Atrial natriuretic peptide locally counteracts the deleterious effects of cardiomyocyte mineralocorticoid receptor activation

Circulation: Heart Failure

Volumn 7, Issue 5, 2014, Pages 814-821

  Nakagawa, Hitoshi ^a,b   Oberwinkler, Heike ^a   Nikolaev, Viacheslav O ^c   Gaßner, Birgit ^a   Umbenhauer, Sandra ^d   Wagner, Helga ^d   Saito, Yoshihiko ^e   Baba, Hideo A ^e   Frantz, Stefan ^b,d   Kuhn, Michaela ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^d NARA MEDICAL UNIVERSITY   (Japan)

^e UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

Aldosterone; Angiotensins; Atrial natriuretic factor; Heart failure

Indexed keywords

ALDOSTERONE; ATRIAL NATRIURETIC FACTOR; CYCLIC GMP DEPENDENT PROTEIN KINASE 1; EPLERENONE; MINERALOCORTICOID RECEPTOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; ATP2A3 PROTEIN, MOUSE; CONNECTIVE TISSUE GROWTH FACTOR; DNA; MINERALOCORTICOID ANTAGONIST; SPIRONOLACTONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOMYOPATHY; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRESSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONGESTIVE CARDIOMYOPATHY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ATRIAL NATRIURETIC FACTOR; BLOTTING, WESTERN; CARDIOMYOPATHY, DILATED; CONNECTIVE TISSUE GROWTH FACTOR; DISEASE MODELS, ANIMAL; DNA; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MINERALOCORTICOID RECEPTOR ANTAGONISTS; MYOCYTES, CARDIAC; RECEPTORS, MINERALOCORTICOID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SIGNAL TRANSDUCTION; SPIRONOLACTONE; VENTRICULAR REMODELING;

EID: 84924420892     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.113.000885     Document Type: Article

References (36)

1. Ohtani T, Ohta M, Yamamoto K, Mano T, Sakata Y, Nishio M, Takeda Y, Yoshida J, Miwa T, Okamoto M, Masuyama T, Nonaka Y, Hori M. Elevated cardiac tißue level of aldosterone and mineralocorticoid receptor in diastolic heart failure: Beneficial effects of mineralocorticoid receptor blocker. Am J Physiol Regul Integr Comp Physiol. 2007;292:R946-R954.
2. Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A, Palensky J, Wittes J. The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N Engl J Med. 1999;341:709-717.
3. Lother A, Berger S, Gilsbach R, Rösner S, Ecke A, Barreto F, Bauersachs J, Schütz G, Hein L. Ablation of mineralocorticoid receptors in myocytes but not in fibroblasts preserves cardiac function. Hypertension. 2011;57:746-754.
4. Fraccarollo D, Berger S, Galuppo P, Kneitz S, Hein L, Schütz G, Frantz S, Ertl G, Bauersachs J. Deletion of cardiomyocyte mineralocorticoid receptor ameliorates adverse remodeling after myocardial infarction. Circulation. 2011;123:400-408.
5. Ouvrard-Pascaud A, Sainte-Marie Y, Bénitah JP, Perrier R, Soukaseum C, Nguyen Dinh Cat A, Royer A, Le Quang K, Charpentier F, Demolombe S, Mechta-Grigoriou F, Beggah AT, Maison-Blanche P, Oblin ME, Delcayre C, Fishman GI, Farman N, Escoubet B, Jaißer F. Conditional mineralocorticoid receptor expreßion in the heart leads to life-threatening arrhythmias. Circulation. 2005;111:3025-3033.
6. Di Zhang A, Nguyen Dinh Cat A, Soukaseum C, Escoubet B, Cherfa A, Meßaoudi S, Delcayre C, Samuel JL, Jaißer F. Croß-talk between mineralocorticoid and angiotensin II signaling for cardiac remodeling. Hypertension. 2008;52:1060-1067.
7. 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.
8. Kishimoto I, Roßi K, Garbers DL. 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. 2001;98:2703-2706.
9. 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.
10. Blanton RM, Takimoto E, Lane AM, Aronovitz M, Piotrowski R, Karas RH, Kaß DA, Mendelsohn ME. Protein kinase g iα inhibits preßure overload-induced cardiac remodeling and is required for the cardioprotective effect of sildenafil in vivo. J Am Heart Aßoc. 2012;1:e003731.
11. Frantz S, Klaiber M, Baba HA, Oberwinkler H, Völker K, Gaßner B, Bayer B, Abeßer M, Schuh K, Feil R, Hofmann F, Kuhn M. Streßdependent dilated cardiomyopathy in mice with cardiomyocyte-restricted inactivation of cyclic GMP-dependent protein kinase I. Eur Heart J. 2013;34:1233-1244.
12. Chen HH, Martin FL, Gibbons RJ, Schirger JA, Wright RS, Schears RM, Redfield MM, Simari RD, Lerman A, Cataliotti A, Burnett JC Jr. Low-dose nesiritide in human anterior myocardial infarction suppreßes aldosterone and preserves ventricular function and structure: a proof of concept study. Heart. 2009;95:1315-1319.
13. von Lueder TG, Sangaralingham SJ, Wang BH, Kompa AR, Atar D, Burnett JC Jr, Krum H. Renin-angiotensin blockade combined with natriuretic peptide system augmentation: novel therapeutic concepts to combat heart failure. Circ Heart Fail. 2013;6:594-605.
14. Kuhn M, Voß M, Mitko D, Stypmann J, Schmid C, Kawaguchi N, Grabellus F, Baba HA. Left ventricular aßist device support reverses altered cardiac expreßion and function of natriuretic peptides and receptors in end-stage heart failure. Cardiovasc Res. 2004;64:308-314.
15. Klaiber M, Dankworth B, Kruse M, Hartmann M, Nikolaev VO, Yang RB, Völker K, Gaßner B, Oberwinkler H, Feil R, Freichel M, Groschner K, Skryabin BV, Frantz S, Birnbaumer L, Pongs O, Kuhn M. 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. 2011;108:18500-18505.
16. Dickey DM, Dries DL, Margulies KB, Potter LR. 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. 2012;52:727-732.
17. Wohlschlaeger J, Levkau B, Brockhoff G, Schmitz KJ, von Winterfeld M, Takeda A, Takeda N, Stypmann J, Vahlhaus C, Schmid C, Pomjanski N, Böcking A, Baba HA. Hemodynamic support by left ventricular aßist devices reduces cardiomyocyte DNA content in the failing human heart. Circulation. 2010;121:989-996.
18. Schröter J, Zahedi RP, Hartmann M, Gaßner B, Gazinski A, Waschke J, Sickmann A, Kuhn M. Homologous desensitization of guanylyl cyclase A, the receptor for atrial natriuretic peptide, is aßociated with a complex phosphorylation pattern. FEBS J. 2010;277:2440-2453.
19. Arriza JL, Weinberger C, Cerelli G, Glaser TM, Handelin BL, Housman DE, Evans RM. Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science. 1987;237:268-275.
20. Funder JW, Pearce PT, Smith R, Smith AI. Mineralocorticoid action: target tißue specificity is enzyme, not receptor, mediated. Science. 1988;242:583-585.
21. Lombès M, Alfaidy N, Eugene E, Leßana A, Farman N, Bonvalet JP. Prerequisite for cardiac aldosterone action. Mineralocorticoid receptor and 11 beta-hydroxysteroid dehydrogenase in the human heart. Circulation. 1995;92:175-182.
22. Meßaoudi S, Gravez B, Tarjus A, Pelloux V, Ouvrard-Pascaud A, Delcayre C, Samuel J, Launay JM, Sierra-Ramos C, Alvarez de la Rosa D, Clément K, Farman N, Jaißer F. Aldosterone-specific activation of cardiomyocyte mineralocorticoid receptor in vivo. Hypertension. 2013;61:361-367.
23. Kato H, Mizuno T, Mizuno M, Sawai A, Suzuki Y, Kinashi H, Nagura F, Maruyama S, Noda Y, Yamada K, Matsuo S, Ito Y. Atrial natriuretic peptide ameliorates peritoneal fibrosis in rat peritonitis model. Nephrol Dial Transplant. 2012;27:526-536.
24. Weber KT, Brilla CG, Janicki JS. Myocardial fibrosis: functional significance and regulatory factors. Cardiovasc Res. 1993;27:341-348.
25. Shao Q, Ren B, Saini HK, Netticadan T, Takeda N, Dhalla NS. Sarcoplasmic reticulum Ca2+ transport and gene expreßion in congestive heart failure are modified by imidapril treatment. Am J Physiol Heart Circ Physiol. 2005;288:H1674-H1682.
26. Großmann C, Huße B, Mildenberger S, Schreier B, Schuman K, Gekle M. Colocalization of mineralocorticoid and EGF receptor at the plasma membrane. Biochim Biophys Acta. 2010;1803:584-590.
27. Mohammed SF, Ohtani T, Korinek J, Lam CS, Larsen K, Simari RD, Valencik ML, Burnett JC Jr, Redfield MM. Mineralocorticoid accelerates transition to heart failure with preserved ejection fraction via 'nongenomic effects'. Circulation. 2010;122:370-378.
28. Schulman G, Lindemeyer R, Barman A, Karnik S, Bastl CP. Atrial natriuretic peptide inhibits mineralocorticoid receptor function in rat colonic surface cells. J Clin Invest. 1996;98:157-166.
29. Barsony J, McKoy W. Molybdate increases intracellular 3',5'-guanosine cyclic monophosphate and stabilizes vitamin D receptor aßociation with tubulin-containing filaments. J Biol Chem. 1992;267:24457-24465.
30. Kumar R, Grammatikakis N, Chinkers M. Regulation of the atrial natriuretic peptide receptor by heat shock protein 90 complexes. J Biol Chem. 2001;276:11371-11375.
31. Nishi M. Dynamics of corticosteroid receptors: leßons from live cell imaging. Acta Histochem Cytochem. 2011;44:1-7.
32. Krug AW, Pojoga LH, Williams GH, Adler GK. Cell membrane-aßociated mineralocorticoid receptors? New evidence. Hypertension. 2011;57: 1019-1025.
33. Chen W, Gaßner B, Börner S, Nikolaev VO, Schlegel N, Waschke J, Steinbronn N, Straßer R, Kuhn M. Atrial natriuretic peptide enhances microvascular albumin permeability by the caveolae-mediated transcellular pathway. Cardiovasc Res. 2012;93:141-151.
34. McKie PM, Rodeheffer RJ, Cataliotti A, Martin FL, Urban LH, Mahoney DW, Jacobsen SJ, Redfield MM, Burnett JC Jr. Amino-terminal pro-B-type natriuretic peptide and B-type natriuretic peptide: biomarkers for mortality in a large community-based cohort free of heart failure. Hypertension. 2006;47:874-880.
35. Mizuno Y, Yoshimura M, Yasue H, Sakamoto T, Ogawa H, Kugiyama K, Harada E, Nakayama M, Nakamura S, Ito T, Shimasaki Y, Saito Y, Nakao K. Aldosterone production is activated in failing ventricle in humans. Circulation. 2001;103:72-77.
36. Menon SG, Mills RM, Schellenberger U, Saqhir S, Protter AA. Clinical implications of defective B-type natriuretic peptide. Clin Cardiol. 2009;32:E36-E41.