-12 (Pubitemid 23021277)
38. Sunahara, R. K., Dessauer, C. W. and Gilman, A. G. (1996) Complexity and diversity of mammalian adenylyl cyclases. Ann. Rev. Pharmacol. Toxicol. 36, 461-480 (Pubitemid 26168706)
39. Lehmann, D. M., Seneviratne, A. M. and Smrcka, A. V. (2008) Small molecule disruption of G protein βγ subunit signaling inhibits neutrophil chemotaxis and inflammation. Mol. Pharmacol. 73, 410-418 (Pubitemid 351159211)
40. Nelson, E. J., Hellevuo, K., Yoshimura, M. and Tabakoff, B. (2003) Ethanol-induced phosphorylation and potentiation of the activity of type 7 adenylyl cyclase. Involvement of protein kinase C δ. J. Biol. Chem. 278, 4552-4560 (Pubitemid 36805609)
41. Jacobowitz, O., Chen, J., Premont, R. T. and Iyengar, R. (1993) Stimulation of specific types of Gs-stimulated adenylyl cyclases by phorbol ester treatment. J. Biol. Chem. 268, 3829-3832 (Pubitemid 23072909)
42. Krupinski, J. and Cali, J. J. (1998) Molecular diversity of the adenylyl cyclases. Adv. Second Messenger Phosphoprotein Res. 32, 53-79
43. Wayman, G. A., Wei, J., Wong, S. and Storm, D. R. (1996) Regulation of type I adenylyl cyclase by calmodulin kinase IV in vivo. Mol. Cell. Biol. 16, 6075-6082 (Pubitemid 26360967)
44. Chen, Y., Harry, A., Li, J., Smit, M. J., Bai, X., Magnusson, R., Pieroni, J. P., Weng, G. and Iyengar, R. (1997) Adenylyl cyclase 6 is selectively regulated by protein kinase A phosphorylation in a region involved in Gαs stimulation. Proc. Natl. Acad. Sci. U.S.A. 94, 14100-14104
45. Tsu, R. C., Allen, R. A. and Wong, Y. H. (1995) Stimulation of type II adenylyl cyclase by chemoattractant formyl peptide and C5a receptors. Mol. Pharmacol. 47, 835-841
46. Diel, S., Klass, K., Wittig, B. and Kleuss, C. (2006) Gβγ activation site in adenylyl cyclase type II. Adenylyl cyclase type III is inhibited by Gβγ . J Biol Chem. 281, 288-294 (Pubitemid 43671188)
47. Yan, S. Z., Beeler, J. A., Chen, Y., Shelton, R. K. and Tang, W. J. (2001) The regulation of type 7 adenylyl cyclase by its C1b region and Escherichia coli peptidylprolyl isomerase, SlyD. J. Biol. Chem. 276, 8500-8506
48. Beeler, J. A., Yan, S. Z., Bykov, S., Murza, A., Asher, S. and Tang, W. J. (2004) A soluble C1b protein and its regulation of soluble type 7 adenylyl cyclase. Biochemistry 43, 15463-15471 (Pubitemid 39647471)
49. Boran, A. D., Chen, Y. and Iyengar, R. (2011) Identification of new Gβγ interaction sites in adenylyl cyclase 2. Cell. Signaling 23, 1489-1495