Scaffold state switching amplifies, accelerates, and insulates protein kinase c signaling

Journal of Biological Chemistry

Volumn 289, Issue 4, 2014, Pages 2353-2360

  Greenwald, Eric C ^a   M Redden, John ^a   Dodge Kafka, Kimberly L ^b   Saucerman, Jeffrey J ^a  

^a University of Virginia   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE C; SCAFFOLD PROTEIN; SIGNALING PROTEINS; STATE SWITCHING;

AMPLIFICATION; PROTEINS; SIGNAL TRANSDUCTION;

SCAFFOLDS (BIOLOGY);

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; BINDING PROTEIN; CALPHOSTIN C; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; PROTEIN AKAP7 ALPHA; PROTEIN KINASE C; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE COMPLEX; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SCAFFOLD STATE SWITCHING; SIGNAL TRANSDUCTION;

AKAP; ANCHORING; CELL SIGNALING; ENZYME KINETICS; MATHEMATICAL MODELING; PROTEIN KINASE C (PKC); SCAFFOLD PROTEINS;

A KINASE ANCHOR PROTEINS; ADENOSINE TRIPHOSPHATE; ANIMALS; CARBAZOLES; CERCOPITHECUS AETHIOPS; ENZYME INHIBITORS; HUMANS; MEMBRANE PROTEINS; MODELS, CHEMICAL; NAPHTHALENES; PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; VERO CELLS;

EID: 84893059304     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.497941     Document Type: Article

References (27)

1. Scott, J. D., Dessauer, C. W., and Taskén, K. (2013) Creating order from chaos: cellular regulation by kinase anchoring. Annu. Rev. Pharmacol. Toxicol. 53, 187-210
2. Edwards, A. S., and Scott, J. D. (2000) A-kinase anchoring proteins: protein kinase A and beyond. Curr. Opin. Cell Biol. 12, 217-221
3. Tavalin, S. J. (2008) AKAP79 selectively enhances protein kinase C regulation of GluR1 at a Ca2+-calmodulin-dependent protein kinase II/protein kinase C site. J. Biol. Chem. 283, 11445-11452
4. 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
5. Park, S. H., Zarrinpar, A., and Lim, W. A. (2003) Rewiring MAP kinase pathways using alternative scaffold assembly mechanisms. Science 299, 1061-1064
6. Greenwald, E. C., and Saucerman, J. J. (2011) Bigger, better, faster: principles and models of AKAP anchoring protein signaling. J. Cardiovasc. Pharmacol. 58, 462-469
7. Pidoux, G., and Taskén, K. (2010) Specificity and spatial dynamics of protein kinase A signaling organized by A-kinase-anchoring proteins. J. Mol. Endocrinol. 44, 271-284
8. 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 A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature 437, 574-578
9. Redden, J. M., Le, A. V., Singh, A., Federkiewicz, K., Smith, S., and Dodge-Kafka, K. L. (2012) Spatiotemporal regulation of PKC via interactions with AKAP7 isoforms. Biochem. J. 446, 301-309
10. Michaelis, L., Menten, M. L., Johnson, K. A., and Goody, R. S. (2011) The original Michaelis constant: translation of the 1913 Michaelis-Menten paper. Biochemistry 50, 8264-8269
11. Faux, M. C., Rollins, E. N., Edwards, A. S., Langeberg, L. K., Newton, A. C., and Scott, J. D. (1999) Mechanism of A-kinase-anchoring protein 79 (AKAP79) and protein kinase C interaction. Biochem. J. 343, 443-452
12. Zhang, J., Ma, Y., Taylor, S. S., and Tsien, R. Y. (2001) Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc. Natl. Acad. Sci. U.S.A. 98, 14997-15002
13. Violin, J. D., Zhang, J., Tsien, R. Y., and Newton, A. C. (2003) A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C. J. Cell Biol. 161, 899-909
14. Patel, H. H., Hamuro, L. L., Chun, B. J., Kawaraguchi, Y., Quick, A., Rebolledo, B., Pennypacker, J., Thurston, J., Rodriguez-Pinto, N., Self, C., Olson, G., Insel, P. A, Giles, W. R., Taylor, S. S., and Roth, D. M. (2010) Disruption of protein kinase A localization using a trans-activator of transcription (TAT)-conjugated A-kinase-anchoring peptide reduces cardiac function. J. Biol. Chem. 285, 27632-27640
15. 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., and Scott, J. D. (2008) AKAP-Lbc mobilizes a cardiac hypertrophy signaling pathway. Mol. Cell 32, 169-179
16. Sanderson, J. L., and Dell'Acqua, M. L. (2011) AKAP signaling complexes in regulation of excitatory synaptic plasticity. Neuroscientist 17, 321-336
17. Lester, L. B. (1997) Anchoring of protein kinase A facilitates hormonemediated insulin secretion. Proc. Natl. Acad. Sci. U.S.A. 94, 14942-14947
18. Levchenko, A., Bruck, J., and Sternberg, P. W. (2000) Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc. Natl. Acad. Sci. U.S.A. 97, 5818-5823
19. O'Shaughnessy, E. C., Palani, S., Collins, J. J., and Sarkar, C. A. (2011) Tunable signal processing in synthetic MAP kinase cascades. Cell 144, 119-131
20. Saucerman, J. J., Brunton, L. L., Michailova, A. P., and McCulloch, A. D. (2003) Modeling β-adrenergic control of cardiac myocyte contractility in silico. J. Biol. Chem. 278, 47997-48003
21. Saucerman, J. J., Healy, S. N., Belik, M. E., Puglisi, J. L., and McCulloch, A. D. (2004) Proarrhythmic consequences of a KCNQ1 AKAP-binding domain mutation: computational models of whole cells and heterogeneous tissue. Circ. Res. 95, 1216-1224
22. Malbon, C. C., Tao, J., Shumay, E., and Wang, H. Y. (2004) AKAP (Akinase anchoring protein) domains: beads of structure-function on the necklace of G-protein signalling. Biochem. Soc. Trans. 32, 861-864
23. Locasale, J. W., Shaw, A. S., and Chakraborty, A. K. (2007) Scaffold proteins confer diverse regulatory properties to protein kinase cascades. Proc. Natl. Acad. Sci. U.S.A. 104, 13307-13312
24. Oliveira, R. F., Terrin, A., Di Benedetto, G., Cannon, R. C., Koh, W., Kim, M., Zaccolo, M., and Blackwell, K. T. (2010) The role of type 4 phosphodiesterases in generating microdomains of cAMP: large scale stochastic simulations. PloS One 5, e11725
25. 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
26. Good, M. C., Zalatan, J. G., and Lim, W. A. (2011) Scaffold proteins: hubs for controlling the flow of cellular information. Science 332, 680-686
27. Good, M., Tang, G., Singleton, J., Reményi, A., and Lim, W. A. (2009) The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation. Cell 136, 1085-1097