Protein kinase a (PKA) phosphorylation of Shp2 protein inhibits its phosphatase activity and modulates ligand specificity

Journal of Biological Chemistry

Volumn 290, Issue 19, 2015, Pages 12058-12067

  Burmeister, Brian T ^a   Wang, Li ^a   Gold, Matthew G ^c   Skidgel, Randal A ^a   O'Bryan, John P ^a,b,d   Carnegie, Graeme K ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYST ACTIVITY; ENZYMES; LIGANDS; PATHOLOGY; PHOSPHATASES; PHOSPHORYLATION; PROTEINS;

CARDIAC FUNCTIONS; CARDIAC HYPERTROPHY; CARDIAC MYOCYTES; LIGAND SPECIFICITY; PHOSPHATASE ACTIVITY; PROTEIN KINASE A; PROTEIN-TYROSINE PHOSPHATASE; SRC HOMOLOGY 2 DOMAINS;

HEART;

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; MUTANT PROTEIN; PROTEIN TYROSINE PHOSPHATASE SHP 2; SERINE; THREONINE; BETA ADRENERGIC RECEPTOR; LIGAND; PROTEIN BINDING; TYROSINE;

ALPHA HELIX; AMINO ACID COMPOSITION; ANIMAL CELL; ARTICLE; BETA ADRENERGIC STIMULATION; BINDING ASSAY; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME SPECIFICITY; HEART VENTRICLE HYPERTROPHY; IN VITRO STUDY; INTRACELLULAR SIGNALING; MOLECULAR MODEL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; ANIMAL; CARDIOMEGALY; CELL CULTURE; CHEMISTRY; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MUTATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN;

ANIMALS; CARDIOMEGALY; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HEK293 CELLS; HUMANS; LIGANDS; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; RATS; RECEPTORS, ADRENERGIC, BETA; SERINE; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; THREONINE; TYROSINE;

EID: 84929093821     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.642983     Document Type: Article

References (37)

1. Scott, J. D., and Pawson, T. (2009) Cell signaling in space and time: where proteins come together and when they're apart. Science 326, 1220-1224
2. Wong, W., and Scott, J. D. (2004) AKAP signalling complexes: focal points in space and time. Nat. Rev. Mol. Cell Biol. 5, 959-970
3. 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
4. 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
5. 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
6. 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
7. Mauban, J. R., O'Donnell, M., Warrier, S., Manni, S., and Bond, M. (2009) AKAP-scaffolding proteins and regulation of cardiac physiology. Physiology 24, 78-87
8. Carnegie, G. K., and Burmeister, B. T. (2011) A-kinase anchoring proteins that regulate cardiac remodeling. J. Cardiovasc. Pharmacol. 58, 451-458
9. Diviani, D. (2008) Modulation of cardiac function by A-kinase anchoring proteins. Curr. Opin. Pharmacol. 8, 166-173
10. 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
11. Aye, T. T., Soni, S., van Veen, T. A., van der Heyden, M. A., Cappadona, S., Varro, A., de Weger, R. A., de Jonge, N., Vos, M. A., Heck, A. J., and Scholten, A. (2012) Reorganized PKA-AKAP associations in the failing human heart. J. Mol. Cell. Cardiol. 52, 511-518
12. Diviani, D., Soderling, J., and Scott, J. D. (2001) AKAP-Lbc anchors protein kinase A and nucleates Gα 12-selective Rho-mediated stress fiber formation. J. Biol. Chem. 276, 44247-44257
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., and Scott, J. D. (2008) AKAP-Lbc mobilizes a cardiac hypertrophy signaling pathway. Mol. Cell 32, 169-179
14. Depre, C., Shipley, G. L., Chen, W., Han, Q., Doenst, T., Moore, M. L., Stepkowski, S., Davies, P. J., and Taegtmeyer, H. (1998) Unloaded heart in vivo replicates fetal gene expression of cardiac hypertrophy. Nat. Med. 4, 1269-1275
15. Frey, N., and Olson, E. N. (2003) Cardiac hypertrophy: the good, the bad, and the ugly. Annu. Rev. Physiol. 65, 45-79
16. Heineke, J., and Molkentin, J. D. (2006) Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat. Rev. Mol. Cell Biol. 7, 589-600
17. Burmeister, B. T., Taglieri, D. M., Wang, L., and Carnegie, G. K. (2012) Src homology 2 domain-containing phosphatase 2 (Shp2) is a component of the A-kinase-anchoring protein (AKAP)-Lbc complex and is inhibited by protein kinase A (PKA) under pathological hypertrophic conditions in the heart. J. Biol. Chem. 287, 40535-40546
18. Nakamura, T., Colbert, M., Krenz, M., Molkentin, J. D., Hahn, H. S., Dorn, G. W., 2nd, and Robbins, J. (2007) Mediating ERK 1/2 signaling rescues congenital heart defects in a mouse model of Noonan syndrome. J. Clin. Invest. 117, 2123-2132
19. Krenz, M., Gulick, J., Osinska, H. E., Colbert, M. C., Molkentin, J. D., and Robbins, J. (2008) Role of ERK1/2 signaling in congenital valve malformations in Noonan syndrome. Proc. Natl. Acad. Sci. U.S.A. 105, 18930-18935
20. Nakamura, T., Gulick, J., Pratt, R., and Robbins, J. (2009) Noonan syndrome is associated with enhanced pERK activity, the repression of which can prevent craniofacial malformations. Proc. Natl. Acad. Sci. U.S.A. 106, 15436-15441
21. Kontaridis, M. I., Swanson, K. D., David, F. S., Barford, D., and Neel, B. G. (2006) PTPN11 (Shp2) mutations in LEOPARD syndrome have dominant negative, not activating, effects. J. Biol. Chem. 281, 6785-6792
22. Stewart, R. A., Sanda, T., Widlund, H. R., Zhu, S., Swanson, K. D., Hurley, A. D., Bentires-Alj, M., Fisher, D. E., Kontaridis, M. I., Look, A. T., and Neel, B. G. (2010) Phosphatase-dependent and -independent functions of Shp2 in neural crest cells underlie LEOPARD syndrome pathogenesis. Dev. Cell 18, 750-762
23. Kontaridis, M. I., Yang, W., Bence, K. K., Cullen, D., Wang, B., Bodyak, N., Ke, Q., Hinek, A., Kang, P. M., Liao, R., and Neel, B. G. (2008) Deletion of Ptpn11 (Shp2) in cardiomyocytes causes dilated cardiomyopathy via effects on the extracellular signal-regulated kinase/mitogen-activated protein kinase and RhoA signaling pathways. Circulation 117, 1423-1435
24. 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
25. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
26. 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
27. Storz, P., Döppler, H., and Toker, A. (2004) Protein kinase CΔ selectively regulates protein kinase D-dependent activation of NF-κB in oxidative stress signaling. Mol. Cell. Biol. 24, 2614-2626
28. Storz, P., Döppler, H., and Toker, A. (2004) Activation loop phosphorylation controls protein kinase D-dependent activation of nuclear factor κB. Mol. Pharmacol. 66, 870-879
29. Döppler, H., and Storz, P. (2007) A novel tyrosine phosphorylation site in protein kinase D contributes to oxidative stress-mediated activation. J. Biol. Chem. 282, 31873-31881
30. Rapacciuolo, A., Suvarna, S., Barki-Harrington, L., Luttrell, L. M., Cong, M., Lefkowitz, R. J., and Rockman, H. A. (2003) Protein kinase A and G protein-coupled receptor kinase phosphorylation mediates β-1 adrenergic receptor endocytosis through different pathways. J. Biol. Chem. 278, 35403-35411
31. Hof, P., Pluskey, S., Dhe-Paganon, S., Eck, M. J., and Shoelson, S. E. (1998) Crystal structure of the tyrosine phosphatase SHP-2. Cell 92, 441-450
32. Kratz, C. P., Niemeyer, C. M., Castleberry, R. P., Cetin, M., Bergsträsser, E., Emanuel, P. D., Hasle, H., Kardos, G., Klein, C., Kojima, S., Stary, J., Trebo, M., Zecca, M., Gelb, B. D., Tartaglia, M., and Loh, M. L. (2005) The mutational spectrum of PTPN11 in juvenile myelomonocytic leukemia and Noonan syndrome/myeloproliferative disease. Blood 106, 2183-2185
33. Keilhack, H., David, F. S., McGregor, M., Cantley, L. C., and Neel, B. G. (2005) Diverse biochemical properties of Shp2 mutants. Implications for disease phenotypes. J. Biol. Chem. 280, 30984-30993
34. Enns, L. C., Bible, K. L., Emond, M. J., and Ladiges, W. C. (2010) Mice lacking the Cβ subunit of PKA are resistant to angiotensin II-induced cardiac hypertrophy and dysfunction. BMC Res. Notes 3, 307
35. Wang L., Burmeister B.T., Johnson K.R., Baillie G.S., Karginov A.V., Skidgel R.A., O'Bryan J.P., Carnegie G.K. (2015) UCR1C is a novel activator of phosphodiesterase 4 (PDE4) long isoforms and attenuates cardiomyocyte hypertrophy. Cell Signal. 27, 908-922
36. Fielitz, J., Kim, M. S., Shelton, J. M., Qi, X., Hill, J. A., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2008) Requirement of protein kinase D1 for pathological cardiac remodeling. Proc. Natl. Acad. Sci. U.S.A. 105, 3059-3063
37. Appert-Collin, A., Cotecchia, S., Nenniger-Tosato, M., Pedrazzini, T., and Diviani, D. (2007) The A-kinase anchoring protein (AKAP)-Lbc-signaling complex mediates alpha1 adrenergic receptor-induced cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 104, 10140-10145