Local cAMP signaling in disease at a glance

Journal of Cell Science

Volumn 126, Issue 20, 2013, Pages 4537-4543

  Gold, Matthew G ^a   Gonen, Tamir ^b   Scott, John D ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN;

ARTICLE; CATARACT; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE OVEREXPRESSION; HEART FAILURE; HEART INFARCTION; HEART VENTRICLE HYPERTROPHY; HUMAN; INSULIN RELEASE; LONG QT SYNDROME; MELANOMA; MEMBRANE DEPOLARIZATION; MISSENSE MUTATION; MITOCHONDRIAL MEMBRANE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; SECOND MESSENGER;

ANIMALS; CARDIOVASCULAR DISEASES; CATARACT; CYCLIC AMP; DIABETES MELLITUS; HUMANS; NEOPLASMS; SECOND MESSENGER SYSTEMS;

EID: 84885441920     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.133751     Document Type: Article

References (109)

1. Ashcroft, F. M. and Rorsman, P. (2012). Diabetes mellitus and the b cell: the last ten years. Cell 148, 1160-1171.
2. Ball, L. E., Garland, D. L., Crouch, R. K. and Schey, K. L. (2004). Post-translational modifications of aquaporin 0 (AQP0) in the normal human lens: spatial and temporal occurrence. Biochemistry 43, 9856-9865.
3. Bernstein, H. G., Dobrowolny, H., Schott, B. H., Gorny, X., Becker, V., Steiner, J., Seidenbecher, C. I., and Bogerts, B. (2013). Increased density of AKAP5-expressing neurons in the anterior cingulate cortex of subjects with bipolar disorder. J. Psychiatr. Res. 47, 699-705.
4. Bloemendal, H., Zweers, A., Vermorken, F., Dunia, I., and Benedetti, E. L. (1972). The plasma membranes of eye lens fibres. Biochemical, and structural characterization. Cell Differ. 1, 91-106.
5. Blundell, T. L., Harrison, S. C., Stroud, R. M., Yokoyama, S., Kay, L. E., Rossman, M. G., Berman, H. M., Wlodawer, A., Conti, E., Kobilka, B. et al. (2011). Celebrating structural biology. Nat. Struct. Mol. Biol. 18, 1304-1316.
6. Bos, J. L. (2006). Epac proteins: multi-purpose cAMP targets. Trends Biochem. Sci. 31, 680-686.
7. Brennan, D. F., Dar, A. C., Hertz, N. T., Chao, W. C., Burlingame, A. L., Shokat, K. M., and Barford, D. (2011). A Raf-induced allosteric transition of KSR stimulates phosphorylation of MEK. Nature 472, 366-369.
8. Brian, G., and Taylor, H. (2001). Cataract blindness-challenges for the 21st century. Bull. World Health Organ. 79, 249-256.
9. Burgering, B. M., Pronk, G. J., van Weeren, P. C., Chardin, P., and Bos, J. L. (1993). cAMP antagonizes p21ras-directed activation of extracellular signalregulated kinase 2, and phosphorylation of mSos nucleotide exchange factor. EMBO J. 12, 4211-4220.
10. Buxton, I. L., and Brunton, L. L. (1983). Compartments of cyclic AMP, and protein kinase in mammalian cardiomyocytes. J. Biol. Chem. 258, 10233-10239.
11. Calvin, H. I., Wu, K., Li, W., Guo, L., Banerjee, U., and Fu, S. C. (2003). Induction of cortical cataracts in cultured mouse lenses with H-89, an inhibitor of protein kinase A. Curr. Eye Res. 27, 269-278.
12. Carnegie, G. K., Smith, F. D., McConnachie, G., Langeberg, L. K., and Scott, J. D. (2004). AKAP-Lbc nucleates a protein kinase D activation scaffold. Mol. Cell 15, 889-899.
13. Carnegie, G. K., Soughayer, J., Smith, F. D., Pedroja, B. S., Zhang, F., Diviani, D., Bristow, M. R., Kunkel, M. T., Newton, A. C., Langeberg, L. K. et al. (2008). AKAP-Lbc mobilizes a cardiac hypertrophy signaling pathway. Mol. Cell 32, 169-179.
14. Chen, L., Marquardt, M. L., Tester, D. J., Sampson, K. J., Ackerman, M. J., and Kass, R. S. (2007). Mutation of an A-kinase-anchoring protein causes long-QT syndrome. Proc. Natl. Acad. Sci. USA 104, 20990-20995.
15. Christian, F., Szaszák, M., Friedl, S., Drewianka, S., Lorenz, D., Goncalves, A., Furkert, J., Vargas, C., Schmieder, P., Götz, F. et al. (2011). 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.
16. Coghlan, V. M., Perrino, B. A., Howard, M., Langeberg, L. K., Hicks, J. B., Gallatin, W. M., and Scott, J. D. (1995). Association of protein kinase A, and protein phosphatase 2B with a common anchoring protein. Science 267, 108-111.
17. Cook, S. J., and McCormick, F. (1993). Inhibition by cAMP of Ras-dependent activation of Raf. Science 262, 1069-1072.
18. Cummings, D. E., Brandon, E. P., Planas, J. V., Motamed, K., Idzerda, R. L., and McKnight, G. S. (1996). Genetically lean mice result from targeted disruption of the RII beta subunit of protein kinase A. Nature 382, 622-626.
19. Czyzyk, T. A., Sikorski, M. A., Yang, L., and McKnight, G. S. (2008). Disruption of the RIIbeta subunit of PKA reverses the obesity syndrome of Agouti lethal yellow mice. Proc. Natl. Acad. Sci. USA 105, 276-281.
20. Davies, H., Bignell, G. R., Cox, C., Stephens, P., Edkins, S., Clegg, S., Teague, J., Woffendin, H., Garnett, M. J., Bottomley, W. et al. (2002). Mutations of the BRAF gene in human cancer. Nature 417, 949-954.
21. Davis, M. I., Hunt, J. P., Herrgard, S., Ciceri, P., Wodicka, L. M., Pallares, G., Hocker, M., Treiber, D. K., and Zarrinkar, P. P. (2011). Comprehensive analysis of kinase inhibitor selectivity. Nat. Biotechnol. 29, 1046-1051.
22. Dessauer, C. W. (2009). Adenylyl cyclase-A-kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol. Pharmacol. 76, 935-941.
23. Diviani, D., Maric, D., Pérez López, I., Cavin, S., and Del Vescovo, C. D. (2013). A-kinase anchoring proteins: molecular regulators of the cardiac stress response. Biochim. Biophys. Acta 1833, 901-908.
24. Dodge, K. L., Khouangsathiene, S., Kapiloff, M. S., Mouton, R., Hill, E. V., Houslay, M. D., Langeberg, L. K., and Scott, J. D. (2001). mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. EMBO J. 20, 1921-1930.
25. Dodge-Kafka, K. L., Soughayer, J., Pare, G. C., Carlisle Michel, J. J., Langeberg, L. K., Kapiloff, M. S., and Scott, J. D. (2005). The protein kinase Aanchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature 437, 574-578.
26. Dumaz, N., and Marais, R. (2003). Protein kinase A blocks Raf-1 activity by stimulating 14-3-3 binding, and blocking Raf-1 interaction with Ras. J. Biol. Chem. 278, 29819-29823.
27. Dumaz, N., and Marais, R. (2005). Integrating signals between cAMP, and the RAS/RAF/MEK/ERK signalling pathways. Based on the anniversary prize of the Gesellschaft für Biochemie und Molekularbiologie Lecture delivered on 5 July 2003 at the Special FEBS Meeting in Brussels. FEBS J. 272, 3491-3504.
28. Filippakopoulos, P., Qi, J., Picaud, S., Shen, Y., Smith, W. B., Fedorov, O., Morse, E. M., Keates, T., Hickman, T. T., Felletar, I. et al. (2010). Selective inhibition of BET bromodomains. Nature 468, 1067-1073.
29. 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.
30. Fowler, D. M., Araya, C. L., Fleishman, S. J., Kellogg, E. H., Stephany, J. J., Baker, D., and Fields, S. (2010). High-resolution mapping of protein sequence-function relationships. Nat. Methods 7, 741-746.
31. Francis, S. H., Blount, M. A., and Corbin, J. D. (2011). Mammalian cyclic nucleotide phosphodiesterases: molecular mechanisms, and physiological functions. Physiol. Rev. 91, 651-690.
32. Fraser, I. D., Cong, M., Kim, J., Rollins, E. N., Daaka, Y., Lefkowitz, R. J., and Scott, J. D. (2000). Assembly of an A kinase-anchoring protein-beta(2)-adrenergic receptor complex facilitates receptor phosphorylation, and signaling. Curr. Biol. 10, 409-412.
33. Gao, T., Yatani, A., Dell'Acqua, M. L., Sako, H., Green, S. A., Dascal, N., Scott, J. D., and Hosey, M. M. (1997). cAMP-dependent regulation of cardiac L-type Ca2+ channels requires membrane targeting of PKA, and phosphorylation of channel subunits. Neuron 19, 185-196.
34. Gao, S., Wang, H. Y., and Malbon, C. C. (2011). AKAP5, and AKAP12 Form Homo-oligomers. J. Mol. Signal. 6, 3.
35. Gerthoffer, W. T., Solway, J., and Camoretti-Mercado, B. (2013). Emerging targets for novel therapy of asthma. Curr. Opin. Pharmacol. 13, 324-330.
36. Gold, M. G., Lygren, B., Dokurno, P., Hoshi, N., McConnachie, G., Taskén, K., Carlson, C. R., Scott, J. D., and Barford, D. (2006). Molecular basis of AKAP specificity for PKA regulatory subunits. Mol. Cell 24, 383-395.
37. Gold, M. G., Stengel, F., Nygren, P. J., Weisbrod, C. R., Bruce, J. E., Robinson, C. V., Barford, D., and Scott, J. D. (2011). Architecture, and dynamics of an Akinase anchoring protein 79 (AKAP79) signaling complex. Proc. Natl. Acad. Sci. USA 108, 6426-6431.
38. Gold, M. G., Reichow, S. L., O'Neill, S. E., Weisbrod, C. R., Langeberg, L. K., Bruce, J. E., Gonen, T., and Scott, J. D. (2012). AKAP2 anchors PKA with aquaporin-0 to support ocular lens transparency. EMBO Mol. Med. 4, 15-26.
39. Gold, M. G., Fowler, D. M., Means, C. K., Pawson, C. T., Stephany, J. J., Langeberg, L. K., Fields, S., and Scott, J. D. (2013). Engineering AKAP-selective regulatory subunits of PKA through structure-based phage selection. J. Biol. Chem. 288, 17111-17121.
40. Gonen, T., and Walz, T. (2006). The structure of aquaporins. Q. Rev. Biophys. 39, 361-396.
41. Gromada, J., Brock, B., Schmitz, O., and Rorsman, P. (2004). Glucagon-like peptide-1: regulation of insulin secretion, and therapeutic potential. Basic Clin. Pharmacol. Toxicol. 95, 252-262.
42. Hanahan, D., and Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
43. Higueruelo, A. P., Jubb, H., and Blundell, T. L. (2013). Protein-protein interactions as druggable targets: recent technological advances. Curr. Opin. Pharmacol.
44. Hill J A., and Olson, E. N. (2008). Cardiac plasticity. N. Engl. J. Med. 358, 1370-1380.
45. Hinke, S. A., Navedo, M. F., Ulman, A., Whiting, J. L., Nygren, P. J., Tian, G., Jimenez-Caliani, A. J., Langeberg, L. K., Cirulli, V., Tengholm, A. et al. (2012). Anchored phosphatases modulate glucose homeostasis. EMBO J. 31, 3991-4004.
46. Hoshi, N., Langeberg, L. K., Gould, C. M., Newton, A. C., and Scott, J. D. (2010). Interaction with AKAP79 modifies the cellular pharmacology of PKC. Mol. Cell 37, 541-550.
47. Josefsen, K., Lee, Y. C., Thams, P., Efendic, S., and Nielsen, J. H. (2010). AKAP 18 alpha, and gamma have opposing effects on insulin release in INS-1E cells. FEBS Lett. 584, 81-85.
48. Kapiloff, M. S., Piggott, L. A., Sadana, R., Li, J., Heredia, L. A., Henson, E., Efendiev, R., and Dessauer, C. W. (2009). An adenylyl cyclasemAKAPbeta signaling complex regulates cAMP levels in cardiac myocytes. J. Biol. Chem. 284, 23540-23546.
49. Keely, S. L. (1977). Activation of cAMP-dependent protein kinase without a corresponding increase in phosphorylase activity. Res. Commun. Chem. Pathol. Pharmacol. 18, 283-290.
50. Kim, C., Cheng, C. Y., Saldanha, S. A., and Taylor, S. S. (2007). PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation. Cell 130, 1032-1043.
51. Kim, H., Scimia, M. C., Wilkinson, D., Trelles, R. D., Wood, M. R., Bowtell, D., Dillin, A., Mercola, M., and Ronai, Z. A. (2011). Fine-tuning of Drp1/Fis1 availability by AKAP121/Siah2 regulates mitochondrial adaptation to hypoxia. Mol. Cell 44, 532-544.
52. Kinderman, F. S., Kim, C., von Daake, S., Ma, Y., Pham, B. Q., Spraggon, G., Xuong, N. H., Jennings, P. A., and Taylor, S. S. (2006). A dynamic mechanism for AKAP binding to RII isoforms of cAMP-dependent protein kinase. Mol. Cell 24, 397-408.
53. Knight, Z. A., Lin, H., and Shokat, K. M. (2010). Targeting the cancer kinome through polypharmacology. Nat. Rev. Cancer 10, 130-137.
54. Leech, C. A., Dzhura, I., Chepurny, O. G., Kang, G., Schwede, F., Genieser, H. G., and Holz, G. G. (2011). Molecular physiology of glucagon-like peptide-1 insulin secretagogue action in pancreatic b cells. Prog. Biophys. Mol. Biol. 107, 236-247.
55. Lester, L. B., Langeberg, L. K., and Scott, J. D. (1997). Anchoring of protein kinase A facilitates hormone-mediated insulin secretion. Proc. Natl. Acad. Sci. USA 94, 14942-14947.
56. Li, H., Zhang, L., Rao, A., Harrison, S. C., and Hogan, P. G. (2007). Structure of calcineurin in complex with PVIVIT peptide: portrait of a low-affinity signalling interaction. J. Mol. Biol. 369, 1296-1306.
57. Li, H., Pink, M. D., Murphy, J. G., Stein, A., Dell'Acqua, M. L., and Hogan, P. G. (2012a). Balanced interactions of calcineurin with AKAP79 regulate Ca2+-calcineurin-NFAT signaling. Nat. Struct. Mol. Biol. 19, 337-345.
58. Li, Y., Chen, L., Kass, R. S., and Dessauer, C. W. (2012b). 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.
59. Light, Y., Paterson, H., and Marais, R. (2002). 14-3-3 antagonizes Ras-mediated Raf-1 recruitment to the plasma membrane to maintain signaling fidelity. Mol. Cell. Biol. 22, 4984-4996.
60. Lindsey Rose, K. M., Wang, Z., Magrath, G. N., Hazard, E. S., Hildebrandt, J. D., and Schey, K. L. (2008). Aquaporin 0-calmodulin interaction, and the effect of aquaporin 0 phosphorylation. Biochemistry 47, 339-347.
61. Lin, H., Hejtmancik, J. F., and Qi, Y. (2007). A substitution of arginine to lysine at the COOH-terminus of MIP caused a different binocular phenotype in a congenital cataract family. Mol. Vis. 13, 1822-1827.
62. Liu, J., Ek Vitorin, J. F., Weintraub, S. T., Gu, S., Shi, Q., Burt, J. M., and Jiang, J. X. (2011). Phosphorylation of connexin 50 by protein kinase A enhances gap junction, and hemichannel function. J. Biol. Chem. 286, 16914-16928.
63. Marquette, A., André, J., Bagot, M., Bensussan, A., and Dumaz, N. (2011). ERK, and PDE4 cooperate to induce RAF isoform switching in melanoma. Nat. Struct. Mol. Biol. 18, 584-591.
64. Marx, S. O., Kurokawa, J., Reiken, S., Motoike, H., D'Armiento, J., Marks, A. R., and Kass, R. S. (2002). Requirement of a macromolecular signaling complex for beta adrenergic receptor modulation of the KCNQ1-KCNE1 potassium channel. Science 295, 496-499.
65. Mathias, R. T., Kistler, J., and Donaldson, P. (2007). The lens circulation. J. Membr. Biol. 216, 1-16.
66. Matulef, K., and Zagotta, W. N. (2003). Cyclic nucleotide-gated ion channels. Annu. Rev. Cell Dev. Biol. 19, 23-44.
67. Maurice, D. H. (2013). PDE8A runs interference to limit PKA inhibition of Raf-1. Proc. Natl. Acad. Sci. USA 110, 6248-6249.
68. Means, C. K., Lygren, B., Langeberg, L. K., Jain, A., Dixon, R. E., Vega, A. L., Gold, M. G., Petrosyan, S., Taylor, S. S., Murphy, A. N. et al. (2011). An entirely specific type I A-kinase anchoring protein that can sequester two molecules of protein kinase A at mitochondria. Proc. Natl. Acad. Sci. USA 108, E1227-E1235.
69. Millar, J. K., Pickard, B. S., Mackie, S., James, R., Christie, S., Buchanan, S. R., Malloy, M. P., Chubb, J. E., Huston, E., Baillie, G. S. et al. (2005). DISC1, and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signaling. Science 310, 1187-1191.
70. Miller, R. A., Chu, Q., Xie, J., Foretz, M., Viollet, B., and Birnbaum, M. J. (2013). Biguanides suppress hepatic glucagon signalling by decreasing production of cyclic AMP. Nature 494, 256-260.
71. Mullard, A. (2012). Protein-protein interaction inhibitors get into the groove. Nat. Rev. Drug Discov. 11, 173-175.
72. Okuzumi, T., Fiedler, D., Zhang, C., Gray, D. C., Aizenstein, B., Hoffman, R., and Shokat, K. M. (2009). Inhibitor hijacking of Akt activation. Nat. Chem. Biol. 5, 484-493.
73. Okuzumi, T., Ducker, G. S., Zhang, C., Aizenstein, B., Hoffman, R., and Shokat, K. M. (2010). Synthesis, and evaluation of indazole based analog sensitive Akt inhibitors. Mol. Biosyst. 6, 1389-1402.
74. Perera, R. K., and Nikolaev, V. O. (2013). Compartmentation of cAMP signalling in cardiomyocytes in health, and disease. Acta Physiol. (Oxf.) 207, 650-662.
75. 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. USA 105, 13835-13840.
76. Poulikakos, P. I., Zhang, C., Bollag, G., Shokat, K. M., and Rosen, N. (2010). RAF inhibitors transactivate RAF dimers, and ERK signalling in cells with wild-type BRAF. Nature 464, 427-430.
77. Prince, J. T., and Ahn, N. G. (2010). The case of the disappearing drug target. Mol. Cell 37, 455-456.
78. Rehmann, H. (2012). Epac2: a sulfonylurea receptor? Biochem. Soc. Trans. 40, 6-10.
79. Reichow, S. L., and Gonen, T. (2008). Noncanonical binding of calmodulin to aquaporin-0: implications for channel regulation. Structure 16, 1389-1398.
80. Reissner, K. J. (2013). Proteomic analyses of PKA, and AKAP signaling in cocaine addiction. Neuropsychopharmacology 38, 251-252.
81. Renthal, W., Kumar, A., Xiao, G., Wilkinson, M., Covington, H. E., 3rd, Maze, I., Sikder, D., Robison, A. J., LaPlant, Q., Dietz, D. M. et al. (2009). Genomewide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 62, 335-348.
82. Richter, S., Gorny, X., Marco-Pallares, J., Krämer, U. M., Machts, J., Barman, A., Bernstein, H. G., Schüle, R., Sch0̈ls, L., Rodriguez-Fornells, A. et al. (2011). A Potential Role for a Genetic Variation of AKAP5 in Human Aggression, and Anger Control. Front Hum. Neurosci 5, 175.
83. Roth, B. L., and Marshall, F. H. (2012). NOBEL 2012 Chemistry: Studies of a ubiquitous receptor family. Nature 492, 57.
84. Sarma, G. N., Kinderman, F. S., Kim, C., von Daake, S., Chen, L., Wang, B. C., and Taylor, S. S. (2010). Structure of D-AKAP2:PKA RI complex: insights into AKAP specificity, and selectivity. Structure 18, 155-166.
85. Sculptoreanu, A., Scheuer, T., and Catterall, W. A. (1993). Voltage-dependent potentiation of L-type Ca2+channels due to phosphorylation by cAMP-dependent protein kinase. Nature 364, 240-243.
86. Shibasaki, T., Takahashi, H., Miki, T., Sunaga, Y., Matsumura, K., Yamanaka, M., Zhang, C., Tamamoto, A., Satoh, T., Miyazaki, J. et al. (2007). Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc. Natl. Acad. Sci. USA 104, 19333-19338.
87. Short, R. A., and Tuttle, K. R. (2005). Clinical evidence for the influence of uric acid on hypertension, cardiovascular disease,, and kidney disease: a statistical modeling perspective. Semin. Nephrol. 25, 25-31.
88. Smith, F. D., Langeberg, L. K., Cellurale, C., Pawson, T., Morrison, D. K., Davis, R. J., and Scott, J. D. (2010). AKAP-Lbc enhances cyclic AMP control of the ERK1/2 cascade. Nat. Cell Biol. 12, 1242-1249.
89. Søberg, K., Jahnsen, T., Rognes, T., Skålhegg, B. S., and Laerdahl, J. K. (2013). Evolutionary paths of the cAMP-dependent protein kinase (PKA) catalytic subunits. PLoS ONE 8, e60935.
90. Sperandio, O., Reynès, C. H., Camproux, A. C., and Villoutreix, B. O. (2010). Rationalizing the chemical space of protein-protein interaction inhibitors. Drug Discov. Today 15, 220-229.
91. Stapleton, M. P. (1997). Sir James Black, and propranolol. The role of the basic sciences in the history of cardiovascular pharmacology. Tex. Heart Inst. J. 24, 336-342.
92. Sutherland, E. W. (1971). [Nobel prize in physiology or medicine 1971: the action of hormones outlined]. Lakartidningen 68, 4991-4995.
93. Taylor, S. S., Ilouz, R., Zhang, P., and Kornev, A. P. (2012). Assembly of allosteric macromolecular switches: lessons from PKA. Nat. Rev. Mol. Cell Biol. 13, 646-658.
94. Terrenoire, C., Houslay, M. D., Baillie, G. S., and Kass, R. S. (2009). The cardiac IKs potassium channel macromolecular complex includes the phosphodiesterase PDE4D3. J. Biol. Chem. 284, 9140-9146.
95. Tr0̈ger, J., Moutty, M. C., Skroblin, P., and Klussmann, E. (2012). A-kinase anchoring proteins as potential drug targets. Br. J. Pharmacol. 166, 420-433.
96. Tuttle, K. R., Bakris, G. L., Toto, R. D., McGill, J. B., Hu, K., and Anderson, P. W. (2005). The effect of ruboxistaurin on nephropathy in type 2 diabetes. Diabetes Care 28, 2686-2690.
97. Varadaraj, K., Kumari, S., Shiels, A., and Mathias, R. T. (2005). Regulation of aquaporin water permeability in the lens. Invest. Ophthalmol. Vis. Sci. 46, 1393-1402.
98. Welch, E. J., Jones, B. W., and Scott, J. D. (2010). Networking with AKAPs: context-dependent regulation of anchored enzymes. Mol. Interv. 10, 86-97.
99. Wells, J. A., and McClendon, C. L. (2007). Reaching for high-hanging fruit in drug discovery at proteinprotein interfaces. Nature 450, 1001-1009.
100. Willoughby, D., Wong, W., Schaack, J., Scott, J. D., and Cooper, D. M. (2006). An anchored PKA, and PDE4 complex regulates subplasmalemmal cAMP dynamics. EMBO J. 25, 2051-2061.
101. Wong, W., and Scott, J. D. (2004). AKAP signalling complexes: focal points in space, and time. Nat. Rev. Mol. Cell Biol. 5, 959-970.
102. Wong, W., Goehring, A. S., Kapiloff, M. S., Langeberg, L. K., and Scott, J. D. (2008). mAKAP compartmentalizes oxygen-dependent control of HIF-1alpha. Sci. Signal. 1, ra18.
103. Wu, J., Dent, P., Jelinek, T., Wolfman, A., Weber, M. J., and Sturgill, T. W. (1993). Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 39,59-monophosphate. Science 262, 1065-1069.
104. Wu, J., Brown, S. H., von Daake, S., and Taylor, S. S. (2007). PKA type IIalpha holoenzyme reveals a combinatorial strategy for isoform diversity. Science 318, 274-279.
105. Yu, H., van Berkel, T. J., and Biessen, E. A. (2007). Therapeutic potential of VIVIT, a selective peptide inhibitor of nuclear factor of activated T cells, in cardiovascular disorders. Cardiovasc. Drug Rev. 25, 175-187.
106. Zaccolo, M., and Pozzan, T. (2002). Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295, 1711-1715.
107. Zetterqvist, O., and Ragnarsson, U. (1982). The structural requirements of substrates of cyclic AMPdependent protein kinase. FEBS Lett. 139, 287-290.
108. Zhang, C. L., Katoh, M., Shibasaki, T., Minami, K., Sunaga, Y., Takahashi, H., Yokoi, N., Iwasaki, M., Miki, T., and Seino, S. (2009). The cAMP sensor Epac2 is a direct target of antidiabetic sulfonylurea drugs. Science 325, 607-610.
109. Zhang, P., Smith-Nguyen, E. V., Keshwani, M. M., Deal, M. S., Kornev, A. P., and Taylor, S. S. (2012). Structure, and allostery of the PKA RIIb tetrameric holoenzyme. Science 335, 712-716.