Adenylyl cyclase isoform-specifi c signaling of GPCRs

G Protein-Coupled Receptors: Structure, Signaling, and Physiology

Volumn , Issue , 2010, Pages 189-216

  Ejendal, Karin F K ^a   Przybyla, Julie A ^a   Watts, Val J ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84867028357     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1017/CBO9780511760334.011     Document Type: Chapter

References (114)

1. Sutherland, E. W. and Rail, T. W. (1958) Fractionation and characterization of a cyclic adenine ribonucleotide formed by tissue particles, J. Biol. Chem. 232, 1077-1091.
2. Chester, J. A. and Watts, V. J. (2007) Adenylyl cyclase 5: a new clue in the search for the “fountain of youth”?, Sci STKE. 2007, e64.
3. Watts, V. J. (2007) Adenylyl cyclase isoforms as novel therapeutic targets: an exciting example of excitotoxicity neuroprotection, Mol. Interv. 7, 70-73.
4. Sadana, R. and Dessauer, C. W. (2009) Physiological roles for G protein-regulated adenylyl cyclase isoforms: insights from knockout and overexpression studies, Neurosignals. 17, 5-22.
5. Dupre, D. J., Robitaille, M., Rebois, R. V., and Hebert, T. E. (2009) The role of Gbetagamma subunits in the organization, assembly, and function of GPCR signaling complexes, Annu. Rev. Pharmacol. Toxicol. 49, 31-56.
6. Omori, K. and Kotera, J. (2007) Overview of PDEs and their regulation, Circ. Res. 100, 309-327.
7. Krupinski, J., Coussen, F., Bakalyar, H. A., Tang, W. J., Feinstein, P. G., Orth, K., Slaughter, C., Reed, R. R., and Gilman, A. G. (1989) Adenylyl cyclase amino acid sequence: possible channel- or transporter-like structure, Science 244, 1558-1564.
8. Buck, J., Sinclair, M. L., Schapal, L., Cann, M. J., and Levin, L. R. (1999) Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals, Proc. Natl. Acad. Sci. U. S. A 96, 79-84.
9. Beazely, M. A. and Watts, V. J. (2006) Regulatory properties of adenylate cyclases type 5 and 6: A progress report, Eur. J. Pharmacol. 535, 1-12.
10. Willoughby, D. and Cooper, D. M. (2007) Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains, Phyisiol. Rev. 87, 965-1010.
11. Cumbay, M. G. and Watts, V. J. (2004) Novel regulatory properties of human type 9 adenylate cyclase (AC9), J. Pharmacol. Exp. Ther.310, 108-115.
12. Cumbay, M. G. and Watts, V. J. (2005) Galphaq potentiation of adenylate cyclase type 9 activity through a Ca2+/calmodulin-dependent pathway, Biochem. Pharmacol.69, 1247-1256.
13. Johnston, C. A., Beazely, M. A., Bilodeau, M. L., Andrisani, O. M., and Watts, V. J. (2004) Differentiation-induced alterations in cyclic & signaling in the Cath.a Differentiated (CAD) neuronal cell line, J. Neurochem. 88, 1497-1508.
14. Visel, A., varez-Bolado, G., Thaller, C., and Eichele, G. (2006) Comprehensive analysis of the expression patterns of the adenylate cyclase gene family in the developing and adult mouse brain, J. Comp Neurol. 496, 684-697.
15. Vortherms, T. A., Nguyen, C. H., Bastepe, M., Juppner, H., and Watts, V. J. (2006) D(2) dopamine receptor-induced sensitization of adenylyl cyclase type 1 is Galpha(s) independent, Neuropharmacology50, 576-584.
16. Chern, Y. (2000) Regulation of adenylyl cyclases in the central nervous system, Cellular Signalling 12, 195-204.
17. 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.
18. Antoni, F. A., Wiegand, U. K., Black, J., and Simpson, J. (2006) Cellular localisation of adenylyl cyclase: a post-genome perspective, Neurochem. Res. 31, 287-295.
19. Ferguson, G. D. and Storm, D. R. (2004) Why calcium-stimulated adenylyl cyclases?, Physiology (Bethesda.) 19, 271-276.
20. McIntire, W. E. (2009) Structural determinants involved in the formation and activation of G protein betagamma dimers, Neurosignals. 17, 82-99.
21. Jiang, L. I., Collins, J., Davis, R., Fraser, I. D., and Sternweis, P. C. (2008) Regulation of cAMP responses by the G12/13 pathway converges on adenylyl cyclase VII, J. Biol.Chem. 283, 23429-23439.
22. Putney, J. W., Jr. (1986) A model for receptor-regulated calcium entry, Cell Calcium 7, 1-12.
23. Martin, A. C., Willoughby, D., Ciruela, A., Ayling, L. J., Pagano, M., Wachten, S., Tengholm, A., and Cooper, D. M. (2009) Capacitative Ca2+ entry via Orai1 and stromal interacting molecule 1 (STIM1) regulates adenylyl cyclase type 8, Mol.Pharmacol.75, 830-842.
24. Nielsen, M. D., Chan, G. C. K., Poser, S. W., and Storm, D. R. (1996) Differential regulation of type I and type VIII Ca2+-stimulated adenylyl cyclases by Gi-coupled receptors in vivo, J. Biol. Chem. 271, 33308-33316.
25. Cumbay, M. G. and Watts, V. J. (2001) Heterologous sensitization of recombinant adenylate cyclases by activation of D2 dopamine receptors, J. Pharmacol. Exp. Ther. 297, 1201-1209.
26. Taussig, R., Iñiguez-Lluhi, J. A., and Gilman, A. (1993) Inhibition of adenylyl cyclase by Gi alpha, Science 261, 218-221.
27. Masada, N., Ciruela, A., Macdougall, D. A., and Cooper, D. M. (2009) Distinct mechanisms of regulation by Ca2+/calmodulin of type 1 and 8 adenylyl cyclases support their different physiological roles, J. Biol. Chem.284, 4451-4463.
28. Choi, E. J., Wong, W. T., Hinds, T. R., and Storm, D. R. (1992) Calcium and muscarinic agonist stimulation of type I adenylylcyclase in whole cells. Biol. Chem.267, 12440-12442.
29. Wayman, G. A., Impey, S., Wu, A., Kindsvogel, W., Prichard, L., and Storm, D. R. (1994) Synergistic activation of the type I adenylyl cyclase by Ca2+ and Gs-coupled receptors in vivo, J. Biol. Chem. 269, 25400-25405.
30. Ostrom, R. S., Naugle, J. E., Hase, M., Gregorian, C., Swaney, J. S., Insel, P. A., Brunton, L. L., and Meszaros, J. G. (2003) Angiotensin II enhances adenylyl cyclase signaling via Ca2+/calmodulin. Gq-Gs cross-talk regulates collagen production in cardiac fibroblasts, J. Biol. Chem.278, 24461-24468.
31. Meszaros, J. G., Gonzalez, A. M., Endo- Mochizuki, Y., Villegas, S., Villarreal, F., and Brunton, L. L. (2000) Identification of G protein-coupled signaling pathways in cardiac fibroblasts: cross talk between G(q) and G(s), Am. J. Physiol Cell Physiol 278, 154-162.
32. 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.
33. Tang, W. J. and Gilman, A. G. (1991) Type-specific regulation of adenylyl cyclase by G protein α subunits, Science 254, 1500-1502.
34. 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 α subunits, Nature 356, 159-161.
35. Taussig, R., Tang, W. J., Hepler, J. R., and Gilman, A. G. (1994) Distinct patterns of bidirectional regulation of mammalian adenylyl cyclases, J. Biol. Chem. 269, 6093-6100.
36. 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 delta, J. Biol. Chem. 278, 4552-4560.
37. 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.
38. Watts, V. J. and Neve, K. A. (1997) Activation of type II adenylate cyclase by D2 and D4 but not D3 dopamine receptors, Mol. Pharmacol. 52, 181-186.
39. Mackay, H. J. and Twelves, C. J. (2007) Targeting the protein kinase C family: are we there yet?, Nat. Rev. Cancer 7, 554-562.
40. 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.
41. Nguyen, C. H. and Watts, V. J. (2006) Dexamethasone-induced Ras protein 1 negatively regulates protein kinase C delta: implications for adenylyl cyclase 2 signaling, Mol. Pharmacol. 69, 1763-1771.
42. Watson, P. A., Krupinski, J., Kempinski, A. M., and Frankenfield, C. D. (1994) Molecular cloning and characterization of the type VII isoform of mammalian ade-nylyl cyclase expressed widely in mouse tissues and in S49 mouse lymphoma cells, J. Biol. Chem. 269, 28893-28898.
43. Hellevuo, K., Yoshimura, M., Mons, N., Hoffman, P. L., Cooper, D. M., and Tabakoff, B. (1995) The characterization of a novel human adenylyl cyclase which is present in brain and other tissues, J. Biol. Chem. 270, 11581-11589.
44. Fagan, K. A., Smith, K. E., and Cooper, D. M. F. (2000) Regulation of the Ca2+-inhibitable adenylyl cyclase type VI by capacitative Ca2+ entry requires localization in cholesterol-rich domains, J. Biol. Chem. 275, 26530-26537.
45. Soboloff, J., Spassova, M. A., Dziadek, M. A., and Gill, D. L. (2006) Calcium signals mediated by STIM and Orai proteins - a new paradigm in inter-organelle communication, Biochim. Biophys. Acta 1763, 1161-1168.
46. Korzeniowski, M. K., Popovic, M. A., Szentpetery, Z., Varnai, P., Stojilkovic, S. S., and Balla, T. (2009) Dependence of stim1/orai1 mediated calcium entry on plasma membrane phosphoinositides, J. Biol. Chem. 284, 21027-21035.
47. Bayewitch, M. L., Avidor-Reiss, T., Levy, R., Pfeuffer, T., Nevo, I., Simonds, W. F., and Vogel, Z. (1998) Inhibition of adenylyl cyclase isoforms V and VI by various Gβγ subunits, FASEB J. 12, 1019-1025.
48. Gao, X., Sadana, R., Dessauer, C. W., and Patel, T. B. (2007) Conditional stimulation of type V and VI adenylyl cyclases by G protein betagamma subunits, J. Biol. Chem. 282, 294-302.
49. Kao, Y. Y., Lai, H. L., Hwang, M. J., and Chern, Y. (2004) An important functional role of the N terminus domain of type VI adenylyl cyclase in Galphai-mediated inhibition, J. Biol. Chem. 279, 34440-34448.
50. Beazely, M. A., Alan, J. K., and Watts, V. J. (2005) Protein kinase C and epidermal growth factor stimulation of Raf1 potentiates adenylyl cyclase type 6 activation in intact cells, Mol. Pharmacol. 67, 250-259.
51. 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 Galphas stimulation, Proc. Natl. Acad. Sci. U. S. A 94, 14100-14104.
52. Iwami, G., Kawabe, J. I., Ebina, T., Cannon, P. J., Homey, C. J., and Ishikawa, Y. (1995) Regulation of adenylyl cyclase by protein kinase A, J. Biol. Chem. 270, 12481-12484.
53. Kawabe, J., Iwami, G., Ebina, T., Ohno, S., Katada, T., Ueda, Y., Homcy, C. J., and Ishikawa, Y. (1994) Differential activation of adenylyl cyclase by protein kinase C isoenzymes, J. Biol. Chem. 269, 16554-16558.
54. Beazely, M. A. and Watts, V. J. (2005) Galpha(q)-coupled receptor signaling enhances adenylate cyclase type 6 activation, Biochem. Pharmacol. 70, 113-120.
55. Yan, S. Z., Huang, Z. H., Andrews, R. K., and Tang, W. J. (1998) Conversion of for-skolin-insensitive to forskolin-sensitive (mouse-type IX) adenylyl cyclase, Molecular Pharmacology 53, 182-187.
56. Paterson, J. M., Smith, S. M., Simpson, J., Grace, O. C., Sosunov, A., Bell, J. E., and Antoni, F. A. (2000) Characterization of human adenylyl cyclase IX reveals inhibition by Ca2+/calcineurin and differential mRNA polyadenylation, J. Neurochem. 75, 1358-1367.
57. Hacker, B. M., Tomlinson, J. E., Wayman, G. A., Sultana, R., Chan, G., Villacres, E., Disteche, C., and Storm, D. R. (1998) Cloning, chromosomal mapping, and regulatory properties of the human type 9 adenylyl cyclase (ADCY9), Genomics 50, 97-104.
58. Sharma, S. K., Klee, W. A., and Nirenberg, M. (1975) Dual regulation of adenylate cyclase accounts for narcotic dependence and tolerance, Proc. Natl. Acad. Sci. U. S. A 72, 3092-3096.
59. Watts, V. J. and Neve, K. A. (2005) Sensitization of adenylate cyclase by Galpha(i/o)-coupled receptors, Pharmacol Ther 106, 405-421.
60. Clark, M. J. and Traynor, J. R. (2006) Mediation of adenylyl cyclase sensitization by PTX-insensitive GalphaoA, Galphai1, Galphai2 or Galphai3, J Neurochem. 99, 1494-1504.
61. Clark, M. J., Harrison, C., Zhong, H., Neubig, R. R., and Traynor, J. R. (2003) Endogenous RGS protein action modulates mu-opioid signaling through Galphao. Effects on adenylyl cyclase, extracellular signal-regulated kinases, and intracellular calcium pathways., J. Biol. Chem. 278, 9418-9425.
62. Watts, V. J., Wiens, B. L., Cumbay, M. G., Vu, M. N., Neve, R. L., and Neve, K. A. (1998) Selective activation of Gao by D2L dopamine receptors in NS20Y neuroblastoma cells, J. Neurosci. 18, 8692-8699.
63. Zhang, L., Tetrault, J., Wang, W., Loh, H. H., and Law, P. Y. (2006) Short- and long-term regulation of adenylyl cyclase activity by delta-opioid receptor are mediated by Galphai2 in neuroblastoma N2A cells, Mol. Pharmacol. 69, 1810-1819.
64. Gintzler, A. R. and Chakrabarti, S. (2006) Post-opioid receptor adaptations to chronic morphine; altered functionality and associations of signaling molecules, Life Sci 79, 717-722.
65. Shy, M., Chakrabarti, S., and Gintzler, A. R. (2008) Plasticity of adenylyl cyclase-related signaling sequelae after long-term morphine treatment, Mol. Pharmacol. 73, 868-879.
66. Beazely, M. A. and Watts, V. J. (2005) Activation of a novel PKC isoform synergisti-cally enhances D2L dopamine receptor-mediated sensitization of adenylate cyclase type 6, Cell Signal 17, 647-653.
67. Tumati, S., Yamamura, H. I., Vanderah, T. W., Roeske, W. R., and Varga, E. V. (2009) Sustained morphine treatment augments capsaicin-evoked CGRP release from primary sensory neurons in a PKA and Raf-1- dependent manner, J. Pharmacol. Exp. Ther. In press.
68. Yue, X., Varga, E. V., Stropova, D., Vanderah, T. W., Yamamura, H. I., and Roeske, W. R. (2006) Chronic morphine-mediated adenylyl cyclase superactivation is attenuated by the Raf-1 inhibitor, GW5074, Eur. J. Pharmacol. 540, 57-59.
69. Nguyen, C. H. and Watts, V. J. (2005) Dexras1 blocks receptor-mediated heterologous sensitization of adenylyl cyclase 1, Biochem Biophys Res Commun 332, 913-920.
70. Steiner, D., Avidor- Reiss, T., Schallmach, E., Saya, D., and Vogel, Z. (2005) Inhibition and superactivation of the calcium-stimulated isoforms of adenylyl cyclase: role of Gbetagamma dimers, J Mol Neurosci 27, 195-203.
71. Fan, P., Jiang, Z., Diamond, I., and Yao, L. (2009) Up-regulation of AGS3 during morphine withdrawal promotes cAMP superactivation via adenylyl cyclase 5 and 7 in rat nucleus accumbens/striatal neurons, Mol. Pharmacol. In press.
72. Rhee, M. H., Nevo, I., Avidor- Reiss, T., Levy, R., and Vogel, Z. (2000) Differential superactivation of adenylyl cyclase isozymes after chronic activation of the CB1 can-nabinoid receptor, Mol. Pharmacol. 57, 746-752.
73. Watts, V. J. and Neve, K. A. (1996) Sensitization of endogenous and recombinant adenylate cyclase by activation of D2 dopamine receptors, Mol. Pharmacol. 50, 966-976.
74. Schallmach, E., Steiner, D., and Vogel, Z. (2006) Adenylyl cyclase type II activity is regulated by two different mechanisms: implications for acute and chronic opioid exposure, Neuropharmacology 50, 998-1005.
75. Vortherms, T. A., Nguyen, C. H., Berlot, C. H., and Watts, V. J. (2004) Using molecular tools to dissect the role of Gs in sensitization of AC1, Mol. Pharmacol. 66, 1617-1624.
76. Chakrabarti, S. and Gintzler, A. R. (2007) Phosphorylation of Galphas influences its association with the micro-opioid receptor and is modulated by long-term morphine exposure, Mol. Pharmacol. 72, 753-760.
77. 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.
78. Cali, J. J., Parekh, R. S., and Krupinski, J. (1996) Splice variants of type VIII adenylyl cyclase. Differences in glycosylation and regulation by Ca2+/calmodulin, J. Biol. Chem. 271, 1089-1095.
79. Wei, J., Wayman, G., and Storm, D. R. (1996) Phosphorylation and inhibition of type III adenylyl cyclase by calmodulin-dependent protein kinase II in vivo, J. Biol. Chem. 271, 24231-24235.
80. Wu, G. C., Lai, H. L., Lin, Y. W., Chu, Y. T., and Chern, Y. (2001) N-Glycosylation and residues Asn805 and Asn890 are involved in the functional properties of type VI adenylyl cyclase, J. Biol. Chem. 276, 35450-35457.
81. McVey, M., Hill, J., Howlett, A., and Klein, C. (1999) Adenylyl cyclase, a coincidence detector for nitric oxide, J. Biol. Chem. 274, 18887-18892.
82. Hill, J., Howlett, A., and Klein, C. (2000) Nitric oxide selectively inhibits adenylyl cyclase isoforms 5 and 6, Cell Signal. 12, 233-237.
83. Arejian, M., Li, Y., and Anand- Srivastava, M. B. (2009) Nitric oxide attenuates the expression of natriuretic peptide receptor C and associated adenylyl cyclase signaling in aortic vascular smooth muscle cells: role of MAPK, Am. J. Physiol Heart Circ. Physiol 296, H1859-H1867.
84. Tesmer, J. J., Sunahara, R. K., Gilman, A. G., and Sprang, S. R. (1997) Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsa GTPS, Science 278, 1907-1916.
85. Zhang, G. Y., Liu, Y., Ruoho, A. E., and Hurley, J. H. (1997) Structure of the adenylyl cyclase catalytic core, Nature 386, 247-253.
86. Tang, W. J., Stanzel, M., and Gilman, A. G. (1995) Truncation and alanine-scanning mutants of type I adenylyl cyclase, Biochemistry 34, 14563-14572.
87. Gu, C., Cali, J. J., and Cooper, D. M. F. (2002) Dimerization of mammalian adenylate cyclases, Eur. J. Biochem. 269, 413-421.
88. Baragli, A., Grieco, M. L., Trieu, P., Villeneuve, L. R., and Hebert, T. E. (2008) Heterodimers of adenylyl cyclases 2 and 5 show enhanced functional responses in the presence of Galpha s, Cell Signal 20, 480-492.
89. Pontier, S. M., Percherancier, Y., Galandrin, S., Breit, A., Gales, C., and Bouvier, M. (2008) Cholesterol-dependent separation of the beta2-adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction, J. Biol. Chem. 283, 24659-24672.
90. Rybin, V. O., Xu, X., Lisanti, M. P., and Steinberg, S. F. (2000) Differential targeting of á-adrenergic receptor subtypes and adenylyl cyclase to cardiomyocyte caveolae, J. Biol. Chem. 275, 41447-41457.
91. Patel, H. H., Murray, F., and Insel, P. A. (2008) G-protein-coupled receptor-signaling components in membrane raft and caveolae microdomains, Handb. Exp. Pharmacol. 167-184.
92. Levitt, E. S., Clark, M. J., Jenkins, P. M., Martens, J. R., and Traynor, J. R. (2009) Differential effect of membrane cholesterol removal on mu and delta opioid receptors: A parallel comparison of acute and chronic signaling to adenylyl cyclase, J. Biol. Chem. 284, 22108-22122.
93. Piggott, L. A., Bauman, A. L., Scott, J. D., and Dessauer, C. W. (2008) The A-kinase anchoring protein Yotiao binds and regulates adenylyl cyclase in brain, Proc Natl Acad Sci U S A 105, 13835-13840.
94. Vidi, P. A. and Watts, V. J. (2009) Fluorescent and bioluminescent protein-fragment complementation assays in the study of G protein-coupled receptor oligomerization and signaling, Mol. Pharmacol. 75, 733-739.
95. Bouvier, M., Heveker, N., J ockers, R., Marullo, S., and Milligan, G. (2007) BRET analysis of GPCR oligomerization: newer does not mean better, Nat Methods 4, 3-4.
96. Dupre, D. J., Baragli, A., Rebois, R. V., Ethier, N., and Hebert, T. E. (2007) Signalling complexes associated with adenylyl cyclase II are assembled during their biosynthesis, Cell Signal 19, 481-489.
97. Jarrahian, A., Watts, V. J., and Barker, E. L. (2004) D2 dopamine receptors modulate Galpha-subunit coupling of the CB1 cannabinoid receptor, J. Pharmacol. Exp. Ther. 308, 880-886.
98. Kearn, C. S., Blake- Palmer, K., Daniel, E., Mackie, K., and Glass, M. (2005) Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: a mechanism for receptor cross-talk?, Mol. Pharmacol. 67, 1697-1704.
99. Lee, S. P., So, C. H., Rashid, A. J., Varghese, G., Cheng, R., Lanca, A. J., O’Dowd B. F., and George, S. R. (2004) Dopamine D1 and D2 receptor Co-activation generates a novel phospholipase C-mediated calcium signal, J. Biol. Chem. 279, 35671-35678.
100. So, C. H., Verma, V., Alijaniaram, M., Cheng, R., Rashid, A. J., O’Dowd B. F., and George, S. R. (2009) Calcium signaling by dopamine D5 receptor and D5-D2 receptor hetero-oligomers occurs by a mechanism distinct from that for dopamine D1-D2 receptor hetero-oligomers, Mol. Pharmacol. 75, 843-854.
101. Fiorentini, C., Busi, C., Gorruso, E., Gotti, C., Spano, P., and Missale, C. (2008) Reciprocal regulation of dopamine D1 and D3 receptor function and trafficking by heterodimerization, Mol. Pharmacol. 74, 59-69.
102. Marcellino, D., Ferre, S., Casado, V., Cortes, A., Le, F. B., Mazzola, C., Drago, F., Saur, O., Stark, H., Soriano, A., Barnes, C., Goldberg, S. R., Lluis, C., Fuxe, K., and Franco, R. (2008) Identification of dopamine D1-D3 receptor heteromers. Indications for a role of synergistic D1-D3 receptor interactions in the striatum, J. Biol. Chem. 283, 26016-26025.
103. McIntire, W. E., MacCleery, G., and Garrison, J. C. (2001) The G protein β subunit is a determinant in the coupling of Gs to the ß1-adrenergic and A2a adenosine receptors, J. Biol. Chem. 276, 15801-15809.
104. Hwang, J. I., Choi, S., Fraser, I. D., Chang, M. S., and Simon, M. I. (2005) Silencing the expression of multiple Gbeta-subunits eliminates signaling mediated by all four families of G proteins, Proc. Natl. Acad. Sci. U. S. A 102, 9493-9498.
105. Wang, Q., Jolly, J. P., Surmeier, J. D., Mullah, B. M., Lidow, M. S., Bergson, C. M., and Robishaw, J. D. (2001) Differential dependence of the D1 and D5 dopamine receptors on the G protein gamma 7 subunit for activation of adenylylcyclase, J. Biol. Chem. 276, 39386–39393.
106. Schwindinger, W. F., Betz, K. S., Giger, K. E., Sabol, A., Bronson, S. K., and Robishaw, J. D. (2003) Loss of G protein gamma 7 alters behavior and reduces striatal alphaolf level and cAMP production, J. Biol. Chem. 278, 6575–6579
107. Pierre, S., Eschenhagen, T., Geisslinger, G., and Scholich, K. (2009) Capturing adenylyl cyclases as potential drug targets, Nat. Rev. Drug Discov. 8, 321–335
108. Wu, Z. L., Thomas, S. A., Villacres, E. C., Xia, Z., Simmons, M. L., Chavkin, C., Palmiter, R. D., and Storm, D. R. (1995) Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice, Proc. Natl. Acad. Sci. U. S. A 92, 220–224
109. Schaefer, M. L., Wong, S. T., Wozniak, D. F., Muglia, L. M., Liauw, J. A., Zhuo, M., Nardi, A., Hartman, R. E., Vogt, S. K., Luedke, C. E., Storm, D. R., and Muglia, L. J. (2000) Altered stress-induced anxiety in adenylyl cyclase type VIII-defi cient mice, J Neurosci 20, 4809–4820
110. Wong, S. T., Athos, J., Figueroa, X. A., Pineda, V. V., Scheafer, M. L., Chavkin, C. C., Muglia, L. J., and Storm, D. R. (1999) Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP, Neuron 23, 787–798.
111. Li, S., Lee, M. L., Bruchas, M. R., Chan, G. C., Storm, D. R., and Chavkin, C. (2006) Calmodulin-stimulated adenylyl cyclase gene deletion affects morphine responses, Mol. Pharmacol. 70, 1742–1749.
112. Yoshimura, M., Wu, P. H., Hoffman, P. L., and Tabakoff, B. (2000) Overexpression of type 7 adenylyl cyclase in the mouse brain enhances acute and chronic actions of morphine, Mol. Pharmacol. 58, 1011–1016.
113. Yan, L., Vatner, D. E., O’ Connor J. P., Ivessa A., Ge H., Chen W., Hirotani S., Ishikawa Y., Sadoshima J., and Vatner S. F. (2007) Type 5 adenylyl cyclase disruption increases longevity and protects against stress, Cell 130, 247–258.
114. Zahniser, N. R., Simosky, J. K., Mayfi eld, R. D., Negri, C. A., Hanania, T., Larson, G. A., Kelly, M. A., Grandy, D. K., Rubinstein, M., Low, M. J., and Fredholm, B. B. (2000) Functional uncoupling of adenosine A2A receptors and reduced response to caffeine in mice lacking dopamine D2 receptors, J. Neurosci. 5949–5957