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Compartmentation of Natriuretic Peptide Signalling in Cardiac Myocytes: Effects on Cardiac Contractility and Hypertrophy

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Microdomains in the Cardiovascular System

Part of the book series: Cardiac and Vascular Biology ((Abbreviated title: Card. vasc. biol.,volume 3))

Abstract

Natriuretic peptides have received considerable attention in the recent years both as biomarkers for heart failure and as treatment for the disease. Atrial (ANP) and B-type natriuretic peptide (BNP) stimulate the natriuretic peptide receptor (NPR)-A, whereas C-type natriuretic peptide (CNP) stimulates the NPR-B. Both NPR-A and NPR-B are guanylyl cyclases which generate cGMP when stimulated. All three peptides bind the NPR-C which does not possess guanylyl cyclase (GC) activity. Evidence is accumulating that natriuretic peptides are involved in regulating contractility and hypertrophic responses through a complex system of signalling pathways, both cGMP dependent and independent, in different compartments in cardiomyocytes. This review discusses compartmentalisation of natriuretic peptide signalling in cardiomyocytes, with focus on contractile and antihypertrophic effects in healthy and diseased hearts.

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Notes

  1. 1.

    https://clinicaltrials.gov/ct2/show/NCT00839007, https://clinicaltrials.gov/ct2/show/NCT00620308, https://clinicaltrials.gov/ct2/show/NCT02071602, https://clinicaltrials.gov/ct2/show/NCT01750905, https://clinicaltrials.gov/ct2/show/nct02359227

  2. 2.

    https://clinicaltrials.gov/ct2/show/NCT01920711

References

  • Aass H, Skomedal T, Osnes JB (1988) Increase of cyclic AMP in subcellular fractions of rat heart muscle after beta-adrenergic stimulation: prenalterol and isoprenaline caused different distribution of bound cyclic AMP. J Mol Cell Cardiol 20:847–860

    CAS  PubMed  Google Scholar 

  • Abraham WT, Lowes BD, Ferguson DA, Odom J, Kim JK, Robertson AD, Bristow MR, Schrier RW (1998) Systemic hemodynamic, neurohormonal, and renal effects of a steady-state infusion of human brain natriuretic peptide in patients with hemodynamically decompensated heart failure. J Card Fail 4:37–44

    CAS  PubMed  Google Scholar 

  • Afzal F, Andressen KW, Mørk HK, Aronsen JM, Sjaastad I, Dahl CP, Skomedal T, Levy FO, Osnes JB, Qvigstad E (2008) 5-HT4-elicited positive inotropic response is mediated by cAMP and regulated by PDE3 in failing rat and human cardiac ventricles. Br J Pharmacol 155:1005–1014. doi:10.1038/bjp.2008.339 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Afzal F, Qvigstad E, Aronsen JM, Moltzau LR, Sjaastad I, Skomedal T, Osnes JB, Levy FO (2011) Agents increasing cyclic GMP amplify 5-HT4-elicited positive inotropic response in failing rat cardiac ventricle. Naunyn Schmiedebergs Arch Pharmacol 384:543–553. doi:10.1007/s00210-011-0670-6 [doi]

    Google Scholar 

  • Airhart N, Yang YF, Roberts CT Jr, Silberbach M (2003) Atrial natriuretic peptide induces natriuretic peptide receptor-cGMP-dependent protein kinase interaction. J Biol Chem 278:38693–38698. doi:10.1074/jbc.M304098200 [doi]; M304098200 [pii]

    Google Scholar 

  • Amsallem E, Kasparian C, Haddour G, Boissel JP, Nony P (2005) Phosphodiesterase III inhibitors for heart failure. Cochrane Database Syst Rev CD002230. doi:10.1002/14651858.CD002230.pub2 [doi]

    Google Scholar 

  • Anand-Srivastava MB, Cantin M (1986) Atrial natriuretic factor receptors are negatively coupled to adenylate cyclase in cultured atrial and ventricular cardiocytes. Biochem Biophys Res Commun 138:427–436. doi:0006-291X(86)90299-8 [pii]

    Google Scholar 

  • Anand-Srivastava MB, Sairam MR, Cantin M (1990) Ring-deleted analogs of atrial natriuretic factor inhibit adenylate cyclase/cAMP system. Possible coupling of clearance atrial natriuretic factor receptors to adenylate cyclase/cAMP signal transduction system. J Biol Chem 265:8566–8572

    Google Scholar 

  • Ashman DF, Lipton R, Melicow MM, Price TD (1963) Isolation of adenosine 3', 5'-monophosphate and guanosine 3', 5'-monophosphate from rat urine. Biochem Biophys Res Commun 11:330–334

    CAS  PubMed  Google Scholar 

  • Bach T, Bergholtz S, Riise J, Qvigstad E, Skomedal T, Osnes JB, Levy FO (2014) Identification of small molecule NPR-B antagonists by high throughput screening—potential use in heart failure. Naunyn Schmiedebergs Arch Pharmacol 387:5–14. doi:10.1007/s00210-013-0940-6 [doi]

    Google Scholar 

  • Beaulieu P, Cardinal R, Page P, Francoeur F, Tremblay J, Lambert C (1997) Positive chronotropic and inotropic effects of C-type natriuretic peptide in dogs. Am J Phys 273:H1933–H1940

    CAS  Google Scholar 

  • Boerrigter G, Lapp H, Burnett JC (2009) Modulation of cGMP in heart failure: a new therapeutic paradigm. Handb Exp Pharmacol 191:485–506. doi:10.1007/978-3-540-68964-5_21 [doi]

    Google Scholar 

  • Brusq JM, Mayoux E, Guigui L, Kirilovsky J (1999) Effects of C-type natriuretic peptide on rat cardiac contractility. Br J Pharmacol 128:206–212. doi:10.1038/sj.bjp.0702766 [doi]

    Google Scholar 

  • Bubikat A, De Windt LJ, Zetsche B, Fabritz L, Sickler H, Eckardt D, Godecke A, Baba HA, Kuhn M (2005) Local atrial natriuretic peptide signaling prevents hypertensive cardiac hypertrophy in endothelial nitric-oxide synthase-deficient mice. J Biol Chem 280:21594–21599. doi:10.1074/jbc.M501103200

    Article  CAS  PubMed  Google Scholar 

  • Burley DS, Cox CD, Zhang J, Wann KT, Baxter GF (2014) Natriuretic peptides modulate ATP-sensitive K+ channels in rat ventricular cardiomyocytes. Basic Res Cardiol 109:402. doi:10.1007/s00395-014-0402-4

  • Buxton IL, Brunton LL (1983) Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes. J Biol Chem 258:10233–10239

    CAS  PubMed  Google Scholar 

  • Cabiati M, Campan M, Caselli C, Prescimone T, Giannessi D, Del Ry S (2010) Sequencing and cardiac expression of natriuretic peptide receptors A and C in normal and heart failure pigs. Regul Pept 162:12–17. doi:10.1016/j.regpep.2010.02.004

    Article  CAS  PubMed  Google Scholar 

  • Calderone A, Thaik CM, Takahashi N, Chang DL, Colucci WS (1998) Nitric oxide, atrial natriuretic peptide, and cyclic GMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts. J Clin Invest 101:812–818. doi:10.1172/jci119883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calvieri C, Rubattu S, Volpe M (2012) Molecular mechanisms underlying cardiac antihypertrophic and antifibrotic effects of natriuretic peptides. J Mol Med (Berl) 90:5–13. doi:10.1007/s00109-011-0801-z [doi]

    Google Scholar 

  • Carnegie GK, Means CK, Scott JD (2009) A-kinase anchoring proteins: from protein complexes to physiology and disease. IUBMB Life 61:394–406. doi:10.1002/iub.168 [doi]

    CAS  PubMed  Google Scholar 

  • Castro LR, Schittl J, Fischmeister R (2010) Feedback control through cGMP-dependent protein kinase contributes to differential regulation and compartmentation of cGMP in rat cardiac myocytes. Circ Res 107:1232–1240. doi:CIRCRESAHA.110.226712 [pii]; 10.1161/CIRCRESAHA.110.226712 [doi]

    Google Scholar 

  • Castro LR, Verde I, Cooper DM, Fischmeister R (2006) Cyclic guanosine monophosphate compartmentation in rat cardiac myocytes. Circulation 113:2221–2228. doi:CIRCULATIONAHA.105.599241 [pii]; 10.1161/CIRCULATIONAHA.105.599241 [doi]

    Google Scholar 

  • Chen Y, Yao F, Chen S, Huang H, Wu L, He J, Dong Y (2014) Endogenous BNP attenuates cardiomyocyte hypertrophy induced by Ang II via p38 MAPK/Smad signaling. Die Pharmazie 69:833–837

    Google Scholar 

  • Colson BA, Locher MR, Bekyarova T, Patel JR, Fitzsimons DP, Irving TC, Moss RL (2010) Differential roles of regulatory light chain and myosin binding protein-C phosphorylations in the modulation of cardiac force development. J Physiol 588:981–993. doi:jphysiol.2009.183897 [pii]; 10.1113/jphysiol.2009.183897 [doi]

    Google Scholar 

  • Colucci WS, Elkayam U, Horton DP, Abraham WT, Bourge RC, Johnson AD, Wagoner LE, Givertz MM, Liang CS, Neibaur M, Haught WH, LeJemtel TH, Nesiritide Study Group. (2000) Intravenous nesiritide, a natriuretic peptide, in the treatment of decompensated congestive heart failure. N Engl J Med 343:246–253. doi:10.1056/NEJM200007273430403 [doi]

    Google Scholar 

  • Corradini E, Burgers PP, Plank M, Heck AJ, Scholten A (2015) Huntingtin-associated protein 1 (HAP1) is a cGMP-dependent kinase anchoring protein (GKAP) specific for the cGMP-dependent protein kinase Ibeta isoform. J Biol Chem 290:7887–7896. doi:10.1074/jbc.M114.622613

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Bold AJ, Borenstein HB, Veress AT, Sonnenberg H (1981) A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sci 28:89–94

    PubMed  Google Scholar 

  • Del Ry S, Cabiati M, Vozzi F, Battolla B, Caselli C, Forini F, Segnani C, Prescimone T, Giannessi D, Mattii L (2011) Expression of C-type natriuretic peptide and its receptor NPR-B in cardiomyocytes. Peptides 32:1713–1718. doi:S0196-9781(11)00239-7 [pii]; 10.1016/j.peptides.2011.06.014 [doi]

    Google Scholar 

  • Del Ry S, Passino C, Maltinti M, Emdin M, Giannessi D (2005) C-type natriuretic peptide plasma levels increase in patients with chronic heart failure as a function of clinical severity. Eur J Heart Fail 7:1145–1148. doi:S1388-9842(04)00378-2 [pii]; 10.1016/j.ejheart.2004.12.009 [doi]

    Google Scholar 

  • Di Benedetto G, Zoccarato A, Lissandron V, Terrin A, Li X, Houslay MD, Baillie GS, Zaccolo M (2008) Protein kinase A type I and type II define distinct intracellular signaling compartments. Circ Res 103:836–844. doi:CIRCRESAHA.108.174813 [pii]; 10.1161/CIRCRESAHA.108.174813 [doi]

    Google Scholar 

  • Dickey DM, Burnett JC Jr, Potter LR (2008) Novel bifunctional natriuretic peptides as potential therapeutics. J Biol Chem 283:35003–35009. doi:M804538200 [pii]; 10.1074/jbc.M804538200 [doi]

    Google Scholar 

  • Dickey DM, Dries DL, Margulies KB, Potter LR (2011) Guanylyl cyclase (GC)-A and GC-B activities in ventricles and cardiomyocytes from failed and non-failed human hearts: GC-A is inactive in the failed cardiomyocyte. J Mol Cell Cardiol. doi:S0022-2828(11)00473-1 [pii]; 10.1016/j.yjmcc.2011.11.007 [doi]

    Google Scholar 

  • Dickey DM, Flora DR, Bryan PM, Xu X, Chen Y, Potter LR (2007) Differential regulation of membrane guanylyl cyclases in congestive heart failure: natriuretic peptide receptor (NPR)-B, Not NPR-A, is the predominant natriuretic peptide receptor in the failing heart. Endocrinology 148:3518–3522. doi:en.2007-0081 [pii]; 10.1210/en.2007-0081 [doi]

    Google Scholar 

  • Dickstein K, Cohen-Solal A, Filippatos G, McMurray JJ, Ponikowski P, Poole-Wilson PA, Stromberg A, van Veldhuisen DJ, Atar D, Hoes AW, Keren A, Mebazaa A, Nieminen M, Priori SG, Swedberg K (2008) ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure 2008: the Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2008 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association of the ESC (HFA) and endorsed by the European Society of Intensive Care Medicine (ESICM). Eur Heart J 29:2388–2442.

    Google Scholar 

  • Doyle DD, Upshaw-Earley J, Bell EL, Palfrey HC (2002) Natriuretic peptide receptor-B in adult rat ventricle is predominantly confined to the nonmyocyte population. Am J Physiol Heart Circ Physiol 282:H2117–H2123. doi:10.1152/ajpheart.00988.2001 [doi]

    Google Scholar 

  • El-Armouche A, Eschenhagen T (2009) Beta-adrenergic stimulation and myocardial function in the failing heart. Heart Fail Rev 14:225–241. doi:10.1007/s10741-008-9132-8 [doi]

    Google Scholar 

  • Fabiato A, Fabiato F (1978) Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. J Physiol 276:233–255

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fischmeister R, Hartzell HC (1987) Cyclic guanosine 3',5'-monophosphate regulates the calcium current in single cells from frog ventricle. J Physiol 387:453–472

    CAS  PubMed  PubMed Central  Google Scholar 

  • Francis SH, Busch JL, Corbin JD, Sibley D (2010) cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 62:525–563. doi:62/3/525 [pii]; 10.1124/pr.110.002907 [doi]

    Google Scholar 

  • Frantz S, Klaiber M, Baba HA, Oberwinkler H, Volker K, Gabetaner B, Bayer B, Abebetaer M, Schuh K, Feil R, Hofmann F, Kuhn M (2013) Stress-dependent dilated cardiomyopathy in mice with cardiomyocyte-restricted inactivation of cyclic GMP-dependent protein kinase I. Eur Heart J 34:1233–1244. doi:ehr445 [pii]; 10.1093/eurheartj/ehr445 [doi]

    Google Scholar 

  • Gisbert MP, Fischmeister R (1988) Atrial natriuretic factor regulates the calcium current in frog isolated cardiac cells. Circ Res 62:660–667

    CAS  PubMed  Google Scholar 

  • Götz KR, Sprenger JU, Perera RK, Steinbrecher JH, Lehnart SE, Kuhn M, Gorelik J, Balligand JL, Nikolaev VO (2014) Transgenic mice for real-time visualization of cGMP in intact adult cardiomyocytes. Circ Res 114:1235–1245. doi:10.1161/circresaha.114.302437

    Article  PubMed  Google Scholar 

  • Hartzell HC, Fischmeister R (1986) Opposite effects of cyclic GMP and cyclic AMP on Ca2+ current in single heart cells. Nature 323:273–275. doi:10.1038/323273a0 [doi]

    Google Scholar 

  • Hayashi D, Kudoh S, Shiojima I, Zou Y, Harada K, Shimoyama M, Imai Y, Monzen K, Yamazaki T, Yazaki Y, Nagai R, Komuro I (2004) Atrial natriuretic peptide inhibits cardiomyocyte hypertrophy through mitogen-activated protein kinase phosphatase-1. Biochem Biophys Res Commun 322:310–319. doi:10.1016/j.bbrc.2004.07.119

    Article  CAS  PubMed  Google Scholar 

  • Hayes JS, Brunton LL, Brown JH, Reese JB, Mayer SE (1979) Hormonally specific expression of cardiac protein kinase activity. Proc Natl Acad Sci U S A 76:1570–1574

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirose M, Furukawa Y, Kurogouchi F, Nakajima K, Miyashita Y, Chiba S (1998) C-type natriuretic peptide increases myocardial contractility and sinus rate mediated by guanylyl cyclase-linked natriuretic peptide receptors in isolated, blood-perfused dog heart preparations. J Pharmacol Exp Ther 286:70–76

    CAS  PubMed  Google Scholar 

  • Holmes SJ, Espiner EA, Richards AM, Yandle TG, Frampton C (1993) Renal, endocrine, and hemodynamic effects of human brain natriuretic peptide in normal man. J Clin Endocrinol Metab 76:91–96

    CAS  PubMed  Google Scholar 

  • Holtwick R, van Eickels M, Skryabin BV, Baba HA, Bubikat A, Begrow F, Schneider MD, Garbers DL, Kuhn M (2003) Pressure-independent cardiac hypertrophy in mice with cardiomyocyte-restricted inactivation of the atrial natriuretic peptide receptor guanylyl cyclase-A. J Clin Invest 111:1399–1407. doi:10.1172/jci17061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Honda A, Adams SR, Sawyer CL, Lev-Ram V, Tsien RY, Dostmann WR (2001) Spatiotemporal dynamics of guanosine 3',5'-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc Natl Acad Sci U S A 98:2437–2442. doi:10.1073/pnas.051631298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horio T, Nishikimi T, Yoshihara F, Matsuo H, Takishita S, Kangawa K (2000) Inhibitory regulation of hypertrophy by endogenous atrial natriuretic peptide in cultured cardiac myocytes. Hypertension 35:19–24

    CAS  PubMed  Google Scholar 

  • Horio T, Tokudome T, Maki T, Yoshihara F, Suga S, Nishikimi T, Kojima M, Kawano Y, Kangawa K (2003) Gene expression, secretion, and autocrine action of C-type natriuretic peptide in cultured adult rat cardiac fibroblasts. Endocrinology 144:2279–2284

    CAS  PubMed  Google Scholar 

  • Hunt PJ, Richards AM, Espiner EA, Nicholls MG, Yandle TG (1994) Bioactivity and metabolism of C-type natriuretic peptide in normal man. J Clin Endocrinol Metab 78:1428–1435

    CAS  PubMed  Google Scholar 

  • Izumiya Y, Araki S, Usuku H, Rokutanda T, Hanatani S, Ogawa H (2012) Chronic C-Type natriuretic peptide infusion attenuates angiotensin II-Induced myocardial superoxide production and cardiac Remodeling. Int J Vasc Med 2012:246058. doi:10.1155/2012/246058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaumann AJ, Birnbaumer L (1974) Prostaglandin E1 action on sinus pacemaker and adenylyl cyclase in kitten myocardium. Nature 251:515–517

    CAS  PubMed  Google Scholar 

  • Kilic A, Rajapurohitam V, Sandberg SM, Zeidan A, Hunter JC, Said Faruq N, Lee CY, Burnett JC Jr, Karmazyn M (2010) A novel chimeric natriuretic peptide reduces cardiomyocyte hypertrophy through the NHE-1-calcineurin pathway. Cardiovasc Res 88:434–442. doi:10.1093/cvr/cvq254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kilic A, Velic A, De Windt LJ, Fabritz L, Voss M, Mitko D, Zwiener M, Baba HA, van Eickels M, Schlatter E, Kuhn M (2005) Enhanced activity of the myocardial Na+/H+ exchanger NHE-1 contributes to cardiac remodeling in atrial natriuretic peptide receptor-deficient mice. Circulation 112:2307–2317. doi:10.1161/circulationaha.105.542209

    CAS  PubMed  Google Scholar 

  • Kinoshita H, Kuwahara K, Nishida M, Jian Z, Rong X, Kiyonaka S, Kuwabara Y, Kurose H, Inoue R, Mori Y, Li Y, Nakagawa Y, Usami S, Fujiwara M, Yamada Y, Minami T, Ueshima K, Nakao K (2010) Inhibition of TRPC6 channel activity contributes to the antihypertrophic effects of natriuretic peptides-guanylyl cyclase-A signaling in the heart. Circ Res 106:1849–1860. doi:10.1161/circresaha.109.208314

    Article  CAS  PubMed  Google Scholar 

  • Kishimoto I, Rossi K, Garbers DL (2001) A genetic model provides evidence that the receptor for atrial natriuretic peptide (guanylyl cyclase-A) inhibits cardiac ventricular myocyte hypertrophy. Proc Natl Acad Sci U S A 98:2703–2706. doi:10.1073/pnas.051625598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klaiber M, Dankworth B, Kruse M, Hartmann M, Nikolaev VO, Yang RB, Volker K, Gassner B, Oberwinkler H, Feil R, Freichel M, Groschner K, Skryabin BV, Frantz S, Birnbaumer L, Pongs O, Kuhn M (2011) A cardiac pathway of cyclic GMP-independent signaling of guanylyl cyclase A, the receptor for atrial natriuretic peptide. Proc Natl Acad Sci U S A 108:18500–18505. doi:1103300108 [pii]; 10.1073/pnas.1103300108 [doi]

    Google Scholar 

  • Klaiber M, Kruse M, Volker K, Schroter J, Feil R, Freichel M, Gerling A, Feil S, Dietrich A, Londono JE, Baba HA, Abramowitz J, Birnbaumer L, Penninger JM, Pongs O, Kuhn M (2010) Novel insights into the mechanisms mediating the local antihypertrophic effects of cardiac atrial natriuretic peptide: role of cGMP-dependent protein kinase and RGS2. Basic Res Cardiol 105:583–595. doi:10.1007/s00395-010-0098-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koller KJ, Lowe DG, Bennett GL, Minamino N, Kangawa K, Matsuo H, Goeddel DV (1991) Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science 252:120–123

    CAS  PubMed  Google Scholar 

  • Kuhn M (2003) Structure, regulation, and function of mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclase-A. Circ Res 93:700–709. doi:10.1161/01.RES.0000094745.28948.4D [doi];93/8/700 [pii]

    Google Scholar 

  • Lainchbury JG, Burnett JC Jr, Meyer D, Redfield MM (2000) Effects of natriuretic peptides on load and myocardial function in normal and heart failure dogs. Am J Physiol Heart Circ Physiol 278:H33–H40

    CAS  PubMed  Google Scholar 

  • Laskowski A, Woodman OL, Cao AH, Drummond GR, Marshall T, Kaye DM, Ritchie RH (2006) Antioxidant actions contribute to the antihypertrophic effects of atrial natriuretic peptide in neonatal rat cardiomyocytes. Cardiovasc Res 72:112–123. doi:10.1016/j.cardiores.2006.07.006

    Article  CAS  PubMed  Google Scholar 

  • Lee CY, Chen HH, Lisy O, Swan S, Cannon C, Lieu HD, Burnett JC Jr. (2009) Pharmacodynamics of a novel designer natriuretic peptide, CD-NP, in a first-in-human clinical trial in healthy subjects. J Clin Pharmacol 49:668–673. doi:0091270009336233 [pii]; 10.1177/0091270009336233 [doi]

    Google Scholar 

  • Lee DI, Zhu G, Sasaki T, Cho GS, Hamdani N, Holewinski R, Jo SH, Danner T, Zhang M, Rainer PP, Bedja D, Kirk JA, Ranek MJ, Dostmann WR, Kwon C, Margulies KB, Van Eyk JE, Paulus WJ, Takimoto E, Kass DA (2015) Phosphodiesterase 9A controls nitric-oxide-independent cGMP and hypertrophic heart disease. Nature 519:472–476. doi:10.1038/nature14332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lefkimmiatis K, Leronni D, Hofer AM (2013) The inner and outer compartments of mitochondria are sites of distinct cAMP/PKA signaling dynamics. J Cell Biol 202:453–462. doi:10.1083/jcb.201303159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leitman DC, Andresen JW, Kuno T, Kamisaki Y, Chang JK, Murad F (1986) Identification of multiple binding sites for atrial natriuretic factor by affinity cross-linking in cultured endothelial cells. J Biol Chem 261:11650–11655

    CAS  PubMed  Google Scholar 

  • Lin X, Hanze J, Heese F, Sodmann R, Lang RE (1995) Gene expression of natriuretic peptide receptors in myocardial cells. Circ Res 77:750–758

    CAS  PubMed  Google Scholar 

  • Marcus LS, Hart D, Packer M, Yushak M, Medina N, Danziger RS, Heitjan DF, Katz SD (1996) Hemodynamic and renal excretory effects of human brain natriuretic peptide infusion in patients with congestive heart failure. A double-blind, placebo-controlled, randomized crossover trial. Circulation 94:3184–3189

    CAS  PubMed  Google Scholar 

  • McMurray JJ, Packer M, Desai AS, Gong J, Lefkowitz MP, Rizkala AR, Rouleau JL, Shi VC, Solomon SD, Swedberg K, Zile MR, Investigators P-H, Committees (2014) Angiotensin-neprilysin inhibition versus enalapril in heart failure. N Engl J Med 371:993–1004. doi:10.1056/NEJMoa1409077

    PubMed  Google Scholar 

  • Meier S, Andressen KW, Aronsen JM, Sjaastad I, Skomedal T, Osnes J-B, Qvigstad E, Levy FO, Moltzau LR (2015) Enhancement of cAMP-mediated inotropic responses by CNP is regulated differently by PDE2 in normal and failing hearts. BMC Pharmacol Toxicol 16:A66. doi:10.1186/2050-6511-16-s1-a66

    Article  PubMed Central  Google Scholar 

  • Mery PF, Lohmann SM, Walter U, Fischmeister R (1991) Ca2+ current is regulated by cyclic GMP-dependent protein kinase in mammalian cardiac myocytes. Proc Natl Acad Sci U S A 88:1197–1201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mery PF, Pavoine C, Belhassen L, Pecker F, Fischmeister R (1993) Nitric oxide regulates cardiac Ca2+ current. Involvement of cGMP-inhibited and cGMP-stimulated phosphodiesterases through guanylyl cyclase activation. J Biol Chem 268:26286–26295

    CAS  PubMed  Google Scholar 

  • Mills RM, LeJemtel TH, Horton DP, Liang C, Lang R, Silver MA, Lui C, Chatterjee K (1999) Sustained hemodynamic effects of an infusion of nesiritide (human b-type natriuretic peptide) in heart failure: a randomized, double-blind, placebo-controlled clinical trial. Natrecor Study Group. J Am Coll Cardiol 34:155–162

    CAS  PubMed  Google Scholar 

  • Moalem J, Davidov T, Zhang Q, Grover GJ, Weiss HR, Scholz PM (2006) Negative inotropic effects of C-type natriuretic peptide are attenuated in hypertrophied ventricular myocytes associated with reduced cyclic GMP production. J Surg Res 135:38–44. doi:S0022-4804(06)00012-6 [pii]; 10.1016/j.jss.2006.01.012 [doi]

    Google Scholar 

  • Molenaar P, Christ T, Hussain RI, Engel A, Berk E, Gillette KT, Chen L, Galindo-Tovar A, Krobert KA, Ravens U, Levy FO, Kaumann AJ (2013) PDE3, but not PDE4, reduces β1-and β2-adrenoceptor-mediated inotropic and lusitropic effects in failing ventricle from metoprolol-treated patients. Br J Pharmacol 169:528–538. doi:10.1111/bph.12167

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moltzau LR, Aronsen JM, Meier S, Nguyen CH, Hougen K, Ørstavik O, Sjaastad I, Christensen G, Skomedal T, Osnes JB, Levy FO, Qvigstad E (2013) SERCA2 activity is involved in the CNP-mediated functional responses in failing rat myocardium. Br J Pharmacol 170:366–379. doi:10.1111/bph.12282 [doi]

    Google Scholar 

  • Moltzau LR, Aronsen JM, Meier S, Skogestad J, Ørstavik O, Lothe GB, Sjaastad I, Skomedal T, Osnes JB, Levy FO, Qvigstad E (2014a) Different compartmentation of responses to brain natriuretic peptide and C-type natriuretic peptide in failing rat ventricle. J Pharmacol Exp Ther 350:681–690. doi:jpet.114.214882 [pii]; 10.1124/jpet.114.214882 [doi]

    Google Scholar 

  • Moltzau LR, Meier S, Aronsen JM, Afzal F, Sjaastad I, Skomedal T, Osnes JB, Levy FO, Qvigstad E (2014b) Differential regulation of C-type natriuretic peptide-induced cGMP and functional responses by PDE2 and PDE3 in failing myocardium. Naunyn Schmiedebergs Arch Pharmacol. doi:10.1007/s00210-013-0953-1 [doi]

    Google Scholar 

  • Mongillo M, Tocchetti CG, Terrin A, Lissandron V, Cheung YF, Dostmann WR, Pozzan T, Kass DA, Paolocci N, Houslay MD, Zaccolo M (2006) Compartmentalized phosphodiesterase-2 activity blunts beta-adrenergic cardiac inotropy via an NO/cGMP-dependent pathway. Circ Res 98:226–234. doi:01.RES.0000200178.34179.93 [pii]; 10.1161/01.RES.0000200178.34179.93 [doi]

    Google Scholar 

  • Murthy KS, Teng BQ, Zhou H, Jin JG, Grider JR, Makhlouf GM (2000) Gi-1/Gi-2-dependent signaling by single-transmembrane natriuretic peptide clearance receptor. Am J Physiol Gastrointest Liver Physiol 278:G974–G980

    CAS  PubMed  Google Scholar 

  • Nagendran J, Archer SL, Soliman D, Gurtu V, Moudgil R, Haromy A, St AC, Webster L, Rebeyka IM, Ross DB, Light PE, Dyck JR, Michelakis ED (2007) Phosphodiesterase type 5 is highly expressed in the hypertrophied human right ventricle, and acute inhibition of phosphodiesterase type 5 improves contractility. Circulation 116:238–248. doi:CIRCULATIONAHA.106.655266 [pii]; 10.1161/CIRCULATIONAHA.106.655266 [doi]

    Google Scholar 

  • Niino Y, Hotta K, Oka K (2009) Simultaneous live cell imaging using dual FRET sensors with a single excitation light. PLoS One 4:e6036. doi:10.1371/journal.pone.0006036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nikolaev VO, Gambaryan S, Lohse MJ (2006) Fluorescent sensors for rapid monitoring of intracellular cGMP. Nat Methods 3:23–25. doi:10.1038/nmeth816

    Article  CAS  PubMed  Google Scholar 

  • Nir A, Zhang DF, Fixler R, Burnett JC Jr, Eilam Y, Hasin Y (2001) C-type natriuretic peptide has a negative inotropic effect on cardiac myocytes. Eur J Pharmacol 412:195–201

    CAS  PubMed  Google Scholar 

  • Nishikimi T, Kuwahara K, Nakao K (2011) Current biochemistry, molecular biology, and clinical relevance of natriuretic peptides. J Cardiol 57:131–140. doi:S0914-5087(11)00003-7 [pii]; 10.1016/j.jjcc.2011.01.002 [doi]

    Google Scholar 

  • Nishikimi T, Maeda N, Matsuoka H (2006) The role of natriuretic peptides in cardioprotection. Cardiovasc Res 69:318–328. doi:10.1016/j.cardiores.2005.10.001

    Article  CAS  PubMed  Google Scholar 

  • O'Connor CM, Starling RC, Hernandez AF, Armstrong PW, Dickstein K, Hasselblad V, Heizer GM, Komajda M, Massie BM, McMurray JJ, Nieminen MS, Reist CJ, Rouleau JL, Swedberg K, Adams KF Jr, Anker SD, Atar D, Battler A, Botero R, Bohidar NR, Butler J, Clausell N, Corbalan R, Costanzo MR, Dahlstrom U, Deckelbaum LI, Diaz R, Dunlap ME, Ezekowitz JA, Feldman D, Felker GM, Fonarow GC, Gennevois D, Gottlieb SS, Hill JA, Hollander JE, Howlett JG, Hudson MP, Kociol RD, Krum H, Laucevicius A, Levy WC, Mendez GF, Metra M, Mittal S, Oh BH, Pereira NL, Ponikowski P, Tang WH, Tanomsup S, Teerlink JR, Triposkiadis F, Troughton RW, Voors AA, Whellan DJ, Zannad F, Califf RM (2011) Effect of nesiritide in patients with acute decompensated heart failure. N Engl J Med 365:32–43. doi:10.1056/NEJMoa1100171

    Article  CAS  PubMed  Google Scholar 

  • O'Tierney PF, Chattergoon NN, Louey S, Giraud GD, Thornburg KL (2010) Atrial natriuretic peptide inhibits angiotensin II-stimulated proliferation in fetal cardiomyocytes. J Physiol 588:2879–2889. doi:10.1113/jphysiol.2010.191098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohte N, Cheng CP, Suzuki M, Little WC (1999) Effects of atrial natriuretic peptide on left ventricular performance in conscious dogs before and after pacing-induced heart failure. J Pharmacol Exp Ther 291:589–595

    CAS  PubMed  Google Scholar 

  • Omori K, Kotera J (2007) Overview of PDEs and their regulation. Circ Res 100:309–327. doi:100/3/309 [pii]; 10.1161/01.RES.0000256354.95791.f1 [doi]

    Google Scholar 

  • Ono K, Trautwein W (1991) Potentiation by cyclic GMP of beta-adrenergic effect on Ca2+ current in guinea-pig ventricular cells. J Physiol 443:387–404

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perera RK, Sprenger JU, Steinbrecher JH, Hubscher D, Lehnart SE, Abesser M, Schuh K, El-Armouche A, Nikolaev VO (2015) Microdomain switch of cGMP-regulated phosphodiesterases leads to ANP-induced augmentation of beta-adrenoceptor-stimulated contractility in early cardiac hypertrophy. Circ Res 116:1304–1311. doi:10.1161/circresaha.116.306082

    Article  CAS  PubMed  Google Scholar 

  • Pierkes M, Gambaryan S, Boknik P, Lohmann SM, Schmitz W, Potthast R, Holtwick R, Kuhn M (2002) Increased effects of C-type natriuretic peptide on cardiac ventricular contractility and relaxation in guanylyl cyclase A-deficient mice. Cardiovasc Res 53:852–861

    CAS  PubMed  Google Scholar 

  • Potter LR (2011) Guanylyl cyclase structure, function and regulation. Cell Signal 23:1921–1926. doi:S0898-6568(11)00280-4 [pii]; 10.1016/j.cellsig.2011.09.001 [doi]

    Google Scholar 

  • Potter LR, Abbey-Hosch S, Dickey DM (2006) Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev 27:47–72. doi:er.2005-0014 [pii]; 10.1210/er.2005-0014 [doi]

    Google Scholar 

  • Potter LR, Yoder AR, Flora DR, Antos LK, Dickey DM (2009) Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handb Exp Pharmacol 191:341–366. doi:10.1007/978-3-540-68964-5_15 [doi]

    Google Scholar 

  • Qvigstad E, Moltzau LR, Aronsen JM, Nguyen CH, Hougen K, Sjaastad I, Levy FO, Skomedal T, Osnes JB (2010) Natriuretic peptides increase beta1-adrenoceptor signalling in failing hearts through phosphodiesterase 3 inhibition. Cardiovasc Res 85:763–772. doi:cvp364 [pii]; 10.1093/cvr/cvp364 [doi]

    Google Scholar 

  • Resink TJ, Panchenko MP, Tkachuk VA, Buhler FR (1988) Involvement of Ni protein in the functional coupling of the atrial natriuretic factor (ANF) receptor to adenylate cyclase in rat lung plasma membranes. Eur J Biochem 174:531–535

    CAS  PubMed  Google Scholar 

  • Rose RA, Giles WR (2008) Natriuretic peptide C receptor signalling in the heart and vasculature. J Physiol 586:353–366. doi:jphysiol.2007.144253 [pii]; 10.1113/jphysiol.2007.144253 [doi]

    Google Scholar 

  • Rose RA, Lomax AE, Giles WR (2003) Inhibition of L-type Ca2+ current by C-type natriuretic peptide in bullfrog atrial myocytes: an NPR-C-mediated effect. Am J Physiol Heart Circ Physiol 285:H2454–H2462. doi:10.1152/ajpheart.00388.2003 [doi];00388.2003 [pii]

    Google Scholar 

  • Rosenkranz AC, Woods RL, Dusting GJ, Ritchie RH (2003) Antihypertrophic actions of the natriuretic peptides in adult rat cardiomyocytes: importance of cyclic GMP. Cardiovasc Res 57:515–522

    CAS  PubMed  Google Scholar 

  • Russwurm M, Mullershausen F, Friebe A, Jager R, Russwurm C, Koesling D (2007) Design of fluorescence resonance energy transfer (FRET)-based cGMP indicators: a systematic approach. Biochem J 407:69–77. doi:10.1042/bj20070348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh G, Kuc RE, Maguire JJ, Fidock M, Davenport AP (2006) Novel snake venom ligand dendroaspis natriuretic peptide is selective for natriuretic peptide receptor-A in human heart: downregulation of natriuretic peptide receptor-A in heart failure. Circ Res 99:183–190. doi:10.1161/01.RES.0000232322.06633.d3

    Article  CAS  PubMed  Google Scholar 

  • Sodi R, Dubuis E, Shenkin A, Hart G (2008) B-type natriuretic peptide (BNP) attenuates the L-type calcium current and regulates ventricular myocyte function. Regul Pept 151:95–105. doi:S0167-0115(08)00113-4 [pii]; 10.1016/j.regpep.2008.06.006 [doi]

    Google Scholar 

  • Spitzer KW, Bridge JH (1992) Relationship between intracellular pH and tension development in resting ventricular muscle and myocytes. Am J Phys 262:C316–C327

    CAS  Google Scholar 

  • Sprenger JU, Perera RK, Steinbrecher JH, Lehnart SE, Maier LS, Hasenfuss G, Nikolaev VO (2015) In vivo model with targeted cAMP biosensor reveals changes in receptor-microdomain communication in cardiac disease. Nat Commun 6:6965. doi:10.1038/ncomms7965

    Article  CAS  PubMed  Google Scholar 

  • Stangherlin A, Gesellchen F, Zoccarato A, Terrin A, Fields LA, Berrera M, Surdo NC, Craig MA, Smith G, Hamilton G, Zaccolo M (2011) cGMP signals modulate cAMP levels in a compartment-specific manner to regulate catecholamine-dependent signaling in cardiac myocytes. Circ Res 108:929–939. doi:CIRCRESAHA.110.230698 [pii]; 10.1161/CIRCRESAHA.110.230698 [doi]

    Google Scholar 

  • Su J, Scholz PM, Weiss HR (2005a) Differential effects of cGMP produced by soluble and particulate guanylyl cyclase on mouse ventricular myocytes. Exp Biol Med (Maywood) 230:242–250. doi:230/4/242 [pii]

    Google Scholar 

  • Su J, Zhang Q, Moalem J, Tse J, Scholz PM, Weiss HR (2005b) Functional effects of C-type natriuretic peptide and nitric oxide are attenuated in hypertrophic myocytes from pressure-overloaded mouse hearts. Am J Physiol Heart Circ Physiol 288:H1367–H1373. doi:00880.2004 [pii]; 10.1152/ajpheart.00880.2004 [doi]

    Google Scholar 

  • Sudoh T, Kangawa K, Minamino N, Matsuo H (1988) A new natriuretic peptide in porcine brain. Nature 332:78–81. doi:10.1038/332078a0 [doi]

    Google Scholar 

  • Sudoh T, Minamino N, Kangawa K, Matsuo H (1990) C-type natriuretic peptide (CNP): a new member of natriuretic peptide family identified in porcine brain. Biochem Biophys Res Commun 168:863–870

    CAS  PubMed  Google Scholar 

  • Suga S, Nakao K, Hosoda K, Mukoyama M, Ogawa Y, Shirakami G, Arai H, Saito Y, Kambayashi Y, Inouye K (1992a) Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-type natriuretic peptide. Endocrinology 130:229–239

    CAS  PubMed  Google Scholar 

  • Suga S, Nakao K, Itoh H, Komatsu Y, Ogawa Y, Hama N, Imura H (1992b) Endothelial production of C-type natriuretic peptide and its marked augmentation by transforming growth factor-beta. Possible existence of “vascular natriuretic peptide system”. J Clin Invest 90:1145–1149. doi:10.1172/JCI115933 [doi]

    Google Scholar 

  • Sumii K, Sperelakis N (1995) cGMP-dependent protein kinase regulation of the L-type Ca2+ current in rat ventricular myocytes. Circ Res 77:803–812

    CAS  PubMed  Google Scholar 

  • Tajima M, Bartunek J, Weinberg EO, Ito N, Lorell BH (1998) Atrial natriuretic peptide has different effects on contractility and intracellular pH in normal and hypertrophied myocytes from pressure-overloaded hearts. Circulation 98:2760–2764

    CAS  PubMed  Google Scholar 

  • Takahashi T, Allen PD, Izumo S (1992) Expression of A-, B-, and C-type natriuretic peptide genes in failing and developing human ventricles. Correlation with expression of the Ca2+-ATPase gene. Circ Res 71:9–17

    CAS  PubMed  Google Scholar 

  • Takayanagi R, Snajdar RM, Imada T, Tamura M, Pandey KN, Misono KS, Inagami T (1987) Purification and characterization of two types of atrial natriuretic factor receptors from bovine adrenal cortex: guanylate cyclase-linked and cyclase-free receptors. Biochem Biophys Res Commun 144:244–250. doi:S0006-291X(87)80502-8 [pii]

    Google Scholar 

  • Takimoto E, Belardi D, Tocchetti CG, Vahebi S, Cormaci G, Ketner EA, Moens AL, Champion HC, Kass DA (2007) Compartmentalization of cardiac beta-adrenergic inotropy modulation by phosphodiesterase type 5. Circulation 115:2159–2167. doi:CIRCULATIONAHA.106.643536 [pii]; 10.1161/CIRCULATIONAHA.106.643536 [doi]

    Google Scholar 

  • Takimoto E, Champion HC, Belardi D, Moslehi J, Mongillo M, Mergia E, Montrose DC, Isoda T, Aufiero K, Zaccolo M, Dostmann WR, Smith CJ, Kass DA (2005) cGMP catabolism by phosphodiesterase 5A regulates cardiac adrenergic stimulation by NOS3-dependent mechanism. Circ Res 96:100–109. doi:01.RES.0000152262.22968.72 [pii]; 10.1161/01.RES.0000152262.22968.72 [doi]

    Google Scholar 

  • Tan T, Scholz PM, Weiss HR (2010) Hypoxia inducible factor-1 improves the negative functional effects of natriuretic peptide and nitric oxide signaling in hypertrophic cardiac myocytes. Life Sci 87:9–16. doi:S0024-3205(10)00199-2 [pii]; 10.1016/j.lfs.2010.05.002 [doi]

    Google Scholar 

  • Tohse N, Nakaya H, Takeda Y, Kanno M (1995) Cyclic GMP-mediated inhibition of L-type Ca2+ channel activity by human natriuretic peptide in rabbit heart cells. Br J Pharmacol 114:1076–1082

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tokudome T, Horio T, Soeki T, Mori K, Kishimoto I, Suga S, Yoshihara F, Kawano Y, Kohno M, Kangawa K (2004) Inhibitory effect of C-type natriuretic peptide (CNP) on cultured cardiac myocyte hypertrophy: interference between CNP and endothelin-1 signaling pathways. Endocrinology 145:2131–2140. doi:10.1210/en.2003-1260

    Article  CAS  PubMed  Google Scholar 

  • Tokudome T, Kishimoto I, Horio T, Arai Y, Schwenke DO, Hino J, Okano I, Kawano Y, Kohno M, Miyazato M, Nakao K, Kangawa K (2008) Regulator of G-protein signaling subtype 4 mediates antihypertrophic effect of locally secreted natriuretic peptides in the heart. Circulation 117:2329–2339. doi:10.1161/circulationaha.107.732990

    Article  CAS  PubMed  Google Scholar 

  • Vandecasteele G, Verde I, Rucker-Martin C, Donzeau-Gouge P, Fischmeister R (2001) Cyclic GMP regulation of the L-type Ca2+ channel current in human atrial myocytes. J Physiol 533:329–340

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vaxelaire JF, Laurent S, Lacolley P, Briand V, Schmitt H, Michel JB (1989) Atrial natriuretic peptide decreases contractility of cultured chick ventricular cells. Life Sci 45:41–48

    CAS  PubMed  Google Scholar 

  • Wakabayashi S, Hisamitsu T, Nakamura TY (2013) Regulation of the cardiac Na+/H+ exchanger in health and disease. J Mol Cell Cardiol 61:68–76. doi:10.1016/j.yjmcc.2013.02.007

    CAS  PubMed  Google Scholar 

  • Wen JF, Cui X, Jin JY, Kim SM, Kim SZ, Kim SH, Lee HS, Cho KW (2004) High and low gain switches for regulation of cAMP efflux concentration: distinct roles for particulate GC- and soluble GC-cGMP-PDE3 signaling in rabbit atria. Circ Res 94:936–943. doi:10.1161/01.RES.0000123826.70125.4D [doi];01.RES.0000123826.70125.4D [pii]

    Google Scholar 

  • Weninger S, De Maeyer JH, Lefebvre RA (2012) Study of the regulation of the inotropic response to 5-HT4 receptor activation via phosphodiesterases and its cross-talk with C-type natriuretic peptide in porcine left atrium. Naunyn Schmiedeberg Arch Pharmacol 385:565–577. doi:10.1007/s00210-012-0746-y

    CAS  PubMed  Google Scholar 

  • William M, Hamilton EJ, Garcia A, Bundgaard H, Chia KK, Figtree GA, Rasmussen HH (2008) Natriuretic peptides stimulate the cardiac sodium pump via NPR-C-coupled NOS activation. Am J Physiol Cell Physiol 294:C1067–C1073. doi:00243.2007 [pii]; 10.1152/ajpcell.00243.2007 [doi]

    Google Scholar 

  • Wollert KC, Yurukova S, Kilic A, Begrow F, Fiedler B, Gambaryan S, Walter U, Lohmann SM, Kuhn M (2003) Increased effects of C-type natriuretic peptide on contractility and calcium regulation in murine hearts overexpressing cyclic GMP-dependent protein kinase I. Br J Pharmacol 140:1227–1236. doi:10.1038/sj.bjp.0705567 [doi];sj.bjp.0705567 [pii]

    Google Scholar 

  • Yasue H, Yoshimura M, Sumida H, Kikuta K, Kugiyama K, Jougasaki M, Ogawa H, Okumura K, Mukoyama M, Nakao K (1994) Localization and mechanism of secretion of B-type natriuretic peptide in comparison with those of A-type natriuretic peptide in normal subjects and patients with heart failure. Circulation 90:195–203

    CAS  PubMed  Google Scholar 

  • Zhang Q, Moalem J, Tse J, Scholz PM, Weiss HR (2005) Effects of natriuretic peptides on ventricular myocyte contraction and role of cyclic GMP signaling. Eur J Pharmacol 510:209–215. doi:S0014-2999(05)00061-0 [pii]; 10.1016/j.ejphar.2005.01.031 [doi]

    Google Scholar 

  • Zhang Q, Scholz PM, Pilzak A, Su J, Weiss HR (2007) Role of phospholamban in cyclic GMP mediated signaling in cardiac myocytes. Cell Physiol Biochem 20:157–166. doi:000104163 [pii]; 10.1159/000104163 [doi]

    Google Scholar 

  • Zhang M, Takimoto E, Lee DI, Santos CX, Nakamura T, Hsu S, Jiang A, Nagayama T, Bedja D, Yuan Y, Eaton P, Shah AM, Kass DA (2012) Pathological cardiac hypertrophy alters intracellular targeting of phosphodiesterase type 5 from nitric oxide synthase-3 to natriuretic peptide signaling. Circulation 126:942–951. doi:10.1161/circulationaha.112.090977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Pharmacology, Faculty of Medicine, University of Oslo and Oslo University Hospital, Oslo, Norway

    Lise Román Moltzau, Silja Meier, Kjetil Wessel Andressen & Finn Olav Levy

  2. Center for Heart Failure Research, Faculty of Medicine, University of Oslo and Oslo University Hospital, Oslo, Norway

    Lise Román Moltzau, Silja Meier, Kjetil Wessel Andressen & Finn Olav Levy

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  1. Lise Román Moltzau
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  2. Silja Meier
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  3. Kjetil Wessel Andressen
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  4. Finn Olav Levy
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  1. Institute of Experimental Cardiovascular Research, University Medical Center, Hamburg-Eppendorf, Germany

    Viacheslav Nikolaev

  2. Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, UK

    Manuela Zaccolo

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Moltzau, L.R., Meier, S., Andressen, K.W., Levy, F.O. (2017). Compartmentation of Natriuretic Peptide Signalling in Cardiac Myocytes: Effects on Cardiac Contractility and Hypertrophy. In: Nikolaev, V., Zaccolo, M. (eds) Microdomains in the Cardiovascular System. Cardiac and Vascular Biology, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-319-54579-0_12

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