Control of cytoplasmic and nuclear protein kinase A by phosphodiesterases and phosphatases in cardiac myocytes

Cardiovascular Research

Volumn 102, Issue 1, 2014, Pages 97-106

  Haj Slimane, Zeineb ^a,b   Bedioune, Ibrahim ^a,b   Lechêne, Patrick ^a,b   Varin, Audrey ^a,b   Lefebvre, Florence ^a,b   Mateo, Philippe ^a,b   Domergue Dupont, Valérie ^b   Dewenter, Matthias ^c   Richter, Wito ^d   Conti, Marco ^d   El Armouche, Ali ^c,e   Zhang, Jin ^f   Fischmeister, Rodolphe ^a,b   Vandecasteele, Grégoire ^a,b  

^a Universite Paris Sud   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

3 5 cyclic nucleotide phosphodiesterases; cAMP dependent protein kinase; Compartmentation; Nucleus; Ser Thr protein phosphatases

Indexed keywords

3 ISOBUTYL 1 METHYLXANTINE; ADENYLATE CYCLASE; CALCINEURIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ISOPRENALINE; MYOSIN BINDING PROTEIN C; PHOSPHODIESTERASE III; PHOSPHODIESTERASE IV; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; UNCLASSIFIED DRUG; ADRENERGIC RECEPTOR; CARDIOTONIC AGENT; CYCLIC AMP; NUCLEAR PROTEIN; PHOSPHATASE; PHOSPHODIESTERASE; PHOSPHODIESTERASE INHIBITOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME KINETICS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION REGULATION; HEART MUSCLE CELL; MALE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; RAT; SPATIOTEMPORAL ANALYSIS; ANIMAL; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; CARDIOTONIC AGENTS; CELL NUCLEUS; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; ISOPROTERENOL; MALE; MYOCYTES, CARDIAC; NUCLEAR PROTEINS; PHOSPHODIESTERASE INHIBITORS; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; RATS, WISTAR; RECEPTORS, ADRENERGIC; SIGNAL TRANSDUCTION;

EID: 84896922824     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu029     Document Type: Article

References (43)

1. Tasken K, Aandahl EM. Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol Rev 2004;84:137-167.
2. Bers DM. Cardiac excitation-contraction coupling. Nature 2002;415:198-205.
3. Scott JD, Santana LF. A-kinase anchoring proteins: getting to the heart of the matter. Circulation 2010;121:1264-1271.
4. Mika D, Leroy J, Vandecasteele G, Fischmeister R. PDEs create local domains of cAMP signaling. J Mol Cell Cardiol 2012;52:323-329.
5. Herzig S, Neumann J. Effectsofserine/threonine protein phosphatasesonion channels in excitable membranes. Physiol Rev 2000;80:173-210.
6. 2+ channel regulation in adult rat ventricular myocytes: role of phosphodiesterases. Circ Res 2008;102: 1091-1100.
7. Saucerman JJ, Zhang J, Martin JC, Peng LX, Stenbit AE, Tsien RY et al. Systems analysis of PKA-mediated phosphorylation gradientsin live cardiac myocytes. Proc Natl Acad Sci USA 2006;103:12923-12928.
8. Muller FU, Neumann J, Schmitz W. Transcriptional regulation by cAMP in the heart. Mol Cell Biochem 2000;212:11-17.
9. Ha CH, Kim JY, Zhao J, Wang W, Jhun BS, Wong C et al. PKA phosphorylates histone deacetylase 5 and prevents its nuclear export, leading to the inhibition of gene transcription and cardiomyocyte hypertrophy. Proc Natl Acad Sci USA 2010;107:15467-15472.
10. Backs J, Worst BC, Lehmann LH, Patrick DM, Jebessa Z, Kreusser MM et al. Selective re-pressionofMEF2 activity by PKA-dependent proteolysis of HDAC4. J Cell Biol 2011;195: 403-415.
11. Chang CW, Lee L, Yu D, Dao K, Bossuyt J, Bers DM. Acute beta-adrenergic activation triggers nuclear import of histone deacetylase 5 and delays Gq-induced transcriptional activation. J Biol Chem 2013;288:192-204.
12. Harootunian AT, Adams SR, Wen W, Meinkoth JL, Taylor SS, Tsien RY. Movementofthe free catalytic subunit of cAMP-dependent protein kinase into and out of the nucleus can be explained by diffusion. Mol Biol Cell 1993;4:993-1002.
13. Sample V, Dipilato LM, Yang JH, Ni Q, Saucerman JJ, Zhang J. Regulation of nuclear PKA revealed by spatiotemporal manipulation of cyclic AMP. Nat Chem Biol 2012;8:375-382.
14. Yang J, Drazba JA, Ferguson DG, Bond M. A-kinase anchoring protein 100 (AKAP100) is localized in multiple subcellular compartments in the adult rat heart. J Cell Biol 1998;142: 511-522.
15. Kapiloff MS, Jackson N, Airhart N. mAKAP and the ryanodine receptor are part of a multi-component signaling complex on the cardiomyocyte nuclear envelope. J Cell Sci 2001;114:3167-3176.
16. Dodge KL, Khouangsathiene S, Kapiloff MS, Mouton R, Hill EV, Houslay MD et al. mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. EMBO J 2001;20:1921-1930.
17. Dodge-Kafka KL, Soughayer J, Pare GC, Carlisle Michel JJ, Langeberg LK, Kapiloff MS et al. The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature 2005;437:574-578.
18. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 2009;10: 32-42.
19. Tomita H, Nazmy M, Kajimoto K, Yehia G, Molina CA, Sadoshima J. Inducible cAMPearly repressor (ICER)is a negative-feedback regulatorof cardiac hypertrophy andan important mediator of cardiac myocyte apoptosis in response to beta-adrenergic receptor stimulation. Circ Res 2003;93:12-22.
20. Lewin G, Matus M, Basu A, Frebel K, Rohsbach SP, Safronenko A et al. Critical role of transcription factor cyclic AMP response element modulator in beta1-adrenoceptor-mediated cardiac dysfunction. Circulation 2009;119:79-88.
21. Di Pilato LM, Zhang J. The role of membrane microdomains in shaping beta2-adrenergic receptor-mediated cAMP dynamics. Mol Biosyst 2009;5:832-837.
22. Allen MD, Zhang J. Subcellular dynamics of protein kinase A activity visualized by FRET-based reporters. Biochem Biophys Res Commun 2006;348:716-721.
23. Rochais F, Vandecasteele G, Lefebvre F, Lugnier C, Lum H, Mazet JL et al. Negative feedback exerted by cAMP-dependent protein kinase and cAMP phosphodiesterase on subsarcolemmal cAMP signals in intact cardiac myocytes: an in vivo study using adenovirus-mediated expression of CNG channels. J Biol Chem 2004;279: 52095-52105.
24. Lum H, Jaffe HA, Schulz IT, Masood A, Ray Chaudhury A, Green RD. Expression of PKA inhibitor (PKI) gene abolishes cAMP-mediated protection to endothelial barrier dysfunction. Am J Physiol 1999;277:C580-C588.
25. Lugnier C, Keravis T, Le Bec A, Pauvert O, Proteau S, Rousseau E. Characterization of cyclic nucleotide phosphodiesterase isoforms associated to isolated cardiac nuclei. Biochim Biophys Acta 1999;1472:431-446.
26. Jin SL, Latour AM, Conti M. Generation of PDE4 knockout mice by gene targeting. Methods Mol Biol 2005;307:191-210.
27. Bialojan C, Takai A. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem J 1988;256:283-290.
28. Gervasi N, Hepp R, Tricoire L, Zhang J, Lambolez B, Paupardin-Tritsch D et al. Dynamics of protein kinase A signaling at the membrane, in the cytosol, and in the nucleus of neurons in mouse brain slices. J Neurosci 2007;27:2744-2750.
29. Pereira L, Ruiz-Hurtado G, Morel E, Laurent AC, Metrich M, Dominguez-Rodriguez A et al. Epac enhances excitation-transcription coupling in cardiac myocytes. J Mol Cell Cardiol 2012;52:283-291.
30. Metrich M, Lucas A, Gastineau M, Samuel JL, Heymes C, Morel E et al. Epac mediates beta-adrenergic receptor-induced cardiomyocyte hypertrophy. Circ Res 2008;102: 959-965.
31. Mc Kinsey TA, Zhang CL, Olson EN. Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc Natl Acad Sci USA 2000;97:14400-14405.
32. Vega RB, Harrison BC, Meadows E, Roberts CR, Papst PJ, Olson EN et al. Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol Cell Biol 2004;24:8374-8385.
33. 2+ signaling in cardiac myocyte excitation-transcription coupling. J Clin Invest 2006;116:675-682.
34. Xiang Y, Naro F, Zoudilova M, Jin SL, Conti M, Kobilka B. Phosphodiesterase 4D is required for {beta}2 adrenoceptor subtype-specific signaling in cardiac myocytes. Proc Natl Acad Sci USA 2005;102:909-914.
35. Lehnart SE, Wehrens XH, Reiken S, Warrier S, Belevych AE, Harvey RD et al. Phospho-diesterase 4Ddeficiency inthe ryanodine-receptor complex promotes heart failure and arrhythmias. Cell 2005;123:25-35.
36. 2+ current. Circ Res 2011;109:1024-1030.
37. Pare GC, Bauman AL, Mc Henry M, Michel JJ, Dodge-Kafka KL, Kapiloff MS. The mAKAP complex participates in the induction of cardiac myocyte hypertrophy by adrenergic receptor signaling. J Cell Sci 2005;118:5637-5646.
38. Lim HW, De Windt LJ, Steinberg L, Taigen T, Witt SA, Kimball TR et al. Calcineurin expression, activation, and function in cardiac pressure-overload hypertrophy. Circulation 2000;101:2431-2437.
39. Mac Donnell SM, Kubo H, Harris DM, Chen X, Berretta R, Barbe MF et al. Calcineurin inhibition normalizes beta-adrenergic responsivenessinthe spontaneously hypertensive rat. Am J Physiol Heart Circ Physiol 2007;293:H3122-H3129.
40. Hallhuber M, Burkard N, Wu R, Buch MH, Engelhardt S, Hein L et al. Inhibition of nuclear import of calcineurin prevents myocardial hypertrophy. Circ Res 2006;99: 626-635.
41. Yang JH, Polanowska-Grabowska RK, Smith JS, Shields CW IV, Saucerman JJ. PKA catalytic subunit compartmentation regulates contractile and hypertrophic responses to beta-adrenergic signaling. J Mol Cell Cardiol 2013;66C:83-93.
42. Bollen M, Beullens M. Signaling by protein phosphatases in the nucleus. Trends Cell Biol 2002;12:138-145.
43. Wittkopper K, Fabritz L, Neef S, Ort KR, Grefe C, Unsold B et al. Constitutively active phosphatase inhibitor-1 improves cardiac contractility in young mice but is deleterious after catecholaminergic stress and with aging. J Clin Invest 2010;120: 617-626.