The A-kinase-anchoring protein AKAP-Lbc facilitates cardioprotective PKA phosphorylation of Hsp20 on ser

Biochemical Journal

Volumn 446, Issue 3, 2012, Pages 437-443

  Edwards, Helen V ^a   Scott, John D ^b   Baillie, George S ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

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

Author keywords

AKAP Lbc; cAMP; cAMP dependent protein kinase (PKA); Cardioprotection; Heat shock protein of 20 kDa (Hsp20); Phosphodiesterase (PDE)

Indexed keywords

CASPASE 3; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; HEAT SHOCK PROTEIN 20; MEMBRANE PROTEIN; PROTEIN AKAP13; SERINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; ENZYME SUBSTRATE; EXTRACELLULAR MATRIX; GENE SILENCING; HEART MUSCLE CELL; HEART PROTECTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

A KINASE ANCHOR PROTEINS; HEK293 CELLS; HSP20 HEAT-SHOCK PROTEINS; HUMANS; MYOCARDIUM; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; SERINE; SIGNAL TRANSDUCTION;

EID: 84865597148     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120570     Document Type: Article

References (43)

1. Edwards, H. V., Cameron, R. T. and Baillie, G. S. (2011) The emerging role of HSP20 as a multifunctional protective agent. Cell. Signalling 23, 1447-1454
2. Fan, G. C. and Kranias, E. G. (2011) Small heat shock protein 20 (HspB6) in cardiac hypertrophy and failure. J. Mol. Cell. Cardiol. 51, 574-577
3. Fan, G. C., Ren, X. P., Qian, J., Yuan, Q. Y., Nicolaou, P., Wang, Y., Jones, W. K., Chu, G. X. and Kranias, E. G. (2005) Novel cardioprotective role of a small heat-shock protein, Hsp20, against ischemia/reperfusion injury. Circulation 111, 1792-1799 (Pubitemid 40525144)
4. Fan, G. C., Ren, X. P., Qian, J., Yuan, Q. Y., Wang, Y., Jones, W. K., Chu, G. X. and Kranias, E. G. (2004) Cardiac-specific overexpression of small heat-shock protein Hsp20 alleviates ischemia/reperfusion injury and myocardial dysfunction. Circulation 110, 1439
5. Fan, G. C., Yuan, Q. Y., Song, G. J., Wang, Y. G., Chen, G. L., Qian, J., Zhou, X. Y., Lee, Y. J., Ashraf, M. and Kranias, E. G. (2006) Small heat-shock protein Hsp20 attenuates β-agonist-mediated cardiac remodeling through apoptosis signal-regulating kinase 1. Circ. Res. 99, 1233-1242 (Pubitemid 44808660)
6. Fan, G. C., Chu, G. X., Mitton, B., Song, Q. J., Yuan, Q. Y. and Kranias, E. G. (2004) Small heat-shock protein Hsp20 phosphorylation inhibits β-agonist-induced cardiac apoptosis. Circ. Res. 94, 1474-1482 (Pubitemid 38780320)
7. Niwa, M., Kozawa, O., Matsuno, H., Kato, K. and Uematsu, T. (2000) Small molecular weight heat shock-related protein, HSP20, exhibits an anti-platelet activity by inhibiting receptor-mediated calcium influx. Life Sci. 66, PL7-PL12
8. Beall, A. C., Kato, K., Goldenring, J. R., Rasmussen, H. and Brophy, C. M. (1997) Cyclic nucleotide-dependent vasorelaxation is associated with the phosphorylation of a small heat shock-related protein. J. Biol. Chem. 272, 11283-11287 (Pubitemid 27184128)
9. Flynn, C. R., Komalavilas, P., Tessier, D., Thresher, J., Niederkofler, E. E., Dreiza, C. M., Nelson, R. W., Panitch, A., Joshi, L. and Brophy, C. M. (2003) Transduction of biologically active motifs of the small heat shock-related protein, HSP20, leads to relaxation of vascular smooth muscle. FASEB J. 17, 1358-1360
10. Qian, J., Ren, X. P., Wang, X. H., Zhang, P. Y., Jones, W. K., Molkentin, J. D., Fan, G. C. and Kranias, E. G. (2009) Blockade of Hsp20 phosphorylation exacerbates cardiac ischemia/reperfusion injury by suppressed autophagy and increased cell death. Circ. Res. 105, 1223-1231
11. Nicolaou, P., Knoll, R., Haghighi, K., Fan, G. C., Dorn, G. W., Hasenfuss, G. and Kranias, E. G. (2008) Human mutation in the anti-apoptotic heat shock protein 20 abrogates its cardioprotective effects. J. Biol. Chem. 283, 33465-33471
12. 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
13. Beavo, J. A. and Brunton, L. L. (2002) Cyclic nucleotide research - still expanding after half a century. Nat. Rev. Mol. Cell. Biol. 3, 710-718 (Pubitemid 34987792)
14. Baillie, G. S. (2009) Compartmentalized signalling: spatial regulation of cAMP by the action of compartmentalized phosphodiesterases. FEBS J. 276, 1790-1799
15. Sin, Y. Y., Edwards, H. V., Li, X., Day, J. P., Christian, F., Dunlop, A. J., Adams, D. R., Zaccolo, M., Houslay, M. D. and Baillie, G. S. (2011) Disruption of the cyclic AMP phosphodiesterase-4 (PDE4)-HSP20 complex attenuates the β-agonist induced hypertrophic response in cardiac myocytes. J. Mol. Cell. Cardiol. 50, 872-883
16. Welch, E. J., Jones, B. W. and Scott, J. D. (2010) Networking with AKAPs: context-dependent regulation of anchored enzymes. Mol. Interventions 10, 86-97
17. 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-β2-adrenergic receptor complex facilitates receptor phosphorylation and signaling. Curr. Biol. 10, 409-412 (Pubitemid 30213389)
18. 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 (Pubitemid 44363046)
19. 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 (Pubitemid 32397394)
20. Gao, T. Y., Yatani, A., DellAcqua, 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 (Pubitemid 27333004)
21. Lygren, B., Carlson, C. R., Santamaria, K., Lissandron, V., McSorley, T., Litzenberg, J., Lorenz, D., Wiesner, B., Rosenthal, W., Zaccolo, M. et al. (2007) AKAP complex regulates Ca2+ re-uptake into heart sarcoplasmic reticulum. EMBO Rep. 8, 1061-1067 (Pubitemid 350042342)
22. Ruehr, M. L., Russell, M. A., Ferguson, D. G., Bhat, M., Ma, J. J., Damron, D. S., Scott, J. D. and Bond, M. (2003) Targeting of protein kinase A by muscle A kinase-anchoring protein (mAKAP) regulates phosphorylation and function of the skeletal muscle ryanodine receptor. J. Biol. Chem. 278, 24831-24836 (Pubitemid 37548641)
23. 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
24. Dodge-Kafka, K. L., Soughayer, J., Pare, G. C., Michel, J. J. C., 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 (Pubitemid 41613557)
25. Diviani, D., Soderling, J. and Scott, J. D. (2001) AKAP-Lbc anchors protein kinase A and nucleates Gα12-selective Rho-mediated stress fiber formation. J. Biol. Chem. 276, 44247-44257
26. Fan, G. C., Chu, G. X., Song, Q. J. and Kranias, E. G. (2003) Phosphorylation of cardiac HSP20 increases contractility and protects myocytes from β-agonist-induced apoptosis. Circulation 108, 541
27. Carr, D. W., Hausken, Z. E., Fraser, I. D. C., Stofkohahn, R. E. and Scott, J. D. (1992) Association of the type-II cAMP-dependent protein-kinase with a human thyroid RII-anchoring protein - cloning and characterization of the RII binding domain. J. Biol. Chem. 267, 13376-13382
28. Chen, L. and Kass, R. S. (2011) A-Kinase anchoring protein 9 and IKs channel regulation. J. Cardiovasc. Pharmacol. 58, 459-461
29. Carnegie, G. K., Smith, F. D., McConnachie, G., Langeberg, L. and Scott, J. D. (2004) AKAP-Lbc nucleates a protein kinase D activation scaffold. Mol. Cell 15, 889-899 (Pubitemid 39277986)
30. 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, 1242-1287
31. Leroy, J., Richter, W., Mika, D., Castro, L. R. V., Abi-Gerges, A., Xie, M., Scheitrum, C., Lefebvre, F., Schittl, J., Mateo, P. et al. (2011) Phosphodiesterase 4B in the cardiac L-type Ca2+ channel complex regulates Ca2+ current and protects against ventricular arrhythmias in mice. J. Clin. Invest. 121, 2651-2661
32. Wang, H.-Y., Tao, J., Shumay, E. and Malbon, C. C. (2006) G-protein-coupled receptor-associated A-kinase anchoring proteins: AKAP79 and AKAP250 (gravin). Eur. J. Cell Biol. 85, 643-650 (Pubitemid 43863029)
33. Rembold, C. M., Foster, D. B., Strauss, J. D., Wingard, C. J. and Van Eyk, J. E. (2000) cGMP-mediated phosphorylation of heat shock protein 20 may cause smooth muscle relaxation without myosin light chain dephosphorylation in swine carotid artery. J. Physiol. 524, 865-878
34. Brophy, C. M., Woodrum, D. A., Pollock, J., Dickinson, M., Komalavilas, P., Cornwell, T. L. and Lincoln, T. M. (2002) cGMP-dependent protein kinase expression restores contractile function in cultured vascular smooth muscle cells. J. Vasc. Res. 39, 95-103 (Pubitemid 34507635)
35. Cariolato, L., Cavin, S. and Diviani, D. (2011) A-kinase anchoring protein (AKAP)-Lbc anchors a PKN-based signaling complex involved in α1-adrenergic receptor-induced p38 activation. J. Biol. Chem. 286, 7925-7937
36. Appert-Collin, A., Cotecchia, S., Nenninger-Tosato, M., Pedrazzini, T. and Diviani, D. (2007) The A-kinase anchoring protein (AKAP)-Lbc-signaling complex mediates α-1 adrenergic receptor-induced cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 104, 10140-10145 (Pubitemid 47175276)
37. Brown, J. H., Del Re, D. P. and Sussman, M. A. (2006) The Rac and Rho hall of fame: a decade of hypertrophic signaling hits. Circ. Res. 98, 730-742
38. Chang, Z. F. and Lee, H. H. (2006) RhoA signaling in phorbol ester-induced apoptosis. J. Biomed. Sci. 13, 173-180
39. Jin, J., Smith, F. D., Stark, C., Wells, C. D., Fawcett, J. P., Kulkarni, S., Metalnikov, P., O'Donnell, P., Taylor, P., Taylor, L. et al. (2004) Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr. Biol. 14, 1436-1450 (Pubitemid 39123741)
40. Diviani, D., Abuin, L., Cotecchia, S. and Pansier, L. (2004) Anchoring of both PKA and 14-3-3 inhibits the Rho-GEF activity of the AKAP-Lbc signaling complex. EMBO J. 23, 2811-2820 (Pubitemid 39013553)
41. Mayers, C. M., Wadell, J., McLean, K., Venere, M., Malik, M., Shibata, T., Driggers, P. H., Kino, T., Guo, X. C., Koide, H. et al. (2010) Rho guanine nucleotide exchange factor AKAP13 (BRX) is essential for cardiac development in mice. J. Biol. Chem. 285, 12344-12354
42. Neuer, A., Spandorfer, S. D., Giraldo, P., Dieterle, S., Rosenwaks, Z. and Witkin, S. S. (2000) The role of heat shock proteins in reproduction. Hum. Reprod. Update 6, 149-159 (Pubitemid 30182296)
43. Qian, J., Vafiadaki, E., Florea, S. M., Singh, V. P., Song, W., Lam, C. K., Wang, Y., Yuan, Q., Pritchard, T. J., Cai, W. et al. (2011) Small heat shock protein 20 interacts with protein phosphatase-1 and enhances sarcoplasmic reticulum calcium cycling. Circ. Res. 108, 1429-1438