AKAP18:PKA-RIIα structure reveals crucial anchor points for recognition of regulatory subunits of PKA

Biochemical Journal

Volumn 473, Issue 13, 2016, Pages 1881-1894

  Götz, Frank ^a,b   Roske, Yvette ^a   Schulz, Maike Svenja ^a   Autenrieth, Karolin ^c   Bertinetti, Daniela ^c   Faelber, Katja ^a   Zühlke, Kerstin ^a   Kreuchwig, Annika ^b   Kennedy, Eileen J ^d   Krause, Gerd ^b   Daumke, Oliver ^a   Herberg, Friedrich W ^c   Heinemann, Udo ^a   Klussmann, Enno ^a,e  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^c UNIVERSITY OF KASSEL   (Germany)

^d UNIVERSITY OF GEORGIA   (United States)

^e DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

A kinase anchoring protein; Compartmentalized cAMP signalling; D D domain; PKA binding domain; Protein kinase A; Protein protein interaction

Indexed keywords

A KINASE ANCHORING PROTEIN 18BETA; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; PROTEIN BINDING; PROTEIN SUBUNIT;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; ISOTHERMAL TITRATION CALORIMETRY; LIGHT SCATTERING; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SUBUNIT; WESTERN BLOTTING; CALORIMETRY; CHEMISTRY; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE;

A KINASE ANCHOR PROTEINS; AMINO ACID SEQUENCE; BINDING SITES; CALORIMETRY; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SUBUNITS; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE;

EID: 85009413846     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20160242     Document Type: Article

References (56)

1. Skroblin, P., Grossmann, S., Schafer, G., Rosenthal, W. and Klussmann, E. (2010) Mechanisms of protein kinase a anchoring. Int. Rev. Cell. Mol. Biol. 283, 235-330 CrossRef PubMed.
2. Scott, J.D., Dessauer, C.W. and Tasken, K. (2013) Creating order from chaos: cellular regulation by kinase anchoring. Annu. Rev. Pharmacol. Toxicol. 53, 187-210 CrossRef PubMed.
3. Troger, J., Moutty, M.C., Skroblin, P. and Klussmann, E. (2012) A-kinase anchoring proteins as potential drug targets. Br. J. Pharmacol. 166, 420-433 CrossRef PubMed.
4. Dema, A., Perets, E., Schulz, M.S., Deak, V.A. and Klussmann, E. (2015) Pharmacological targeting of AKAP-directed compartmentalized cAMP signalling. Cell Signal. 27, 2474-2487 CrossRef PubMed.
5. Langeberg, L.K. and Scott, J.D. (2015) Signalling scaffolds and local organization of cellular behaviour. Nat. Rev. Mol. Cell Biol. 16, 232-244 CrossRef PubMed.
6. Klussmann, E. (2015) Protein-protein interactions of PDE4 family members - functions, interactions and therapeutic value. Cell Signal., 21 October, ii: S0898-6568(15)00287-9.
7. 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 CrossRef PubMed.
8. Huang, L.J., Durick, K., Weiner, J.A., Chun, J. and Taylor, S.S. (1997) D-AKAP2, a novel protein kinase A anchoring protein with a putative RGS domain. Proc. Natl. Acad. Sci. U.S.A. 94, 11184-11189 CrossRef PubMed.
9. Huang, L.J., Durick, K., Weiner, J.A., Chun, J. and Taylor, S.S. (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 CrossRef PubMed.
10. Henn, V., Edemir, B., Stefan, E., Wiesner, B., Lorenz, D., Theilig, F., Schmitt, R., Vossebein, L., Tamma, G., Beyermann, M. et al. (2004) Identification of a novel A-kinase anchoring protein 18 isoform and evidence for its role in the vasopressin-induced aquaporin-2 shuttle in renal principal cells. J. Biol. Chem. 279, 26654-26665 CrossRef PubMed.
11. McSorley, T., Stefan, E., Henn, V., Wiesner, B., Baillie, G.S., Houslay, M.D., Rosenthal, W. and Klussmann, E. (2006) Spatial organisation of AKAP18 and PDE4 isoforms in renal collecting duct principal cells. Eur. J. Cell Biol. 85, 673-678 CrossRef PubMed.
12. 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. U.S.A. 108, E1227-E1235 CrossRef PubMed.
13. Kovanich, D., van der Heyden, M.A., Aye, T.T., van Veen, T.A., Heck, A.J. and Scholten, A. (2010) Sphingosine kinase interacting protein is an A-kinase anchoring protein specific for type I cAMP-dependent protein kinase. ChemBioChem 11, 963-971 CrossRef PubMed.
14. Burgers, P.P., Ma, Y., Margarucci, L., Mackey, M., van der Heyden, M.A., Ellisman, M., Scholten, A., Taylor, S.S. and Heck, A.J. (2012) A small novel A-kinase anchoring protein (AKAP) that localizes specifically protein kinase A-regulatory subunit I (PKA-RI) to the plasma membrane. J. Biol. Chem. 287, 43789-43797 CrossRef PubMed.
15. Newlon, M.G., Roy, M., Morikis, D., Hausken, Z.E., Coghlan, V., Scott, J.D. and Jennings, P.A. (1999) The molecular basis for protein kinase A anchoring revealed by solution NMR. Nat. Struct. Biol. 6, 222-227 CrossRef PubMed.
16. Newlon, M.G., Roy, M., Morikis, D., Carr, D.W., Westphal, R., Scott, J.D. and Jennings, P.A. (2001) A novel mechanism of PKA anchoring revealed by solution structures of anchoring complexes. EMBO J. 20, 1651-1662 CrossRef PubMed.
17. 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 CrossRef PubMed.
18. Gold, M.G., Lygren, B., Dokurno, P., Hoshi, N., McConnachie, G., Tasken, 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 CrossRef PubMed.
19. Hundsrucker, C., Skroblin, P., Christian, F., Zenn, H.M., Popara, V., Joshi, M., Eichhorst, J., Wiesner, B., Herberg, F.W., Reif, B. et al. (2010) Glycogen synthase kinase 3beta interaction protein functions as an A-kinase anchoring protein. J. Biol. Chem. 285, 5507-5521 CrossRef PubMed.
20. Burgers, P.P., van der Heyden, M.A., Kok, B., Heck, A.J. and Scholten, A. (2015) A systematic evaluation of protein kinase a-A-kinase anchoring protein interaction motifs. Biochemistry 54, 11-21 CrossRef PubMed.
21. Jarnaess, E., Ruppelt, A., Stokka, A.J., Lygren, B., Scott, J.D. and Tasken, K. (2008) Dual specificity A-kinase anchoring proteins (AKAPs) contain an additional binding region that enhances targeting of protein kinase A type I. J. Biol. Chem. 283, 33708-33718 CrossRef PubMed.
22. Christian, F., Szaszak, M., Friedl, S., Drewianka, S., Lorenz, D., Goncalves, A., Furkert, J., Vargas, C., Schmieder, P., Gotz, 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 CrossRef PubMed.
23. Klussmann, E., Maric, K., Wiesner, B., Beyermann, M. and Rosenthal, W. (1999) Protein kinase A anchoring proteins are required for vasopressin-mediated translocation of aquaporin-2 into cell membranes of renal principal cells. J. Biol. Chem. 274, 4934-4938 CrossRef PubMed.
24. Klussmann, E. and Rosenthal, W. (2001) Role and identification of protein kinase A anchoring proteins in vasopressin-mediated aquaporin-2 translocation. Kidney Int. 60, 446-449 CrossRef PubMed.
25. Diviani, D., Dodge-Kafka, K.L., Li, J. and Kapiloff, M.S. (2011) A-kinase anchoring proteins: scaffolding proteins in the heart. Am. J. Physiol. Heart Circ. Physiol. 301, H1742-H1753 CrossRef PubMed.
26. Pidoux, G., Witczak, O., Jarnaess, E., Myrvold, L., Urlaub, H., Stokka, A.J., Kuntziger, T. and Tasken, K. (2011) Optic atrophy 1 is an A-kinase anchoring protein on lipid droplets that mediates adrenergic control of lipolysis. EMBO J. 30, 4371-4386 CrossRef PubMed.
27. Szaszak, M., Christian, F., Rosenthal, W. and Klussmann, E. (2008) Compartmentalized cAMP signalling in regulated exocytic processes in non-neuronal cells. Cell Signal. 20, 590-601 CrossRef PubMed.
28. Henn, V., Stefan, E., Baillie, G.S., Houslay, M.D., Rosenthal, W. and Klussmann, E. (2005) Compartmentalized cAMP signalling regulates vasopressin-mediated water reabsorption by controlling aquaporin-2. Biochem. Soc. Trans. 33, 1316-1318 CrossRef PubMed.
29. Fraser, I.D., Tavalin, S.J., Lester, L.B., Langeberg, L.K., Westphal, A.M., Dean, R.A., Marrion, N.V. and Scott, J.D. (1998) A novel lipid-Anchored A-kinase Anchoring Protein facilitates cAMP-responsive membrane events. EMBO J. 17, 2261-2272 CrossRef PubMed.
30. Trotter, K.W., Fraser, I.D., Scott, G.K., Stutts, M.J., Scott, J.D. and Milgram, S.L. (1999) Alternative splicing regulates the subcellular localization of A-kinase anchoring protein 18 isoforms. J. Cell Biol. 147, 1481-1492 CrossRef PubMed.
31. Gray, P.C., Johnson, B.D., Westenbroek, R.E., Hays, L.G., Yates, J.R. 3rd, Scheuer, T., Catterall, W.A. and Murphy, B.J. (1998) Primary structure and function of an A kinase anchoring protein associated with calcium channels. Neuron 20, 1017-1026 CrossRef PubMed.
32. Ahmad, F., Shen, W., Vandeput, F., Szabo-Fresnais, N., Krall, J., Degerman, E., Goetz, F., Klussmann, E., Movsesian, M. and Manganiello, V. (2015) Regulation of sarcoplasmic reticulum Ca2+ ATPase 2 (SERCA2) activity by phosphodiesterase 3A (PDE3A) in human myocardium: phosphorylation-dependent interaction of PDE3A1 with SERCA2. J. Biol. Chem. 290, 6763-6776 CrossRef PubMed.
33. 2+re-uptake into heart sarcoplasmic reticulum. EMBO Rep. 8, 1061-1067 CrossRef PubMed.
34. Carr, D.W., Stofko-Hahn, R.E., Fraser, I.D., Bishop, S.M., Acott, T.S., Brennan, R.G. and Scott, J.D. (1991) Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-Anchoring proteins occurs through an amphipathic helix binding motif. J. Biol. Chem. 266, 14188-14192 PubMed.
35. Hundsrucker, C., Krause, G., Beyermann, M., Prinz, A., Zimmermann, B., Diekmann, O., Lorenz, D., Stefan, E., Nedvetsky, P., Dathe, M. et al. (2006) High-Affinity AKAP7delta-protein kinase A interaction yields novel protein kinase A-Anchoring disruptor peptides. Biochem. J. 396, 297-306 CrossRef PubMed.
36. Wang, Y., Ho, T.G., Bertinetti, D., Neddermann, M., Franz, E., Mo, G.C., Schendowich, L.P., Sukhu, A., Spelts, R. C., Zhang, J. et al. (2014) Isoform-selective disruption of AKAP-localized PKA using hydrocarbon stapled peptides. ACS Chem. Biol. 9, 635-642 CrossRef PubMed.
37. Carlson, C.R., Lygren, B., Berge, T., Hoshi, N., Wong, W., Tasken, K. and Scott, J.D. (2006) Delineation of type I protein kinase A-selective signaling events using an RI anchoring disruptor. J. Biol. Chem. 281, 21535-21545 CrossRef PubMed.
38. Alto, N.M., Soderling, S.H., Hoshi, N., Langeberg, L.K., Fayos, R., Jennings, P.A. and Scott, J.D. (2003) Bioinformatic design of A-kinase anchoring protein-in silico: A potent and selective peptide antagonist of type II protein kinase A anchoring. Proc. Natl. Acad. Sci. U.S.A. 100, 4445-4450 CrossRef PubMed.
39. Burns-Hamuro, L.L., Ma, Y., Kammerer, S., Reineke, U., Self, C., Cook, C., Olson, G.L., Cantor, C.R., Braun, A. and Taylor, S.S. (2003) Designing isoform-specific peptide disruptors of protein kinase A localization. Proc. Natl. Acad. Sci. U.S.A. 100, 4072-4077 CrossRef PubMed.
40. Wang, Y., Ho, T.G., Franz, E., Hermann, J.S., Smith, F.D., Hehnly, H., Esseltine, J.L., Hanold, L.E., Murph, M.M., Bertinetti, D. et al. (2015) PKA-Type i selective constrained peptide disruptors of AKAP complexes. ACS Chem. Biol. 10, 1502-1510 CrossRef PubMed.
41. Deak, V.A. and Klussmann, E. (2015) Pharmacological interference with protein-protein interactions of A-kinase anchoring proteins as a strategy for the treatment of disease. Curr. Drug Targets. 2015 Apr 16. [Epub ahead of print].
42. 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 A-kinase anchoring protein (AKAP)-selective regulatory subunits of protein kinase A (PKA) through structure-based phage selection. J. Biol. Chem. 288, 17111-17121 CrossRef PubMed.
43. Schafer, G., Milic, J., Eldahshan, A., Gotz, F., Zuhlke, 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 CrossRef PubMed.
44. Krug, M., Weiss, M.S., Heinemann, U. and Mueller, U. (2012) XDSAPP: A graphical user interface for the convenient processing of diffraction data using XDS. J. Appl. Crystallogr. 45, 568-572 CrossRef.
45. McCoy, A.J., Grosse-Kunstleve, R.W., Storoni, L.C. and Read, R.J. (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458-464 CrossRef PubMed.
46. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 CrossRef PubMed.
47. Jesu Jaya Sudan, R. and Sudandiradoss, C. (2012) Pattern prediction and coordination geometry analysis from cadmium-binding proteins: A computational approach. Acta Crystallogr. D Biol. Crystallogr. 68, 1346-1358 CrossRef PubMed.
48. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619 CrossRef PubMed.
49. Bertinetti, D., Schweinsberg, S., Hanke, S.E., Schwede, F., Bertinetti, O., Drewianka, S., Genieser, H.G. and Herberg, F.W. (2009) Chemical tools selectively target components of the PKA system. BMC Chem. Biol. 9, 3 CrossRef PubMed.
50. Herberg, F.W., Maleszka, A., Eide, T., Vossebein, L. and Tasken, K. (2000) Analysis of A-kinase anchoring protein (AKAP) interaction with protein kinase A (PKA) regulatory subunits: PKA isoform specificity in AKAP binding. J. Mol. Biol. 298, 329-339 CrossRef PubMed.
51. Maass, P.G., Aydin, A., Luft, F.C., Schachterle, C., Weise, A., Stricker, S., Lindschau, C., Vaegler, M., Qadri, F., Toka, H.R. et al. (2015) PDE3A mutations cause autosomal dominant hypertension with brachydactyly. Nat. Genet. 47, 647-653 CrossRef PubMed.
52. Stefan, E., Wiesner, B., Baillie, G.S., Mollajew, R., Henn, V., Lorenz, D., Furkert, J., Santamaria, K., Nedvetsky, P., Hundsrucker, C. et al. (2007) Compartmentalization of cAMP-dependent signaling by phosphodiesterase-4D is involved in the regulation of vasopressin-mediated water reabsorption in renal principal cells. J. Am. Soc. Nephrol. 18, 199-212 CrossRef PubMed.
53. 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 CrossRef PubMed.
54. Horner, A., Goetz, F., Tampe, R., Klussmann, E. and Pohl, P. (2012) Mechanism for targeting the A-kinase anchoring protein AKAP18delta to the membrane. J. Biol. Chem. 287, 42495-42501 CrossRef PubMed.
55. Smith, F.D., Reichow, S.L., Esseltine, J.L., Shi, D., Langeberg, L.K., Scott, J.D. and Gonen, T. (2013) Intrinsic disorder within an AKAP-protein kinase A complex guides local substrate phosphorylation. eLife 2, e01319 PubMed.
56. Gold, M.G., Smith, F.D., Scott, J.D. and Barford, D. (2008) AKAP18 contains a phosphoesterase domain that binds AMP. J. Mol. Biol. 375, 1329-1343 CrossRef PubMed.