Protein kinase A opposes the phosphorylation-dependent recruitment of glycogen synthase kinase 3β to A-kinase Anchoring Protein 220

Journal of Biological Chemistry

Volumn 290, Issue 32, 2015, Pages 19445-19457

  Whiting, Jennifer L ^a   Nygren, Patrick J ^a   Tunquist, Brian J ^b   Langeberg, Lorene K ^a   Seternes, Ole Morten ^a,c   Scott, John D ^a  

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

^b ARRAY BIOPHARMA INC   (United States)

^c UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING SITES; CROSSTALK; PHOSPHORYLATION; PROTEINS; SCAFFOLDS (BIOLOGY); SIGNAL TRANSDUCTION;

A-KINASE-ANCHORING PROTEINS; AFFINITY MEASUREMENT; GLYCOGEN SYNTHASE KINASE-3; MEMBRANE RUFFLES; MULTIENZYME COMPLEXES; PKA HOLOENZYME; PROTEIN KINASE A; REGULATORY MECHANISM;

ENZYMES;

A KINASE ANCHORING PROTEIN 220; BETA CATENIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; SERINE; THREONINE; UNCLASSIFIED DRUG; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; HOLOENZYME; PROTEIN BINDING; PROTEIN SUBUNIT; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; MOUSE; PHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; PROTEIN SUBUNIT; SEQUENCE ALIGNMENT;

A KINASE ANCHOR PROTEINS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HOLOENZYMES; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 84939158995     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.654822     Document Type: Article

References (61)

1. 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
2. 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
3. Taskén, K., and Aandahl, E. M. (2004) Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol. Rev. 84, 137-167
4. Langeberg, L. K., and Scott, J. D. (2015) Signalling scaffolds and local organization of cellular behaviour. Nat. Rev. Mol. Cell Biol. 16, 232-244
5. Bauman, A. L., Soughayer, J., Nguyen, B. T., Willoughby, D., Carnegie, G. K., Wong, W., Hoshi, N., Langeberg, L. K., Cooper, D. M., 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
6. 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., Dell'Acqua, M. L., Santana, L. F., and Scott, J. D. (2012) Anchored phosphatases modulate glucose homeostasis. EMBO J. 31, 3991-4004
7. Navedo, M. F., Nieves-Cintrón, M., Amberg, G. C., Yuan, C., Votaw, V. S., Lederer, W. J., McKnight, G. S., and Santana, L. F. (2008) AKAP150 is required for stuttering persistent Ca2+ sparklets and angiotensin II-induced hypertension. Circ. Res. 102, e1-e11
8. Tunquist, B. J., Hoshi, N., Guire, E. S., Zhang, F., Mullendorff, K., Langeberg, L. K., Raber, J., and Scott, J. D. (2008) Loss of AKAP150 perturbs distinct neuronal processes in mice. Proc. Natl. Acad. Sci. U.S.A. 105, 12557-12562
9. 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
10. Kritzer, M. D., Li, J., Passariello, C. L., Gayanilo, M., Thakur, H., Dayan, J., Dodge-Kafka, K., and Kapiloff, M. S. (2014) The scaffold protein muscle A-kinase anchoring protein β orchestrates cardiac myocyte hypertrophic signaling required for the development of heart failure. Circ. Heart Fail. 7, 663-672
11. 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
12. Knighton, D. R., Zheng, J. H., Ten Eyck, L. F., Ashford, V. A., Xuong, N.-H., Taylor, S. S., and Sowadski, J. M. (1991) Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253, 407-414
13. Su, Y., Dostmann, W. R., Herberg, F. W., Durick, K., Xuong, N.-H., Ten Eyck, L., Taylor, S. S., and Varughese, K. I. (1995) Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding proteins. Science 269, 807-813
14. 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
15. 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
16. 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
17. 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
18. 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
19. Dessauer, C. W. (2009) Adenylyl cyclase-A-kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol. Pharmacol. 76, 935-941
20. Lester, L. B., Coghlan, V. M., Nauert, B., and Scott, J. D. (1996) Cloning and characterization of a novel A-kinase anchoring protein: AKAP 220, association with testicular peroxisomes. J. Biol. Chem. 271, 9460-9465
21. Day, M. E., Gaietta, G. M., Sastri, M., Koller, A., Mackey, M. R., Scott, J. D., Perkins, G. A., Ellisman, M. H., and Taylor, S. S. (2011) Isoform-specific targeting of PKA to multivesicular bodies. J. Cell Biol. 193, 347-363
22. Schillace, R. V., and Scott, J. D. (1999) Association of the type 1 protein phosphatase PP1 with the A-kinase anchoring protein AKAP220. Curr. Biol. 9, 321-324
23. Schillace, R. V., Voltz, J. W., Sim, A. T., Shenolikar, S., and Scott, J. D. (2001) Multiple interactions within the AKAP220 signaling complex contribute to protein phosphatase 1 regulation. J. Biol. Chem. 276, 12128-12134
24. Tanji, C., Yamamoto, H., Yorioka, N., Kohno, N., Kikuchi, K., and Kikuchi, A. (2002) A-kinase anchoring protein AKAP220 binds to glycogen synthase kinase-3β (GSK-3β) and mediates protein kinase A-dependent inhibition of GSK-3β. J. Biol. Chem. 277, 36955-36961
25. Fang, X., Yu, S. X., Lu, Y., Bast, R. C., Jr., Woodgett, J. R., and Mills, G. B. (2000) Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc. Natl. Acad. Sci. U.S.A. 97, 11960-11965
26. Doble, B. W., and Woodgett, J. R. (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116, 1175-1186
27. ter Haar, E., Coll, J. T., Austen, D. A., Hsiao, H. M., Swenson, L., and Jain, J. (2001) Structure of GSK3β reveals a primed phosphorylation mechanism. Nat. Struct. Biol. 8, 593-596
28. Scales, T. M., Lin, S., Kraus, M., Goold, R. G., and Gordon-Weeks, P. R. (2009) Nonprimed and DYRK1A-primed GSK3 β-phosphorylation sites on MAP1B regulate microtubule dynamics in growing axons. J. Cell Sci. 122, 2424-2435
29. Weston, C. R., and Davis, R. J. (2001) Signal transduction: signaling specificity: a complex affair. Science 292, 2439-2440
30. Logue, J. S., Whiting, J. L., and Scott, J. D. (2011) Sequestering Rac with PKA confers cAMP control of cytoskeletal remodeling. Small GTPases 2, 173-176
31. 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
32. Smith, F. D., Samelson, B. K., and Scott, J. D. (2011) Discovery of cellular substrates for protein kinase A using a peptide array screening protocol. Biochem. J. 438, 103-110
33. Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., and Zhang, F. (2013) Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308
34. Doench, J. G., Hartenian, E., Graham, D. B., Tothova, Z., Hegde, M., Smith, I., Sullender, M., Ebert, B. L., Xavier, R. J., and Root, D. E. (2014) Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat. Biotechnol. 32, 1262-1267
35. Gajadhar, A., and Guha, A. (2010) A proximity ligation assay using transiently transfected, epitope-tagged proteins: application for in situ detection of dimerized receptor tyrosine kinases. Biotechniques 48, 145-152
36. Obenauer, J. C., Cantley, L. C., and Yaffe, M. B. (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641
37. Frame, S., Cohen, P., and Biondi, R. M. (2001) A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol. Cell 7, 1321-1327
38. Logue, J. S., Whiting, J. L., Tunquist, B., Langeberg, L. K., and Scott, J. D. (2011) Anchored protein kinase A recruitment of active Rac GTPase. J. Biol. Chem. 286, 22113-22121
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
40. 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
41. Asirvatham, A. L., Galligan, S. G., Schillace, R. V., Davey, M. P., Vasta, V., Beavo, J. A., and Carr, D. W. (2004) A-kinase anchoring proteins interact with phosphodiesterases in T lymphocyte cell lines. J. Immunol. 173, 4806-4814
42. 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
43. 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
44. 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., Ha, T., Santana, L. F., Tasken, K., and Scott, J. D. (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
45. 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
46. Huang, L. J., Wang, L., Ma, Y., Durick, K., Perkins, G., Deerinck, T. J., Ellisman, M. H., and Taylor, S. S. (1999) NH2-terminal targeting motifs direct dual specificity A-kinase- anchoring protein 1 (D-AKAP1) to either mitochondria or endoplasmic reticulum. J. Cell Biol. 145, 951-959
47. 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
48. 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
49. Carlson, C. R., Lygren, B., Berge, T., Hoshi, N., Wong, W., Taskén, 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
50. Cohen, P., and Frame, S. (2001) The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2, 769-776
51. Carnegie, G. K., Means, C. K., and Scott, J. D. (2009) A-kinase anchoring proteins: from protein complexes to physiology and disease. IUBMB Life 61, 394-406
52. Wong, W., Goehring, A. S., Kapiloff, M. S., Langeberg, L. K., and Scott, J. D. (2008) mAKAP compartmentalizes oxygen-dependent control of HIF-1α. Sci. Signal. 1, ra18
53. 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
54. 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
55. Prince, J. T., and Ahn, N. G. (2010) The case of the disappearing drug target. Mol. Cell 37, 455-456
56. Westphal, R. S., Tavalin, S. J., Lin, J. W., Alto, N. M., Fraser, I. D., Langeberg, L. K., Sheng, M., and Scott, J. D. (1999) Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex. Science 285, 93-96
57. Witczak, O., Skålhegg, B. S., Keryer, G., Bornens, M., Taskén, K., Jahnsen, T., and Orstavik, S. (1999) Cloning and characterization of a cDNA encoding an A-kinase anchoring protein located in the centrosome, AKAP450. EMBO J. 18, 1858-1868
58. 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 A-kinase anchoring protein 79 (AKAP79) signaling complex. Proc. Natl. Acad. Sci. U.S.A. 108, 6426-6431
59. Amieux, P. S., and McKnight, G. S. (2002) The essential role of RI α in the maintenance of regulated PKA activity. Ann. N.Y. Acad. Sci. 968, 75-95
60. Brandon, E. P., Idzerda, R. L., and McKnight, G. S. (1997) PKA isoforms, neural pathways, and behaviour: making the connection. Curr. Opin. Neurobiol. 7, 397-403
61. Hernández, F., Langa, E., Cuadros, R., Avila, J., and Villanueva, N. (2010) Regulation of GSK3 isoforms by phosphatases PP1 and PP2A. Mol. Cell Biochem. 344, 211-215