Microdomain switch of cGMP-regulated phosphodiesterases leads to ANP-induced augmentation of β-adrenoceptor-stimulated contractility in early cardiac hypertrophy

Circulation Research

Volumn 116, Issue 8, 2015, Pages 1304-1311

  Perera, Ruwan K ^a,b,c,d   Sprenger, Julia U ^a,b,c,d   Steinbrecher, Julia H ^b,c   Hübscher, Daniela ^a,b,c   Lehnart, Stephan E ^b,c   Abesser, Marco ^e   Schuh, Kai ^e   El Armouche, Ali ^b,c,f   Nikolaev, Viacheslav O ^a,b,c,d  

^a Deutsche Forschungsgemeinschaft   (Germany)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d German Center for Cardiovascular Research   (Germany)

^e UNIVERSITY OF WÜRZBURG   (Germany)

^f DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

3',5' cyclic AMP phosphodiesterases; Atrial natriuretic factor; Hypertrophy; Membrane microdomains; Phosphodiesterase 3 inhibitors; Receptors, adrenergic

Indexed keywords

ATRIAL NATRIURETIC FACTOR; BETA ADRENERGIC RECEPTOR; CYCLIC AMP; CYCLIC GMP; PHOSPHODIESTERASE; BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CYCLIC AMP PHOSPHODIESTERASE; CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 2; GUANINE NUCLEOTIDE EXCHANGE FACTOR; ISOPRENALINE; PHOSPHODIESTERASE III;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEART MUSCLE CONTRACTILITY; HEART VENTRICLE HYPERTROPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CARDIOMEGALY; CELL MEMBRANE; DISEASE MODEL; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; FEMALE; GENETIC PROCEDURES; GENETICS; HEART CONTRACTION; HEART MUSCLE CELL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN TRANSPORT; SECOND MESSENGER; TIME; TRANSGENIC MOUSE;

3',5'-CYCLIC-AMP PHOSPHODIESTERASES; ADRENERGIC BETA-AGONISTS; ANIMALS; ATRIAL NATRIURETIC FACTOR; BIOSENSING TECHNIQUES; CARDIOMEGALY; CYCLIC GMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 2; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 3; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GUANINE NUCLEOTIDE EXCHANGE FACTORS; ISOPROTERENOL; MEMBRANE MICRODOMAINS; MICE; MICE, TRANSGENIC; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PROTEIN TRANSPORT; RECEPTOR CROSS-TALK; RECEPTORS, ADRENERGIC, BETA; RECEPTORS, ADRENERGIC, BETA-1; RECEPTORS, ADRENERGIC, BETA-2; SECOND MESSENGER SYSTEMS; TIME FACTORS;

EID: 84930816052     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.306082     Document Type: Article

References (24)

1. Perino A, Ghigo A, Scott JD, Hirsch E., Anchoring proteins as regulators of signaling pathways. Circ Res 2012; 111: 482-492. doi: 10.1161/CIRCRESAHA.111.262899
2. Perera RK, Nikolaev VO., Compartmentation of cAMP signalling in cardiomyocytes in health and disease. Acta Physiol (Oxf) 2013; 207: 650-662. doi: 10.1111/apha.12077
3. Zaccolo M, Movsesian MA., cAMP and cGMP signaling cross-talk: role of phosphodiesterases and implications for cardiac pathophysiology. Circ Res 2007; 100: 1569-1578. doi: 10.1161/CIRCRESAHA.106.144501
4. Stangherlin A, Gesellchen F, Zoccarato A, Terrin A, Fields LA, Berrera M, Surdo NC, Craig MA, Smith G, Hamilton G, Zaccolo M., cGMP signals modulate cAMP levels in a compartment-specific manner to regulate catecholamine-dependent signaling in cardiac myocytes. Circ Res 2011; 108: 929-939. doi: 10.1161/CIRCRESAHA.110.230698
5. Xiao RP., Beta-adrenergic signaling in the heart: dual coupling of the beta2-adrenergic receptor to G(s) and G(i) proteins. Sci STKE 2001; 2001: re15. doi: 10.1126/stke.2001.104.re15
6. Nikolaev VO, Moshkov A, Lyon AR, Miragoli M, Novak P, Paur H, Lohse MJ, Korchev YE, Harding SE, Gorelik J., Beta2-adrenergic receptor redistribution in heart failure changes cAMP compartmentation. Science 2010; 327: 1653-1657. doi: 10.1126/science.1185988
7. Tsai EJ, Kass DA., Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics. Pharmacol Ther 2009; 122: 216-238. doi: 10.1016/j.pharmthera.2009.02.009
8. Holtwick R, van Eickels M, Skryabin BV, Baba HA, Bubikat A, Begrow F, Schneider MD, Garbers DL, Kuhn M., Pressure-independent cardiac hypertrophy in mice with cardiomyocyte-restricted inactivation of the atrial natriuretic peptide receptor guanylyl cyclase-A. J Clin Invest 2003; 111: 1399-1407. doi: 10.1172/JCI17061
9. Knowles JW, Esposito G, Mao L, Hagaman JR, Fox JE, Smithies O, Rockman HA, Maeda N., Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice. J Clin Invest 2001; 107: 975-984. doi: 10.1172/JCI11273
10. Bristow MR, Ginsburg R, Minobe W, Cubicciotti RS, Sageman WS, Lurie K, Billingham ME, Harrison DC, Stinson EB., Decreased catecholamine sensitivity and beta-adrenergic-receptor density in failing human hearts. N Engl J Med 1982; 307: 205-211. doi: 10.1056/NEJM198207223070401
11. Kuhn M., Structure, regulation, and function of mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclase-A. Circ Res 2003; 93: 700-709. doi: 10.1161/01.RES.0000094745.28948.4D
12. Börner S, Schwede F, Schlipp A, Berisha F, Calebiro D, Lohse MJ, Nikolaev VO., FRET measurements of intracellular cAMP concentrations and cAMP analog permeability in intact cells. Nat Protoc 2011; 6: 427-438. doi: 10.1038/nprot.2010.198
13. Götz KR, Sprenger JU, Perera RK, Steinbrecher JH, Lehnart SE, Kuhn M, Gorelik J, Balligand JL, Nikolaev VO., Transgenic mice for real-time visualization of cGMP in intact adult cardiomyocytes. Circ Res 2014; 114: 1235-1245. doi: 10.1161/CIRCRESAHA.114.302437
14. Takimoto E, Belardi D, Tocchetti CG, Vahebi S, Cormaci G, Ketner EA, Moens AL, Champion HC, Kass DA., Compartmentalization of cardiac beta-adrenergic inotropy modulation by phosphodiesterase type 5. Circulation 2007; 115: 2159-2167. doi: 10.1161/CIRCULATIONAHA.106.643536
15. Lohse MJ, Engelhardt S, Eschenhagen T., What is the role of beta-adrenergic signaling in heart failure? Circ Res 2003; 93: 896-906. doi: 10.1161/01.RES.0000102042.83024.CA
16. Lainchbury JG, Burnett JC Jr, Meyer D, Redfield MM., Effects of natriuretic peptides on load and myocardial function in normal and heart failure dogs. Am J Physiol Heart Circ Physiol 2000; 278: H33-H40.
17. Ohte N, Cheng CP, Suzuki M, Little WC., Effects of atrial natriuretic peptide on left ventricular performance in conscious dogs before and after pacing-induced heart failure. J Pharmacol Exp Ther 1999; 291: 589-595.
18. Abi-Gerges A, Richter W, Lefebvre F, Mateo P, Varin A, Heymes C, Samuel JL, Lugnier C, Conti M, Fischmeister R, Vandecasteele G., Decreased expression and activity of cAMP phosphodiesterases in cardiac hypertrophy and its impact on beta-adrenergic cAMP signals. Circ Res 2009; 105: 784-792. doi: 10.1161/CIRCRESAHA.109.197947
19. Ding B, Abe J, Wei H, Huang Q, Walsh RA, Molina CA, Zhao A, Sadoshima J, Blaxall BC, Berk BC, Yan C., Functional role of phosphodiesterase 3 in cardiomyocyte apoptosis: implication in heart failure. Circulation 2005; 111: 2469-2476. doi: 10.1161/01.CIR.0000165128.39715.87
20. Castro LR, Verde I, Cooper DM, Fischmeister R., Cyclic guanosine monophosphate compartmentation in rat cardiac myocytes. Circulation 2006; 113: 2221-2228. doi: 10.1161/CIRCULATIONAHA.105.599241
21. Mehel H, Emons J, Vettel C, Phosphodiesterase-2 is up-regulated in human failing hearts and blunts β-adrenergic responses in cardiomyocytes. J Am Coll Cardiol 2013; 62: 1596-1606. doi: 10.1016/j.jacc.2013.05.057
22. Richter W, Day P, Agrawal R, Bruss MD, Granier S, Wang YL, Rasmussen SG, Horner K, Wang P, Lei T, Patterson AJ, Kobilka B, Conti M., Signaling from beta1-and beta2-adrenergic receptors is defined by differential interactions with PDE4. EMBO J 2008; 27: 384-393. doi: 10.1038/sj.emboj.7601968
23. Patrucco E, Albergine MS, Santana LF, Beavo JA., Phosphodiesterase 8A (PDE8A) regulates excitation-contraction coupling in ventricular myocytes. J Mol Cell Cardiol 2010; 49: 330-333. doi: 10.1016/j.yjmcc.2010.03.016
24. Shakur Y, Takeda K, Kenan Y, Yu ZX, Rena G, Brandt D, Houslay MD, Degerman E, Ferrans VJ, Manganiello VC., Membrane localization of cyclic nucleotide phosphodiesterase 3 (PDE3). Two N-terminal domains are required for the efficient targeting to, and association of, PDE3 with endoplasmic reticulum. J Biol Chem 2000; 275: 38749-38761. doi: 10.1074/jbc.M001734200