CAMP signal transduction in the heart: Understanding spatial control for the development of novel therapeutic strategies

British Journal of Pharmacology

Volumn 158, Issue 1, 2009, Pages 50-60

  Zaccolo, Manuela ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

A kinase anchoring proteins; CAMP; Compartmentalization; G protein coupled receptors; Heart failure; Live imaging; Phosphodiesterases; Protein kinase A; Signalling

Indexed keywords

CYCLIC AMP; NEUROTRANSMITTER;

CATECHOLAMINERGIC SYSTEM; HEART; HEART MUSCLE CONTRACTILITY; HEART RATE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOVASCULAR AGENTS; CARDIOVASCULAR DISEASES; CYCLIC AMP; DRUG DISCOVERY; HEART; HUMANS; MYOCARDIUM; MYOCYTES, CARDIAC; SIGNAL TRANSDUCTION;

EID: 69249211018     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2009.00185.x     Document Type: Review

References (119)

1. Alexander SP, Mathie A, Peters JA (2008). Guide to Receptors and Channels (GRAC), 3rd edn. Br J Pharmacol 153 (Suppl. 2 S1 S209.
2. Angelo R, Rubin CS (1998). Molecular characterization of an anchor protein (AKAPCE) that binds the RI subunit (RCE) of type I protein kinase A from Caenorhabditis elegans. J Biol Chem 273 : 14633 14643.
3. Bacskai BJ, Hochner B, Mahaut-Smith M, Adams SR, Kaang BK, Kandel ER et al. (1993). Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science 260 : 222 226.
4. Baillie GS, Sood A, McPhee I, Gall I, Perry SJ, Lefkowitz RJ et al. (2003). beta-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc Natl Acad Sci USA 100 : 940 945.
5. Baillie GS, Scott JD, Houslay MD (2005). Compartmentalisation of phosphodiesterases and protein kinase A: opposites attract. FEBS Lett 579 : 3264 3270.
6. Balijepalli RC, Foell JD, Hall DD, Hell JW, Kamp TJ (2006). Localization of cardiac L-type Ca(2+) channels to a caveolar macromolecular signaling complex is required for beta(2)-adrenergic regulation. Proc Natl Acad Sci USA 103 : 7500 7505.
7. Barnes AP, Livera G, Huang P, Sun C, O'Neal WK, Conti M et al. (2005). Phosphodiesterase 4D forms a cAMP diffusion barrier at the apical membrane of the airway epithelium. J Biol Chem 280 : 7997 8003.
8. Barradeau S, Imaizumi-Scherrer T, Weiss MC, Faust DM (2000). Alternative 5′-exons of the mouse cAMP-dependent protein kinase subunit RIalpha gene are conserved and expressed in both a ubiquitous and tissue-restricted fashion. FEBS Lett 476 : 272 276.
9. Beene DL, Scott JD (2007). A-kinase anchoring proteins take shape. Curr Opin Cell Biol 19 : 192 198.
10. Bers DM (2008). Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol 70 : 23 49.
11. Bhatnagar A, Sheffler DJ, Kroeze WK, Compton-Toth B, Roth BL (2004). Caveolin-1 interacts with 5-HT2A serotonin receptors and profoundly modulates the signaling of selected Galphaq-coupled protein receptors. J Biol Chem 279 : 34614 34623.
12. Brandon EP, Zhuo M, Huang YY, Qi M, Gerhold KA, Burton KA et al. (1995). Hippocampal long-term depression and depotentiation are defective in mice carrying a targeted disruption of the gene encoding the RI beta subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 92 : 8851 8855.
13. Brazer SC, Singh BB, Liu X, Swaim W, Ambudkar IS (2003). Caveolin-1 contributes to assembly of store-operated Ca2+ influx channels by regulating plasma membrane localization of TRPC1. J Biol Chem 278 : 27208 27215.
14. Brunton LL, Hayes JS, Mayer SE (1979). Hormonally specific phosphorylation of cardiac troponin I and activation of glycogen phosphorylase. Nature 280 : 78 80.
15. Carlisle Michel JJ, Dodge KL, Wong W, Mayer NC, Langeberg LK, Scott JD (2004). PKA-phosphorylation of PDE4D3 facilitates recruitment of the mAKAP signalling complex. Biochem J 381 : 587 592.
16. Carr DW, Hausken ZE, Fraser ID, Stofko-Hahn RE, Scott JD (1992). Association of the type II cAMP-dependent protein kinase with a human thyroid RII-anchoring protein. Cloning and characterization of the RII-binding domain. J Biol Chem 267 : 13376 13382.
17. Chen C, Nakamura T, Koutalos Y (1999). Cyclic AMP diffusion coefficient in frog olfactory cilia. Biophys J 76 : 2861 2867.
18. Chiono M, Mahey R, Tate G, Cooper DM (1995). Capacitative Ca2+ entry exclusively inhibits cAMP synthesis in C6-2B glioma cells. Evidence that physiologically evoked Ca2+ entry regulates Ca(2+)-inhibitable adenylyl cyclase in non-excitable cells. J Biol Chem 270 : 1149 1155.
19. Coghlan VM, Hausken ZE, Scott JD (1995). Subcellular targeting of kinases and phosphatases by association with bifunctional anchoring proteins. Biochem Soc Trans 23 : 592 596.
20. Conti M, Beavo J (2007). Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76 : 481 511.
21. Corbin JD, Sugden PH, Lincoln TM, Keely SL (1977). Compartmentalization of adenosine 3′:5′-monophosphate and adenosine 3′:5′- monophosphate-dependent protein kinase in heart tissue. J Biol Chem 252 : 3854 3861.
22. Cuello F, Bardswell SC, Haworth RS, Yin X, Lutz S, Wieland T et al. (2007). Protein kinase D selectively targets cardiac troponin I and regulates myofilament Ca2+ sensitivity in ventricular myocytes. Circ Res 100 : 864 873.
23. Cummings DE, Brandon EP, Planas JV, Motamed K, Idzerda RL, McKnight GS (1996). Genetically lean mice result from targeted disruption of the RII beta subunit of protein kinase A. Nature 382 : 622 626.
24. Defer N, Best-Belpomme M, Hanoune J (2000). Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. Am J Physiol Renal Physiol 279 : F400 416.
25. Dell'Acqua ML, Faux MC, Thorburn J, Thorburn A, Scott JD (1998). Membrane-targeting sequences on AKAP79 bind phosphatidylinositol-4, 5-bisphosphate. Embo J 17 : 2246 2260.
26. Di Benedetto G, Zoccarato A, Lissandron V, Terrin A, Li X, Houslay MD et al. (2008). Protein kinase A type I and type II define distinct intracellular signaling compartments. Circ Res 103 : 836 844.
27. DiPilato LM, Cheng X, Zhang J (2004). Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signalling within discrete subcellular compartments. Proc Natl Acad Sci USA 101 : 16513 16518.
28. Diviani D (2008). Modulation of cardiac function by A-kinase anchoring proteins. Curr Opin Pharmacol 8 : 166 173.
29. Dodge-Kafka KL, Soughayer J, Pare GC, Carlisle Michel JJ, Langeberg LK, Kapiloff MS et al. (2005). The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature 437 : 574 578.
30. Dodge KL, Khouangsathiene S, Kapiloff MS, Mouton R, Hill EV, Houslay MD et al. (2001). mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. Embo J 20 : 1921 1930.
31. Domanski MJ, Krause-Steinrauf H, Massie BM, Deedwania P, Follmann D, Kovar D et al. (2003). A comparative analysis of the results from 4 trials of beta-blocker therapy for heart failure: BEST, CIBIS-II, MERIT-HF, and COPERNICUS. J Card Fail 9 : 354 363.
32. Dostmann WR, Taylor SS, Genieser HG, Jastorff B, Doskeland SO, Ogreid D (1990). Probing the cyclic nucleotide binding sites of cAMP-dependent protein kinases I and II with analogs of adenosine 3′,5′-cyclic phosphorothioates. J Biol Chem 265 : 10484 10491.
33. Fischmeister R, Castro LR, Abi-Gerges A, Rochais F, Jurevicius J, Leroy J et al. (2006). Compartmentation of cyclic nucleotide signaling in the heart: the role of cyclic nucleotide phosphodiesterases. Circ Res 99 : 816 828.
34. Floras JS (2003). Sympathetic activation in human heart failure: diverse mechanisms, therapeutic opportunities. Acta Physiol Scand 177 : 391 398.
35. Fodstad H, Swan H, Laitinen P, Piippo K, Paavonen K, Viitasalo M et al. (2004). Four potassium channel mutations account for 73% of the genetic spectrum underlying long-QT syndrome (LQTS) and provide evidence for a strong founder effect in Finland. Ann Med 36 (Suppl. 1 53 63.
36. Förster T (1948). Intermolecular energy migration and fluorescence. Annals of Physics 2 : 55 57.
37. Francis SH, Corbin JD (1994). Structure and function of cyclic nucleotide-dependent protein kinases. Annu Rev Physiol 56 : 237 272.
38. Gardner LA, Tavalin SJ, Goehring AS, Scott JD, Bahouth SW (2006). AKAP79-mediated targeting of the cyclic AMP-dependent protein kinase to the beta1-adrenergic receptor promotes recycling and functional resensitization of the receptor. J Biol Chem 281 : 33537 33553.
39. Gold MG, Lygren B, Dokurno P, Hoshi N, McConnachie G, Tasken K et al. (2006). Molecular basis of AKAP specificity for PKA regulatory subunits. Mol Cell 24 : 383 395.
40. Gray PC, Johnson BD, Westenbroek RE, Hays LG, Yates JR 3rd., Scheuer T et al. (1998). Primary structure and function of an A kinase anchoring protein associated with calcium channels. Neuron 20 : 1017 1026.
41. Haworth RS, Roberts NA, Cuello F, Avkiran M (2007). Regulation of protein kinase D activity in adult myocardium: novel counter-regulatory roles for protein kinase Cepsilon and protein kinase A. J Mol Cell Cardiol 43 : 686 695.
42. Hayes JS, Brunton LL (1982). Functional compartments in cyclic nucleotide action. J Cyclic Nucleotide Res 8 : 1 16.
43. Hayes JS, Brunton LL, Brown JH, Reese JB, Mayer SE (1979). Hormonally specific expression of cardiac protein kinase activity. Proc Natl Acad Sci USA 76 : 1570 1574.
44. Hayes JS, Brunton LL, Mayer SE (1980). Selective activation of particulate cAMP-dependent protein kinase by isoproterenol and prostaglandin E1. J Biol Chem 255 : 5113 5119.
45. Head BP, Patel HH, Roth DM, Lai NC, Niesman IR, Farquhar MG et al. (2005). G-protein-coupled receptor signaling components localize in both sarcolemmal and intracellular caveolin-3-associated microdomains in adult cardiac myocytes. J Biol Chem 280 : 31036 31044.
46. Hensch TK, Gordon JA, Brandon EP, McKnight GS, Idzerda RL, Stryker MP (1998). Comparison of plasticity in vivo and in vitro in the developing visual cortex of normal and protein kinase A RIbeta-deficient mice. J Neurosci 18 : 2108 2117.
47. Hohl CM, Li QA (1991). Compartmentation of cAMP in adult canine ventricular myocytes. Relation to single-cell free Ca2+ transients. Circ Res 69 : 1369 1379.
48. Huang LJ, Durick K, Weiner JA, Chun J, Taylor SS (1997). Identification of a novel protein kinase A anchoring protein that binds both type I and type II regulatory subunits. J Biol Chem 272 : 8057 8064.
49. Hulme JT, Lin TW, Westenbroek RE, Scheuer T, Catterall WA (2003). Beta-adrenergic regulation requires direct anchoring of PKA to cardiac CaV1.2 channels via a leucine zipper interaction with A kinase-anchoring protein 15. Proc Natl Acad Sci USA 100 : 13093 13098.
50. Hulme JT, Westenbroek RE, Scheuer T, Catterall WA (2006). Phosphorylation of serine 1928 in the distal C-terminal domain of cardiac CaV1.2 channels during beta1-adrenergic regulation. Proc Natl Acad Sci USA 103 : 16574 16579.
51. Imaizumi-Scherrer T, Faust DM, Benichou JC, Hellio R, Weiss MC (1996). Accumulation in fetal muscle and localization to the neuromuscular junction of cAMP-dependent protein kinase A regulatory and catalytic subunits RI alpha and C alpha. J Cell Biol 134 : 1241 1254.
52. Imaizumi-Scherrer T, Faust DM, Barradeau S, Hellio R, Weiss MC (2001). Type I protein kinase a is localized to interphase microtubules and strongly associated with the mitotic spindle. Exp Cell Res 264 : 250 265.
53. Iwatsubo K, Minamisawa S, Tsunematsu T, Nakagome M, Toya Y, Tomlinson JE et al. (2004). Direct inhibition of type 5 adenylyl cyclase prevents myocardial apoptosis without functional deterioration. J Biol Chem 279 : 40938 40945.
54. Jurevicius J, Fischmeister R (1996). cAMP compartmentation is responsible for a local activation of cardiac Ca2+ channels by beta-adrenergic agonists. Proc Natl Acad Sci USA 93 : 295 299.
55. Kapiloff MS, Jackson N, Airhart N (2001). mAKAP and the ryanodine receptor are part of a multi-component signaling complex on the cardiomyocyte nuclear envelope. J Cell Sci 114 : 3167 3176.
56. Kaye DM, Smirk B, Finch S, Williams C, Esler MD (2004). Interaction between cardiac sympathetic drive and heart rate in heart failure: modulation by adrenergic receptor genotype. J Am Coll Cardiol 44 : 2008 2015.
57. Keely SL (1977). Activation of cAMP-dependent protein kinase without a corresponding increase in phosphorylase activity. Res Commun Chem Pathol Pharmacol 18 : 283 290.
58. Khac LD, Harbon S, Clauser HJ (1973). Intracellular titration of cyclic AMP bound to receptor proteins and correlation with cyclic-AMP levels in the surviving rat diaphragm. Eur J Biochem 40 : 177 185.
59. Kim C, Cheng CY, Saldanha SA, Taylor SS (2007). PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation. Cell 130 : 1032 1043.
60. Kinderman FS, Kim C, von Daake S, Ma Y, Pham BQ, Spraggon G et al. (2006). A dynamic mechanism for AKAP binding to RII isoforms of cAMP-dependent protein kinase. Mol Cell 24 : 397 408.
61. Kuschel M, Zhou YY, Spurgeon HA, Bartel S, Karczewski P, Zhang SJ et al. (1999). beta2-adrenergic cAMP signaling is uncoupled from phosphorylation of cytoplasmic proteins in canine heart. Circulation 99 : 2458 2465.
62. Lai NC, Roth DM, Gao MH, Fine S, Head BP, Zhu J et al. (2000). Intracoronary delivery of adenovirus encoding adenylyl cyclase VI increases left ventricular function and cAMP-generating capacity. Circulation 102 : 2396 2401.
63. Lefkowitz RJ, Rockman HA, Koch WJ (2000). Catecholamines, cardiac beta-adrenergic receptors, and heart failure. Circulation 101 : 1634 1637.
64. Lugnier C (2006). Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol Ther 109 : 366 398.
65. Lygren B, Carlson CR, Santamaria K, Lissandron V, McSorley T, Litzenberg J et al. (2007). AKAP complex regulates Ca2+ re-uptake into heart sarcoplasmic reticulum. EMBO Rep 8 : 1061 1067.
66. Lynch MJ, Hill EV, Houslay MD (2006). Intracellular targeting of phosphodiesterase-4 underpins compartmentalized cAMP signaling. Curr Top Dev Biol 75 : 225 259.
67. MacKenzie SJ, Baillie GS, McPhee I, MacKenzie C, Seamons R, McSorley T et al. (2002). Long PDE4 cAMP specific phosphodiesterases are activated by protein kinase A-mediated phosphorylation of a single serine residue in Upstream Conserved Region 1 (UCR1). Br J Pharmacol 136 : 421 433.
68. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N et al. (2000). PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101 : 365 376.
69. Marx SO, Kurokawa J, Reiken S, Motoike H, D'Armiento J, Marks AR et al. (2002). Requirement of a macromolecular signaling complex for beta adrenergic receptor modulation of the KCNQ1-KCNE1 potassium channel. Science 295 : 496 499.
70. Mongillo M, McSorley T, Evellin S, Sood A, Lissandron V, Terrin A et al. (2004). Fluorescence resonance energy transfer-based analysis of cAMP dynamics in live neonatal rat cardiac myocytes reveals distinct functions of compartmentalized phosphodiesterases. Circ Res 95 : 67 75.
71. Mongillo M, Tocchetti CG, Terrin A, Lissandron V, Cheung YF, Dostmann WR et al. (2006). Compartmentalized phosphodiesterase-2 activity blunts beta-adrenergic cardiac inotropy via an NO/cGMP-dependent pathway. Circ Res 98 : 226 234.
72. Muller FU, Boknik P, Knapp J, Linck B, Luss H, Neumann J et al. (2001). Activation and inactivation of cAMP-response element-mediated gene transcription in cardiac myocytes. Cardiovasc Res 52 : 95 102.
73. Newlon MG, Roy M, Morikis D, Hausken ZE, Coghlan V, Scott JD et al. (1999). The molecular basis for protein kinase A anchoring revealed by solution NMR. Nat Struct Biol 6 : 222 227.
74. Nikolaev VO, Bunemann M, Schmitteckert E, Lohse MJ, Engelhardt S (2006). Cyclic AMP imaging in adult cardiac myocytes reveals far-reaching beta1-adrenergic but locally confined beta2-adrenergic receptor-mediated signaling. Circ Res 99 : 1084 1091.
75. Okumura S, Takagi G, Kawabe J, Yang G, Lee MC, Hong C et al. (2003). Disruption of type 5 adenylyl cyclase gene preserves cardiac function against pressure overload. Proc Natl Acad Sci USA 100 : 9986 9990.
76. Ostrom RS, Violin JD, Coleman S, Insel PA (2000). Selective enhancement of beta-adrenergic receptor signaling by overexpression of adenylyl cyclase type 6: colocalization of receptor and adenylyl cyclase in caveolae of cardiac myocytes. Mol Pharmacol 57 : 1075 1079.
77. Ostrom RS, Gregorian C, Drenan RM, Xiang Y, Regan JW, Insel PA (2001). Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J Biol Chem 276 : 42063 42069.
78. Ostrom RS, Bundey RA, Insel PA (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.
79. Pare GC, Bauman AL, McHenry M, Michel JJ, Dodge-Kafka KL, Kapiloff MS (2005a). The mAKAP complex participates in the induction of cardiac myocyte hypertrophy by adrenergic receptor signaling. J Cell Sci 118 : 5637 5646.
80. Pare GC, Easlick JL, Mislow JM, McNally EM, Kapiloff MS (2005b). Nesprin-1alpha contributes to the targeting of mAKAP to the cardiac myocyte nuclear envelope. Exp Cell Res 303 : 388 399.
81. Patel HH, Murray F, Insel PA (2008). G-protein-coupled receptor-signaling components in membrane raft and caveolae microdomains. Handb Exp Pharmacol 167 184.
82. Penela P, Ribas C, Mayor F Jr. (2003). Mechanisms of regulation of the expression and function of G protein-coupled receptor kinases. Cell Signal 15 : 973 981.
83. Port JD, Bristow MR (2001). Altered beta-adrenergic receptor gene regulation and signaling in chronic heart failure. J Mol Cell Cardiol 33 : 887 905.
84. Puceat M, Bony C, Jaconi M, Vassort G (1998). Specific activation of adenylyl cyclase V by a purinergic agonist. FEBS Lett 431 : 189 194.
85. Putney JW (2005). Physiological mechanisms of TRPC activation. Pflugers Arch 451 : 29 34.
86. Rich TC, Fagan KA, Nakata H, Schaack J, Cooper DM, Karpen JW (2000). Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J Gen Physiol 116 : 147 161.
87. Rich TC, Fagan KA, Tse TE, Schaack J, Cooper DM, Karpen JW (2001). A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc Natl Acad Sci USA 98 : 13049 13054.
88. Rochais F, Abi-Gerges A, Horner K, Lefebvre F, Cooper DM, Conti M et al. (2006). A specific pattern of phosphodiesterases controls the cAMP signals generated by different Gs-coupled receptors in adult rat ventricular myocytes. Circ Res 98 : 1081 1088.
89. Roth DM, Bayat H, Drumm JD, Gao MH, Swaney JS, Ander A et al. (2002). Adenylyl cyclase increases survival in cardiomyopathy. Circulation 105 : 1989 1994.
90. Ruehr ML, Russell MA, Bond M (2004). A-kinase anchoring protein targeting of protein kinase A in the heart. J Mol Cell Cardiol 37 : 653 665.
91. Rybin VO, Xu X, Lisanti MP, Steinberg SF (2000). Differential targeting of beta-adrenergic receptor subtypes and adenylyl cyclase to cardiomyocyte caveolae. A mechanism to functionally regulate the cAMP signaling pathway. J Biol Chem 275 : 41447 41457.
92. Saucerman JJ, Zhang J, Martin JC, Peng LX, Stenbit AE, Tsien RY et al. (2006). Systems analysis of PKA-mediated phosphorylation gradients in live cardiac myocytes. Proc Natl Acad Sci USA 103 : 12923 12928.
93. Schillace RV, Scott JD (1999). Association of the type 1 protein phosphatase PP1 with the A-kinase anchoring protein AKAP220. Curr Biol 9 : 321 324.
94. Sette C, Conti M (1996). Phosphorylation and activation of a cAMP-specific phosphodiesterase by the cAMP-dependent protein kinase. Involvement of serine 54 in the enzyme activation. J Biol Chem 271 : 16526 16534.
95. Shih M, Lin F, Scott JD, Wang HY, Malbon CC (1999). Dynamic complexes of beta2-adrenergic receptors with protein kinases and phosphatases and the role of gravin. J Biol Chem 274 : 1588 1595.
96. Skalhegg BS, Tasken K (2000). Specificity in the cAMP/PKA signaling pathway. Differential expression,regulation, and subcellular localization of subunits of PKA. Front Biosci 5 : D678 D693.
97. Skalhegg BS, Tasken K, Hansson V, Huitfeldt HS, Jahnsen T, Lea T (1994). Location of cAMP-dependent protein kinase type I with the TCR-CD3 complex. Science 263 : 84 87.
98. Stokka AJ, Gesellchen F, Carlson CR, Scott JD, Herberg FW, Tasken K (2006). Characterization of A-kinase-anchoring disruptors using a solution-based assay. Biochem J 400 : 493 499.
99. Tang T, Gao MH, Roth DM, Guo T, Hammond HK (2004). Adenylyl cyclase type VI corrects cardiac sarcoplasmic reticulum calcium uptake defects in cardiomyopathy. Am J Physiol Heart Circ Physiol 287 : H1906 H1912.
100. Tasken KA, Collas P, Kemmner WA, Witczak O, Conti M, Tasken K (2001). Phosphodiesterase 4D and protein kinase a type II constitute a signaling unit in the centrosomal area. J Biol Chem 276 : 21999 22002.
101. Taylor SS, Knighton DR, Zheng J, Ten Eyck LF, Sowadski JM (1992). Structural framework for the protein kinase family. Annu Rev Cell Biol 8 : 429 462.
102. Taylor SS, Kim C, Cheng CY, Brown SH, Wu J, Kannan N (2008). Signaling through cAMP and cAMP-dependent protein kinase: diverse strategies for drug design. Biochim Biophys Acta 1784 : 16 26.
103. Terasaki WL, Brooker G (1977). Cardiac adenosine 3′:5′- monophosphate. Free and bound forms in the isolated rat atrium. J Biol Chem 252 : 1041 1050.
104. Terrin A, Di Benedetto G, Pertegato V, Cheung YF, Baillie G, Lynch MJ et al. (2006). PGE(1) stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: role of compartmentalized phosphodiesterases. J Cell Biol 175 : 441 451.
105. Tingley WG, Pawlikowska L, Zaroff JG, Kim T, Nguyen T, Young SG et al. (2007). Gene-trapped mouse embryonic stem cell-derived cardiac myocytes and human genetics implicate AKAP10 in heart rhythm regulation. Proc Natl Acad Sci USA 104 : 8461 8466.
106. Trotter KW, Fraser ID, Scott GK, Stutts MJ, Scott JD, Milgram SL (1999). Alternative splicing regulates the subcellular localization of A-kinase anchoring protein 18 isoforms. J Cell Biol 147 : 1481 1492.
107. Vega RB, Harrison BC, Meadows E, Roberts CR, Papst PJ, Olson EN et al. (2004). Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol Cell Biol 24 : 8374 8385.
108. Vila Petroff MG, Egan JM, Wang X, Sollott SJ (2001). Glucagon-like peptide-1 increases cAMP but fails to augment contraction in adult rat cardiac myocytes. Circ Res 89 : 445 452.
109. Willoughby D, Cooper DM (2007). Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol Rev 87 : 965 1010.
110. Willoughby D, Masada N, Crossthwaite AJ, Ciruela A, Cooper DM (2005). Localized Na+/H+ exchanger 1 expression protects Ca2+-regulated adenylyl cyclases from changes in intracellular pH. J Biol Chem 280 : 30864 30872.
111. Wong W, Scott JD (2004). AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5 : 959 970.
112. Wu J, Brown SH, von Daake S, Taylor SS (2007). PKA type IIalpha holoenzyme reveals a combinatorial strategy for isoform diversity. Science 318 : 274 279.
113. Xiao RP, Hohl C, Altschuld R, Jones L, Livingston B, Ziman B et al. (1994). Beta 2-adrenergic receptor-stimulated increase in cAMP in rat heart cells is not coupled to changes in Ca2+ dynamics, contractility, or phospholamban phosphorylation. J Biol Chem 269 : 19151 19156.
114. Yu HJ, Ma H, Green RD (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.
115. Zaccolo M, Pozzan T (2002). Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295 : 1711 1715.
116. Zaccolo M, De Giorgi F, Cho CY, Feng L, Knapp T, Negulescu PA et al. (2000). A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat Cell Biol 2 : 25 29.
117. Zakhary DR, Moravec CS, Bond M (2000). Regulation of PKA binding to AKAPs in the heart: alterations in human heart failure. Circulation 101 : 1459 1464.
118. Zhang J, Ma Y, Taylor SS, Tsien RY (2001). Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc Natl Acad Sci USA 98 : 14997 15002.
119. Zhang J, Hupfeld CJ, Taylor SS, Olefsky JM, Tsien RY (2005). Insulin disrupts beta-adrenergic signalling to protein kinase A in adipocytes. Nature 437 : 569 573.