Adenylate cyclase-centred microdomains

Biochemical Journal

Volumn 462, Issue 2, 2014, Pages 199-213

  Cooper, Dermot M F ^a   Tabbasum, Valentina G ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

A kinase anchoring protein (AKAP); Adenylate cyclase; Focal adhesion; Microdomain; Protein kinase; Scaffold

Indexed keywords

ADENYLATE CYCLASE; ANIMALS; CALCIUM; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HUMANS; MEMBRANE MICRODOMAINS; SIGNAL TRANSDUCTION;

EID: 84905903575     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140560     Document Type: Review

References (172)

1. Halls, M. L. and Cooper, D. M. F. (2011) Regulation by Ca2+ -signaling pathways of adenylyl cyclases. Cold Spring Harb. Perspect. Biol. 3, a004143
2. Sunahara, R. K., Dessauer, C. W. and Gilman, A. G. (1996) Complexity and diversity of mammalian adenylyl cyclases. Annu. Rev. Pharmacol. Toxicol. 36, 461-480 (Pubitemid 26168706)
3. 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
4. Ostrom, R. S., Bogard, A. S., Gros, R. and Feldman, R. D. (2012) Choreographing the adenylyl cyclase signalosome: sorting out the partners and the steps. Naunyn Schmiedebergs Arch. Pharmacol. 385, 5-12
5. 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 (Pubitemid 19189731)
6. Baillie, G. S. and Houslay, M. D. (2005) Arrestin times for compartmentalised cAMP signalling and phosphodiesterase-4 enzymes. Curr. Opin. Cell Biol. 17, 129-134 (Pubitemid 40380935)
7. MacKenzie, S. J., Baillie, G. S., McPhee, I., Bolger, G. B. and Houslay, M. D. (2000) ERK2 mitogen-activated protein kinase binding, phosphorylation, and regulation of the PDE4D cAMP-specific phosphodiesterases: the involvement of COOH-terminal docking sites and NH2-terminal UCR regions. J. Biol. Chem. 275, 16609-16617 (Pubitemid 30398887)
8. Edwards, H. V., Christian, F. and Baillie, G. S. (2012) cAMP: novel concepts in compartmentalised signalling. Semin. Cell Dev. Biol. 23, 181-190
9. Willis, M. J. and Baillie, G. S. (2014) Arrestin-dependent localization of phosphodiesterases. Handb. Exp. Pharmacol. 219, 293-307
10. Cooper, D. M. F. (2003) Regulation and organization of adenylyl cyclases and cAMP. Biochem. J. 375, 517-529 (Pubitemid 37433500)
11. 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
12. 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
13. Falke, J. J., Drake, S. K., Hazard, A. L. and Peersen, O. B. (1994) Molecular tuning of ion binding to calcium signaling proteins. Q. Rev. Biophys. 27, 219-290 (Pubitemid 24368671)
14. Mou, T. C., Masada, N., Cooper, D. M. F. and Sprang, S. R. (2009) Structural basis for inhibition of mammalian adenylyl cyclase by calcium. Biochemistry 48, 3387-3397
15. Wu, Z., Wong, S. T. and Storms, D. R. (1993) Modification of the calcium and calmodulin sensitivity of the type I adenylyl cyclase by mutagenesis of its calmodulin binding domain. J. Biol. Chem. 268, 23766-23768 (Pubitemid 23335341)
16. Masada, N., Ciruela, A., Macdougall, D. A. and Cooper, D. M. F. (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
17. Catterall, W. A. (2011) Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 3, a003947
18. Mori, M. X., Erickson, M. G. and Yue, D. T. (2004) Functional stoichiometry and local enrichment of calmodulin interacting with Ca2+ channels. Science 304, 432-435 (Pubitemid 38495937)
19. Tran, Q. K., Black, D. J. and Persechini, A. (2003) Intracellular coupling via limiting calmodulin. J. Biol. Chem. 278, 24247-24250 (Pubitemid 37548572)
20. Gu, C. and Cooper, D. M. F. (1999) Calmodulin-binding sites on adenylyl cyclase type VIII. J. Biol. Chem. 274, 8012-8021
21. Simpson, R. E., Ciruela, A. and Cooper, D. M. F. (2006) The role of calmodulin recruitment in Ca2+ -stimulation of adenylyl cyclase type 8. J. Biol. Chem. 281, 17379-17389
22. Macdougall, D. A., Wachten, S., Ciruela, A., Sinz, A. and Cooper, D. M. F. (2009) Separate elements within a single IQ-like motif in adenylyl cyclase type 8 impart Ca2+ /calmodulin binding and autoinhibition. J. Biol. Chem. 284, 15573-15588
23. Herbst, S., Masada, N., Pfennig, S., Ihling, C. H., Cooper, D. M. F. and Sinz, A. (2013) Structural insights into calmodulin/adenylyl cyclase 8 interaction. Anal. Bioanal. Chem. 405, 9333-9342
24. Masada, N., Schaks, S., Jackson, S. E., Sinz, A. and Cooper, D. M. F. (2012) Distinct mechanisms of calmodulin binding and regulation of adenylyl cyclases 1 and 8. Biochemistry 51, 7917-7929
25. Putney, Jr, J. W. (1991) The capacitative model for receptor-activated calcium entry. Adv. Pharmacol. 22, 251-269
26. Willoughby, D. and Cooper, D. M. F. (2007) Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol. Rev. 87, 965-1010 (Pubitemid 47084674)
27. Kitaguchi, T., Oya, M., Wada, Y., Tsuboi, T. and Miyawaki, A. (2013) Extracellular calcium influx activates adenylate cyclase 1 and potentiates insulin secretion in MIN6 cells. Biochem. J. 450, 365-373
28. Kryukova, Y. N., Protas, L. and Robinson, R. B. (2012) Ca2+ -activated adenylyl cyclase 1 introduces Ca2+ -dependence to adrenergic stimulation of HCN2 current. J. Mol. Cell. Cardiol. 52, 1233-1239
29. Fagan, K. A., Graf, R. A., Tolman, S., Schaack, J. and Cooper, D. M. F. (2000) Regulation of a Ca2+ -sensitive adenylyl cyclase in an excitable cell: role of voltage-gated versus capacitative Ca2+ entry. J. Biol. Chem. 275, 40187-40194 (Pubitemid 32064648)
30. Fagan, K. A., Rich, T. C., Tolman, S., Schaack, J., Karpen, J. W. and Cooper, D. M. F. (1999) Adenovirus-mediated expression of an olfactory cyclic nucleotide-gated channel regulates the endogenous Ca2+ -inhibitable adenylyl cyclase in C6-2B glioma cells. J. Biol. Chem. 274, 12445-12453
31. Everett, K. L. and Cooper, D. M. F. (2013) An improved targeted cAMP sensor to study the regulation of adenylyl cyclase 8 by Ca2+ entry through voltage-gated channels. PLoS ONE 8, e75942
32. Yu, H. J., Ma, H. and Green, R. D. (1993) Calcium entry via L-type calcium channels acts as a negative regulator of adenylyl cyclase activity and cyclic AMP levels in cardiac myocytes. Mol. Pharmacol. 44, 689-693 (Pubitemid 23317279)
33. Chetkovich, D. M., Gray, R., Johnston, D. and Sweatt, J. D. (1991) N-methyl-D-aspartate receptor activation increases cAMP levels and voltage-gated Ca2+ channel activity in area Ca1 of hippocampus. Proc. Natl. Acad. Sci. U.S.A. 88, 6467-6471 (Pubitemid 21914967)
34. Dai, S., Hall, D. D. and Hell, J. W. (2009) Supramolecular assemblies and localized regulation of voltage-gated ion channels. Physiol. Rev. 89, 411-452
35. Lefkimmiatis, K., Srikanthan, M., Maiellaro, I., Moyer, M. P., Curci, S. and Hofer, A. M. (2009) Store-operated cyclic AMP signalling mediated by STIM1. Nat. Cell Biol. 11, 433-442
36. Maiellaro, I., Lefkimmiatis, K., Moyer, M. P., Curci, S. and Hofer, A. M. (2012) Termination and activation of store-operated cyclic AMP production. J. Cell. Mol. Med. 16, 2715-2725
37. Grigoriev, I., Gouveia, S. M., van der Vaart, B., Demmers, J., Smyth, J. T., Honnappa, S., Splinter, D., Steinmetz, M. O., Putney, Jr, J. W., Hoogenraad, C. C. and Akhmanova, A. (2008) STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr. Biol. 18, 177-182
38. Blau, L. and Weissmann, G. (1988) Transmembrane calcium movements mediated by ionomycin and phosphatidate in liposomes with Fura 2 entrapped. Biochemistry 27, 5661-5666
39. Tallini, Y. N., Ohkura, M., Choi, B. R., Ji, G., Imoto, K., Doran, R., Lee, J., Plan, P., Wilson, J., Xin, H. B. et al. (2006) Imaging cellular signals in the heart in vivo: cardiac expression of the high-signal Ca2+ indicator GCaMP2. Proc. Natl. Acad. Sci. U.S.A. 103, 4753-4758
40. Willoughby, D., Wachten, S., Masada, N. and Cooper, D. M. F. (2010) Direct demonstration of discrete Ca2+ microdomains associated with different isoforms of adenylyl cyclase. J. Cell Sci. 123, 107-117
41. Willoughby, D., Everett, K. L., Halls, M. L., Pacheco, J., Skroblin, P., Vaca, L., Klussmann, E. and Cooper, D. M. F. (2012) Direct binding between Orai1 and AC8 mediates dynamic interplay between Ca2+ and cAMPs. Sci. Signal. 5, ra29
42. Tadross, M. R., Dick, I. E. and Yue, D. T. (2008) Mechanism of local and global Ca2+ sensing by calmodulin in complex with a Ca2+ channel. Cell 133, 1228-1240 (Pubitemid 351852914)
43. Alvarez, L., Dai, L., Friedrich, B. M., Kashikar, N. D., Gregor, I., Pascal, R. and Kaupp, U. B. (2012) The rate of change in Ca2+ concentration controls sperm chemotaxis. J. Cell Biol. 196, 653-663
44. Dessauer, C. W. (2009) Adenylyl cyclase-A-kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol. Pharmacol. 76, 935-941
45. Rubin, C. S. (1994) A kinase anchor proteins and the intracellular targeting of signals carried by cyclic AMP. Biochim. Biophys. Acta 1224, 467-479
46. Scott, J. D., Dessauer, C. W. and Taskén, K. (2012) Creating order from chaos: cellular regulation by kinase anchoring. Annu. Rev. Pharmacol. Toxicol. 53, 187-210
47. Bauman, A. L., Soughayer, J., Nguyen, B. T., Willoughby, D., Carnegie, G. K., Wong, W., Hoshi, N., Langeberg, L. K., Cooper, D. M. F., Dessauer, C. W. and Scott, J. D. (2006) Dynamic regulation of cAMP synthesis through anchored PKA-adenylyl cyclase V/VI complexes. Mol. Cell 23, 925-931 (Pubitemid 44363046)
48. Willoughby, D., Masada, N., Wachten, S., Pagano, M., Halls, M. L., Everett, K. L., Ciruela, A. and Cooper, D. M. F. (2010) AKAP79/150 interacts with AC8 and regulates Ca2+ -dependent cAMP synthesis in pancreatic and neuronal systems. J. Biol. Chem. 285, 20328-20342
49. Kapiloff, M. S., Piggott, L. A., Sadana, R., Li, J., Heredia, L. A., Henson, E., Efendiev, R. and Dessauer, C. W. (2009) An adenylyl cyclase-mAKAP signaling complex regulates cAMP levels in cardiac myocytes. J. Biol. Chem. 284, 23540-23546
50. Shen, J. X. and Cooper, D. M. F. (2013) AKAP79, PKC, PKA and PDE4 participate in a Gq-linked muscarinic receptor and adenylate cyclase 2 cAMP signalling complex. Biochem. J. 455, 47-56
51. Li, Y., Chen, L., Kass, R. S. and Dessauer, C. W. (2012) The A-kinase anchoring protein Yotiao facilitates complex formation between adenylyl cyclase type 9 and the IKs potassium channel in heart. J. Biol. Chem. 287, 29815-29824
52. Halls, M. L. and Cooper, D. M. F. (2010) Sub-picomolar relaxin signalling by a pre-assembled RXFP1, AKAP79, AC2, arrestin 2, PDE4D3 complex. EMBO J. 29, 2772-2787
53. Willoughby, D., Halls, M. L., Everett, K. L., Ciruela, A., Skroblin, P., Klussmann, E. and Cooper, D. M. F. (2012) A key phosphorylation site in AC8 mediates regulation of Ca2+ -dependent cAMP dynamics by an AC8-AKAP79-PKA signalling complex. J. Cell Sci. 125, 5850-5859
54. 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
55. Wu, Z., Wong, S. T. and Storm, D. R. (1993) Modification of the calcium and calmodulin sensitivity of the type I adenylyl cyclase by mutagenesis of its calmodulin binding domain. J. Biol. Chem. 268, 23766-23768 (Pubitemid 23335341)
56. Vorherr, T., Knopfel, L., Hofmann, F., Mollner, S., Pfeuffer, T. and Carafoli, E. (1993) The calmodulin binding domain of nitric oxide synthase and adenylyl cyclase. Biochemistry 32, 6081-6088 (Pubitemid 23198769)
57. 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
58. Efendiev, R., Samelson, B. K., Nguyen, B. T., Phatarpekar, P. V., Baameur, F., Scott, J. D. and Dessauer, C. W. (2010) AKAP79 interacts with multiple adenylyl cyclase (AC) isoforms and scaffolds AC5 and -6 to amino-3-hydroxyl-5-methyl-4- isoxazole-propionate (AMPA) receptors. J. Biol. Chem. 285, 14450-14458
59. Wang, H. Y. and Burns, L. H. (2006) G that interacts with adenylyl cyclase in opioid tolerance originates from a Gs protein. J. Neurobiol. 66, 1302-1310 (Pubitemid 44713809)
60. Schwencke, C., Yamamoto, M., Okumura, S., Toya, Y., Kim, S. J. and Ishikawa, Y. (1999) Compartmentation of cyclic adenosine 3,5-monophosphate signaling in caveolae. Mol. Endocrinol. 13, 1061-1070 (Pubitemid 30644295)
61. Wang, Z., Balet Sindreu, C., Li, V., Nudelman, A., Chan, G. C. and Storm, D. R. (2006) Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J. Neurosci. 26, 7375-7379 (Pubitemid 44315205)
62. Wang, S. C., Lai, H. L., Chiu, Y. T., Ou, R., Huang, C. L. and Chern, Y. (2007) Regulation of type V adenylyl cyclase by Ric8a, a guanine nucleotide exchange factor. Biochem. J. 406, 383-388 (Pubitemid 47425444)
63. Scholich, K., Pierre, S. and Patel, T. B. (2001) Protein associated with Myc (PAM) is a potent inhibitor of adenylyl cyclases. J. Biol. Chem. 276, 47583-47589
64. Salim, S., Sinnarajah, S., Kehrl, J. H. and Dessauer, C. W. (2003) Identification of RGS2 and type V adenylyl cyclase interaction sites. J. Biol. Chem. 278, 15842-15849 (Pubitemid 36799699)
65. Swaney, J. S., Patel, H. H., Yokoyama, U., Head, B. P., Roth, D. M. and Insel, P. A. (2006) Focal adhesions in (myo)fibroblasts scaffold adenylyl cyclase with phosphorylated caveolin. J. Biol. Chem. 281, 17173-17179
66. Schwencke, C., Oka, N., Toya, Y. and Ishikawa, Y. (1997) Isoform-specific interaction of adenylyl cyclase with caveolin. FASEB J. 2, A323 (Pubitemid 127811165)
67. Wu, C. S., Lin, J. T., Chien, C. L., Chang, W. C., Lai, H. L., Chang, C. P. and Chern, Y. (2011) Type VI adenylyl cyclase regulates neurite extension by binding to Snapin and Snap25. Mol. Cell. Biol. 31, 4874-4886
68. Chou, J. L., Huang, C. L., Lai, H. L., Hung, A. C., Chien, C. L., Kao, Y. Y. and Chern, Y. (2004) Regulation of type VI adenylyl cyclase by Snapin, a SNAP25-binding protein. J. Biol. Chem. 279, 46271-46279 (Pubitemid 39491622)
69. Ayling, L. J., Briddon, S. J., Halls, M. L., Hammond, G. R., Vaca, L., Pacheco, J., Hill, S. J. and Cooper, D. M. F. (2012) Adenylyl cyclase AC8 directly controls its micro-environment by recruiting the actin cytoskeleton in a cholesterol-rich milieu. J. Cell Sci. 125, 869-886
70. Fonseca, S. G., Urano, F., Weir, G. C., Gromada, J. and Burcin, M. (2012) Wolfram syndrome 1 and adenylyl cyclase 8 interact at the plasma membrane to regulate insulin production and secretion. Nat. Cell Biol. 14, 1105-1112
71. Crossthwaite, A. J., Ciruela, A., Rayner, T. F. and Cooper, D. M. F. (2006) A direct interaction between the N terminus of adenylyl cyclase AC8 and the catalytic subunit of protein phosphatase 2A. Mol. Pharmacol. 69, 608-617 (Pubitemid 43121958)
72. Herzog, F., Kahraman, A., Boehringer, D., Mak, R., Bracher, A., Walzthoeni, T., Leitner, A., Beck, M., Hartl, F. U., Ban, N. et al. (2012) Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 337, 1348-1352
73. Willoughby, D., Everett, K. L., Halls, M. L., Pacheco, J., Skroblin, P., Vaca, L., Klussmann, E. and Cooper, D. M. F. (2012) Direct binding between Orai1 and AC8 mediates dynamic interplay between Ca2+ and cAMP signaling. Sci. Signal. 5, ra29
74. Smith, K. E., Gu, C., Fagan, K. A., Hu, B. and Cooper, D. M. F. (2002) Residence of adenylyl cyclase type 8 in caveolae is necessary but not sufficient for regulation by capacitative Ca2+ entry. J. Biol. Chem. 277, 6025-6031 (Pubitemid 34968386)
75. Wang, S. C., Lin, J. T. and Chern, Y. (2009) Novel regulation of adenylyl cyclases by direct protein-protein interactions: insights from snapin and ric8a. Neurosignals 17, 169-180
76. Gao, M. H., Tang, T., Lai, N. C., Miyanohara, A., Guo, T., Tang, R., Firth, A. L., Yuan, J. X. and Hammond, H. K. (2011) Beneficial effects of adenylyl cyclase type 6 (AC6) expression persist using a catalytically inactive AC6 mutant. Mol. Pharmacol. 79, 381-388
77. Gao, M. H., Lai, N. C., Tang, T., Guo, T., Tang, R., Chun, B. J., Wang, H., Dalton, N. N., Suarez, J., Dillmann, W. H. and Hammond, H. K. (2013) Preserved cardiac function despite marked impairment of cAMP generation. PLoS ONE 8, e72151
78. Tang, T., Lai, N. C., Hammond, H. K., Roth, D. M., Yang, Y., Guo, T. and Gao, M. H. (2010) Adenylyl cyclase 6 deletion reduces left ventricular hypertrophy, dilation, dysfunction, and fibrosis in pressure-overloaded female mice. J. Am. Coll. Cardiol. 55, 1476-1486
79. Wang, H. and Storm, D. R. (2003) Calmodulin-regulated adenylyl cyclases: cross-talk and plasticity in the central nervous system. Mol. Pharmacol. 63, 463-468 (Pubitemid 36297314)
80. Putney, J. W. (2013) Alternative forms of the store-operated calcium entry mediators, STIM1 and Orai1. Curr. Top. Membr. 71, 109-123
81. Rajendran, L. and Simons, K. (2005) Lipid rafts and membrane dynamics. J. Cell Sci. 118, 1099-1102 (Pubitemid 40528680)
82. Ostrom, R. S. and Insel, P. A. (2004) The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br. J. Pharmacol. 143, 235-245 (Pubitemid 39315143)
83. Owen, D. M., Magenau, A., Williamson, D. and Gaus, K. (2012) The lipid raft hypothesis revisited: new insights on raft composition and function from super-resolution fluorescence microscopy. BioEssays 34, 739-747
84. Janosi, L., Li, Z., Hancock, J. F. and Gorfe, A. A. (2012) Organization, dynamics, and segregation of Ras nanoclusters in membrane domains. Proc. Natl. Acad. Sci. U.S.A. 109, 8097-8102
85. Foster, L. J., De Hoog, C. L. and Mann, M. (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. U.S.A. 100, 5813-5818 (Pubitemid 36576890)
86. Simons, K. and Toomre, D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39
87. Jacobson, K., Mouritsen, O. G. and Anderson, R. G. (2007) Lipid rafts: at a crossroad between cell biology and physics. Nat. Cell Biol. 9, 7-14 (Pubitemid 46024188)
88. Patel, H. H., Murray, F. and Insel, P. A. (2008) Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu. Rev. Pharmacol. Toxicol. 48, 359-391 (Pubitemid 351738158)
89. Cooper, D. M. F. and Crossthwaite, A. J. (2006) Higher-order organization and regulation of adenylyl cyclases. Trends Pharmacol. Sci. 27, 426-431 (Pubitemid 44069584)
90. Head, B. P., Patel, H. H., Roth, D. M., Murray, F., Swaney, J. S., Niesman, I. R., Farquhar, M. G. and Insel, P. A. (2006) Microtubules and actin microfilaments regulate lipid raft/caveolae localization of adenylyl cyclase signaling components. J. Biol. Chem. 281, 26391-26399 (Pubitemid 44401847)
91. Pagano, M., Clynes, M. A., Masada, N., Ciruela, A., Ayling, L. J., Wachten, S. and Cooper, D. M. F. (2009) Insights into the residence in lipid rafts of adenylyl cyclase AC8 and its regulation by capacitative calcium entry. Am. J. Physiol. Cell Physiol. 296, C607-C619
92. Crossthwaite, A. J., Seebacher, T., Masada, N., Ciruela, A., Dufraux, K., Schultz, J. E. and Cooper, D. M. F. (2005) The cytosolic domains of Ca2+ -sensitive adenylyl cyclases dictate their targeting to plasma membrane lipid rafts. J. Biol. Chem. 280, 6380-6391 (Pubitemid 40341184)
93. Thangavel, M., Liu, X., Sun, S. Q., Kaminsky, J. and Ostrom, R. S. (2009) The C1 and C2 domains target human type 6 adenylyl cyclase to lipid rafts and caveolae. Cell. Signal. 21, 301-308
94. Delint-Ramirez, I., Willoughby, D., Hammond, G. V., Ayling, L. J. and Cooper, D. M. F. (2011) Palmitoylation targets AKAP79 protein to lipid rafts and promotes its regulation of calcium-sensitive adenylyl cyclase type 8. J. Biol. Chem. 286, 32962-32975
95. Keith, D. J., Sanderson, J. L., Gibson, E. S., Woolfrey, K. M., Robertson, H. R., Olszewski, K., Kang, R., El-Husseini, A. and Dell'acqua, M. L. (2012) Palmitoylation of A-kinase anchoring protein 79/150 regulates dendritic endosomal targeting and synaptic plasticity mechanisms. J. Neurosci. 32, 7119-7136
96. Pani, B., Ong, H. L., Liu, X., Rauser, K., Ambudkar, I. S. and Singh, B. B. (2008) Lipid rafts determine clustering of STIM1 in endoplasmic reticulum-plasma membrane junctions and regulation of store-operated Ca2+ entry (SOCE). J. Biol. Chem. 283, 17333-17340
97. Martin, A. C., Willoughby, D., Ciruela, A., Ayling, L. J., Pagano, M., Wachten, S., Tengholm, A. and Cooper, D. M. F. (2009) Capacitative Ca2+ entry via Orai1 and stromal interacting molecule 1 (STIM1) regulates adenylyl cyclase type 8. Mol. Pharmacol. 75, 830-842
98. Brady, J. D., Rich, T. C., Le, X., Stafford, K., Fowler, C. J., Lynch, L., Karpen, J. W., Brown, R. L. and Martens, J. R. (2004) Functional role of lipid raft microdomains in cyclic nucleotide-gated channel activation. Mol. Pharmacol. 65, 503-511 (Pubitemid 38264017)
99. Balijepalli, R. C., Foell, J. D., Hall, D. D., Hell, J. W. and Kamp, T. J. (2006) Localization of cardiac L-type Ca2+ channels to a caveolar macromolecular signaling complex is required for 2-adrenergic regulation. Proc. Natl. Acad. Sci. U.S.A. 103, 7500-7505 (Pubitemid 43727862)
100. Parton, R. G. and del Pozo, M. A. (2013) Caveolae as plasma membrane sensors, protectors and organizers. Nat. Rev. Mol. Cell Biol. 14, 98-112
101. Helms, J. B. and Zurzolo, C. (2004) Lipids as targeting signals: lipid rafts and intracellular trafficking. Traffic 5, 247-254 (Pubitemid 38455748)
102. Simons, K. and Ehehalt, R. (2002) Cholesterol, lipid rafts, and disease. J. Clin. Invest. 110, 597-603 (Pubitemid 34988781)
103. Ikonen, E. (2001) Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13, 470-477 (Pubitemid 32709771)
104. Ikonen, E. and Simons, K. (1998) Protein and lipid sorting from the trans-Golgi network to the plasma membrane in polarized cells. Semin. Cell Dev. Biol. 9, 503-509 (Pubitemid 128353015)
105. Mundy, D. I., Machleidt, T., Ying, Y. S., Anderson, R. G. and Bloom, G. S. (2002) Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J. Cell Sci. 115, 4327-4339 (Pubitemid 35460703)
106. Kusumi, A. and Sako, Y. (1996) Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8, 566-574 (Pubitemid 26254055)
107. Muriel, O., Echarri, A., Hellriegel, C., Pavon, D. M., Beccari, L. and Del Pozo, M. A. (2011) Phosphorylated filamin A regulates actin-linked caveolae dynamics. J. Cell Sci. 124, 2763-2776
108. Sayner, S. L., Balczon, R., Frank, D. W., Cooper, D. M. F. and Stevens, T. (2011) Filamin A is a phosphorylation target of membrane but not cytosolic adenylyl cyclase activity. Am. J. Physiol. Lung Cell. Mol. Physiol. 301, L117-L124
109. Rybin, V. O., Xu, X., Lisanti, M. P. and Steinberg, S. F. (2000) Differential targeting of -adrenergic receptor subtypes and adenylyl cyclase to cardiomyocyte caveolae: a mechanism to functionally regulate the cAMP signaling pathway. J. Biol. Chem. 275, 41447-41457 (Pubitemid 32054981)
110. Gabay, M., Pinter, M. E., Wright, F. A., Chan, P., Murphy, A. J., Valenzuela, D. M., Yancopoulos, G. D. and Tall, G. G. (2011) Ric-8 proteins are molecular chaperones that direct nascent G protein subunit membrane association. Sci. Signal. 4, ra79
111. Ye, X. and Cai, Q. (2014) Snapin-mediated BACE1 retrograde transport is essential for its degradation in lysosomes and regulation of APP processing in neurons. Cell Rep. 6, 24-31
112. Feron, O., Michel, J. B., Sase, K. and Michel, T. (1998) Dynamic regulation of endothelial nitric oxide synthase: complementary roles of dual acylation and caveolin interactions. Biochemistry 37, 193-200 (Pubitemid 28049121)
113. Collins, B. M., Davis, M. J., Hancock, J. F. and Parton, R. G. (2012) Structure-based reassessment of the caveolin signaling model: do caveolae regulate signaling through caveolin-protein interactions? Dev. Cell 23, 11-20
114. Byrne, D. P., Dart, C. and Rigden, D. J. (2012) Evaluating caveolin interactions: do proteins interact with the caveolin scaffolding domain through a widespread aromatic residue-rich motif? PLoS ONE 7, e44879
115. Ostrom, R. S., Bundey, R. A. and Insel, P. A. (2004) Nitric oxide inhibition of adenylyl cyclase type 6 activity is dependent upon lipid rafts and caveolin signaling complexes. J. Biol. Chem. 279, 19846-19853 (Pubitemid 38623425)
116. Gu, C., Cali, J. J. and Cooper, D. M. F. (2002) Dimerization of mammalian adenylate cyclases. Eur. J. Biochem. 269, 413-421
117. Gu, C., Sorkin, A. and Cooper, D. M. F. (2001) Persistent interactions between the two transmembrane clusters dictate the targeting and functional assembly of adenylyl cyclase. Curr. Biol. 11, 185-190 (Pubitemid 32152104)
118. Wehrle-Haller, B. (2012) Assembly and disassembly of cell matrix adhesions. Curr. Opin. Cell Biol. 24, 569-581
119. Howe, A. K. (2011) Cross-talk between calcium and protein kinase A in the regulation of cell migration. Curr. Opin. Cell Biol. 23, 554-561
120. Tojima, T., Hines, J. H., Henley, J. R. and Kamiguchi, H. (2011) Second messengers and membrane trafficking direct and organize growth cone steering. Nat. Rev. Neurosci. 12, 191-203
121. Norambuena, A. and Schwartz, M. A. (2011) Effects of integrin-mediated cell adhesion on plasma membrane lipid raft components and signaling. Mol. Biol. Cell 22, 3456-3464
122. Logue, J. S., Whiting, J. L., Tunquist, B., Sacks, D. B., Langeberg, L. K., Wordeman, L. and Scott, J. D. (2011) AKAP220 protein organizes signaling elements that impact cell migration. J. Biol. Chem. 286, 39269-39281
123. Schafer, C., Rymarczyk, G., Ding, L., Kirber, M. T. and Bolotina, V. M. (2012) Role of molecular determinants of store-operated Ca2+ entry (Orai1, phospholipase A2 group 6, and STIM1) in focal adhesion formation and cell migration. J. Biol. Chem. 287, 40745-40757
124. 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
125. Geiger, B., Spatz, J. P. and Bershadsky, A. D. (2009) Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10, 21-33
126. Harburger, D. S. and Calderwood, D. A. (2009) Integrin signalling at a glance. J. Cell Sci. 122, 159-163
127. Giannone, G., Ronde, P., Gaire, M., Beaudouin, J., Haiech, J., Ellenberg, J. and Takeda, K. (2004) Calcium rises locally trigger focal adhesion disassembly and enhance residency of focal adhesion kinase at focal adhesions. J. Biol. Chem. 279, 28715-28723 (Pubitemid 38900156)
128. Howe, A. K. (2004) Regulation of actin-based cell migration by cAMP/PKA. Biochim. Biophys. Acta 1692, 159-174 (Pubitemid 38891772)
129. Houslay, M. D. and Milligan, G. (1997) Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem. Sci. 22, 217-224 (Pubitemid 27246638)
130. Calebiro, D., Nikolaev, V. O., Gagliani, M. C., de Filippis, T., Dees, C., Tacchetti, C., Persani, L. and Lohse, M. J. (2009) Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol. 7, e1000172
131. Neumann, S., Geras-Raaka, E., Marcus-Samuels, B. and Gershengorn, M. C. (2010) Persistent cAMP signaling by thyrotropin (TSH) receptors is not dependent on internalization. FASEB J. 24, 3992-3999
132. De Arcangelis, V., Liu, S., Zhang, D., Soto, D. and Xiang, Y. K. (2010) Equilibrium between adenylyl cyclase and phosphodiesterase patterns adrenergic agonist dose-dependent spatiotemporal cAMP/protein kinase A activities in cardiomyocytes. Mol. Pharmacol. 78, 340-349
133. Garbers, D. L. (1981) The elevation of cyclic AMP concentrations in flagella-less sea urchin sperm heads. J. Biol. Chem. 256, 620-624
134. Stengel, D. and Hanoune, J. (1984) The sperm adenylate cyclase. Ann. N.Y. Acad. Sci. 438, 18-28 (Pubitemid 15243848)
135. Zippin, J. H., Chen, Y., Straub, S. G., Hess, K. C., Diaz, A., Lee, D., Tso, P., Holz, G. G., Sharp, G. W., Levin, L. R. and Buck, J. (2013) CO2/HCO3 - and calcium-regulated soluble adenylyl cyclase as a physiological ATP sensor. J. Biol. Chem. 288, 33283-33291
136. Esposito, G., Jaiswal, B. S., Xie, F., Krajnc-Franken, M. A., Robben, T. J., Strik, A. M., Kuil, C., Philipsen, R. L., van Duin, M., Conti, M. and Gossen, J. A. (2004) Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc. Natl. Acad. Sci. U.S.A. 101, 2993-2998 (Pubitemid 38332002)
137. Tian, G., Sandler, S., Gylfe, E. and Tengholm, A. (2011) Glucose- and hormone-induced cAMP oscillations in - and cells within intact pancreatic islets. Diabetes 60, 1535-1543
138. Kramer, R. H. (1990) Patch cramming: monitoring intracellular messengers in intact cells with membrane patches containing detector ion channels. Neuron 4, 335-341 (Pubitemid 20155024)
139. Adams, S. R., Harootunian, A. T., Buechler, Y. J., Taylor, S. S. and Tsien, R. Y. (1991) Fluorescence ratio imaging of cyclic AMP in single cells. Nature 349, 694-697 (Pubitemid 21912139)
140. 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)
141. Ponsioen, B., Zhao, J., Riedl, J., Zwartkruis, F., van der Krogt, G., Zaccolo, M., Moolenaar, W. H., Bos, J. L. and Jalink, K. (2004) Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep. 5, 1176-1180 (Pubitemid 40103613)
142. DiPilato, L. M., Cheng, X. and Zhang, J. (2004) Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signaling within discrete subcellular compartments. Proc. Natl. Acad. Sci. U.S.A. 101, 16513-16518 (Pubitemid 39557744)
143. 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 GH3B6 cells. J. Cell Sci. 123, 95-106
144. Buxton, I. L. and Brunton, L. L. (1983) Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes. J. Biol. Chem. 258, 10233-10239 (Pubitemid 14241179)
145. Allbritton, N. L., Meyer, T. and Stryer, L. (1992) Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258, 1812-1815 (Pubitemid 23087352)
146. Tsien, R. Y., Pozzan, T. and Rink, T. J. (1982) Calcium homeostasis in intact lymphocytes: cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator. J. Cell Biol. 94, 325-334 (Pubitemid 12026780)
147. Zaccolo, M. and Pozzan, T. (2002) Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295, 1711-1715 (Pubitemid 34202906)
148. Rich, T. C., Fagan, K. A., Nakata, H., Schaack, J., Cooper, D. M. F. and Karpen, J. W. (2000) Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J. Gen. Physiol. 116, 147-161 (Pubitemid 30637001)
149. Berridge, M. J. and Dupont, G. (1994) Spatial and temporal signalling by calcium. Curr. Opin. Cell Biol. 6, 267-274 (Pubitemid 24109786)
150. Dupont, G., Houart, G. and De Koninck, P. (2003) Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations: a simple model. Cell Calcium 34, 485-497 (Pubitemid 37493346)
151. De Koninck, P. and Schulman, H. (1998) Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279, 227-230 (Pubitemid 28103880)
152. Dolmetsch, R. E., Lewis, R. S., Goodnow, C. C. and Healy, J. I. (1997) Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386, 855-858 (Pubitemid 27181262)
153. Brooker, G. (1973) Oscillation of cyclic adenosine monophosphate concentration during the myocardial contraction cycle. Science 182, 933-934
154. Gorbunova, Y. V. and Spitzer, N. C. (2002) Dynamic interactions of cyclic AMP transients and spontaneous Ca2+ spikes. Nature 418, 93-96 (Pubitemid 34742577)
155. Nicol, X., Hong, K. P. and Spitzer, N. C. (2011) Spatial and temporal second messenger codes for growth cone turning. Proc. Natl. Acad. Sci. U.S.A. 108, 13776-13781
156. Dyachok, O., Isakov, Y., Sagetorp, J. and Tengholm, A. (2006) Oscillations of cyclic AMP in hormone-stimulated insulin-secreting cells. Nature 439, 349-352 (Pubitemid 43128861)
157. Willoughby, D. and Cooper, D. M. F. (2006) Ca2+ stimulation of adenylyl cyclase generates dynamic oscillations in cyclic AMP. J. Cell Sci. 119, 828-836
158. Nicol, X., Voyatzis, S., Muzerelle, A., Narboux-Neme, N., Sudhof, T. C., Miles, R. and Gaspar, P. (2007) cAMP oscillations and retinal activity are permissive for ephrin signaling during the establishment of the retinotopic map. Nat. Neurosci. 10, 340-347
159. Taylor, S. S., Ilouz, R., Zhang, P. and Kornev, A. P. (2013) Assembly of allosteric macromolecular switches: lessons from PKA. Nat. Rev. Mol. Cell Biol. 13, 646-658
160. Pierre, S., Eschenhagen, T., Geisslinger, G. and Scholich, K. (2009) Capturing adenylyl cyclases as potential drug targets. Nat. Rev. Drug Discov. 8, 321-335
161. Brand, C. S., Hocker, H. J., Gorfe, A. A., Cavasotto, C. N. and Dessauer, C. W. (2013) Isoform selectivity of adenylyl cyclase inhibitors: characterization of known and novel compounds. J. Pharmacol. Exp. Ther. 347, 265-275
162. Braeunig, J. H., 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
163. Emery, A. C., Eiden, M. V. and Eiden, L. E. (2013) A new site and mechanism of action for the widely used adenylate cyclase inhibitor SQ22,536. Mol. Pharmacol. 83, 95-105
164. Conley, J. M., Brand, C. S., Bogard, A. S., Pratt, E. P., Xu, R., Hockerman, G. H., Ostrom, R. S., Dessauer, C. W. and Watts, V. J. (2013) Development of a high-throughput screening paradigm for the discovery of small-molecule modulators of adenylyl cyclase: identification of an adenylyl cyclase 2 inhibitor. J. Pharmacol. Exp. Ther. 347, 276-287
165. Esseltine, J. L. and Scott, J. D. (2013) AKAP signaling complexes: pointing towards the next generation of therapeutic targets? Trends Pharmacol. Sci. 34, 648-655
166. Schäfer, G., Milíc, J., Eldahshan, A., Götz, F., Zühlke, K., Schillinger, C., Kreuchwig, A., Elkins, J. M., Abdul Azeez, K. R., Oder, A. et al. (2013) Highly functionalized terpyridines as competitive inhibitors of AKAP-PKA interactions. Angew. Chem. Int. Ed. Engl. 52, 12187-12191
167. Christian, F., Szaszák, M., Friedl, S., Drewianka, S., Lorenz, D., Goncalves, A., Furkert, J., Vargas, C., Schmieder, P., Götz, F. et al. (2012) Small molecule AKAP-protein kinase A (PKA) interaction disruptors that activate PKA interfere with compartmentalized cAMP signaling in cardiac myocytes. J. Biol. Chem. 286, 9079-9096
168. Groc, L., Lafourcade, M., Heine, M., Renner, M., Racine, V., Sibarita, J. B., Lounis, B., Choquet, D. and Cognet, L. (2007) Surface trafficking of neurotransmitter receptor: comparison between single-molecule/quantum dot strategies. J. Neurosci. 27, 12433-12437 (Pubitemid 350127795)
169. Kanchanawong, P., Shtengel, G., Pasapera, A. M., Ramko, E. B., Davidson, M. W., Hess, H. F. and Waterman, C. M. Nanoscale architecture of integrin-based cell adhesions. Nature 468, 580-584
170. Brameshuber, M. and Schutz, G. J. Detection and quantification of biomolecular association in living cells using single-molecule microscopy. Methods Enzymol. 505, 159-186
171. Dunn, T. A., Wang, C. T., Colicos, M. A., Zaccolo, M., DiPilato, L. M., Zhang, J., Tsien, R. Y. and Feller, M. B. (2006) Imaging of cAMP levels and protein kinase A activity reveals that retinal waves drive oscillations in second-messenger cascades. J. Neurosci. 26, 12807-12815 (Pubitemid 44904576)
172. Zhang, J., Bal, M., Bierbower, S., Zaika, O. and Shapiro, M. S. (2011) AKAP79/150 signal complexes in G-protein modulation of neuronal ion channels. J. Neurosci. 31, 7199-7211