Sustained hemodynamic stress disrupts normal circadian rhythms in calcineurin-dependent signaling and protein phosphorylation in the heart

Circulation Research

Volumn 108, Issue 4, 2011, Pages 437-445

  Sachan, Nita ^a   Dey, Asim ^a   Rotter, David ^a   Grinsfelder, D Bennett ^a   Battiprolu, Pavan K ^a   Sikder, Devanjan ^c   Copeland, Victoria ^d   Oh, Misook ^a   Bush, Erik ^e   Shelton, John M ^a   Bibb, James A ^b   Hill, Joseph A ^a,b   Rothermel, Beverly A ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c BURNHAM INSTITUTE   (United States)

^d GlycoFi   (United States)

^e Thermo Fisher Scientific   (United States)

Author keywords

calcineurin; circadian rhythms; heart failure; RCAN1 MCIP1

Indexed keywords

CALCINEURIN; PHOSPHOLAMBAN; PHOSPHOPROTEIN PHOSPHATASE 1; REGULATOR OF CALCINEURIN 1; REGULATOR PROTEIN; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ADRENERGIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CIRCADIAN RHYTHM; GENE DISRUPTION; GENE TARGETING; GENETIC TRANSCRIPTION; HEART HEMODYNAMICS; HEART LEFT VENTRICLE OVERLOAD; HEART MUSCLE; HEART VENTRICLE HYPERTROPHY; MALE; MOUSE; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CALCINEURIN; CALCIUM-BINDING PROTEINS; CIRCADIAN RHYTHM; DISEASE MODELS, ANIMAL; HEART FAILURE; HEART VENTRICLES; HEMODYNAMICS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MUSCLE PROTEINS; NFATC TRANSCRIPTION FACTORS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 1; PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 79952068771     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.235309     Document Type: Article

References (32)

1. Young ME. The circadian clock within the heart: potential influence on myocardial gene expression, metabolism, and function. Am J Physiol Heart Circ Physiol. 2006;290:H1-H16.
2. Mitler MM, Hajdukovic RM, Shafor R, Hahn PM, Kripke DF. When people die. Cause of death versus time of death. Am J Med. 1987;82: 266-274.
3. Ko CH, Takahashi JS. Molecular components of the mammalian circadian clock. Hum Mol Genet. 2006;15:R271-R277.
4. Honma S, Honma K. The biological clock: Ca2+ links the pendulum to the hands. Trends Neurosci. 2003;26:650-653.
5. Bers DM, Guo T. Calcium signaling in cardiac ventricular myocytes. Ann N Y Acad Sci. 2005;1047:86-98.
6. Wilkins BJ, Molkentin JD. Calcium-calcineurin signaling in the regulation of cardiac hypertrophy. Biochem Biophys Res Commun. 2004;322: 1178-1191.
7. Rothermel BA, Vega RB, Williams RS. The role of modulatory calcineurin-interacting proteins in calcineurin signaling. Trends Cardiovasc Med. 2003; 13:15-21.
8. Yang J, Rothermel B, Vega RB, Frey N, McKinsey TA, Olson EN, Bassel-Duby R, Williams RS. Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles. Circ Res. 2000;87:e61-e68.
9. El-Armouche A, Boknik P, Eschenhagen T, Carrier L, Knaut M, Ravens U, Dobrev D. Molecular determinants of altered Ca2+ handling in human chronic atrial fibrillation. Circulation. 2006;114:670-680.
10. El-Armouche A, Rau T, Zolk O, Ditz D, Pamminger T, Zimmermann WH, Jackel E, Harding SE, Boknik P, Neumann J, Eschenhagen T. Evidence for protein phosphatase inhibitor-1 playing an amplifier role in beta-adrenergic signaling in cardiac myocytes. FASEB J. 2003;17: 437-439.
11. Mudd JO, Kass DA. Tackling heart failure in the twenty-first century. Nature. 2008;451:919-928.
12. Bibb JA, Nishi A, O'Callaghan JP, Ule J, Lan M, Snyder GL, Horiuchi A, Saito T, Hisanaga S, Czernik AJ, Nairn AC, Greengard P. Phosphorylation of protein phosphatase inhibitor-1 by Cdk5. J Biol Chem. 2001; 276:14490-14497.
13. Mulkey RM, Endo S, Shenolikar S, Malenka RC. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature. 1994;369:486-488.
14. El-Armouche A, Bednorz A, Pamminger T, Ditz D, Didie M, Dobrev D, Eschenhagen T. Role of calcineurin and protein phosphatase-2A in the regulation of phosphatase inhibitor-1 in cardiac myocytes. Biochem Biophys Res Commun. 2006;346:700-706.
15. MacDonnell SM, Kubo H, Harris DM, Chen X, Berretta R, Barbe MF, Kolwicz S, Reger PO, Eckhart A, Renna BF, Koch WJ, Houser SR, Libonati JR. Calcineurin inhibition normalizes beta-adrenergic responsiveness in the spontaneously hypertensive rat. Am J Physiol Heart Circ Physiol. 2007;293:H3122-H3129.
16. Rothermel BA, Berenji K, Tannous P, Kutschke W, Dey A, Nolan B, Yoo KD, Demetroulis E, Gimbel M, Cabuay B, Karimi M, Hill JA. Differential activation of stress-response signaling in load-induced cardiac hypertrophy and failure. Physiol Genomics. 2005;23:18-27.
17. Rothermel BA, McKinsey TA, Vega RB, Nicol RL, Mammen P, Yang J, Antos CL, Shelton JM, Bassel-Duby R, Olson EN, Williams RS. Myocyte-enriched calcineurin-interacting protein, MCIP1, inhibits cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A. 2001;98: 3328-3333.
18. Bray MS, Shaw CA, Moore MW, Garcia RA, Zanquetta MM, Durgan DJ, Jeong WJ, Tsai JY, Bugger H, Zhang D, Rohrwasser A, Rennison JH, Dyck JR, Litwin SE, Hardin PE, Chow CW, Chandler MP, Abel ED, Young ME. Disruption of the circadian clock within the cardiomyocyte influences myocardial contractile function, metabolism, and gene expression. Am J Physiol Heart Circ Physiol. 2008;294:H1036-H1047.
19. Young ME, Razeghi P, Cedars AM, Guthrie PH, Taegtmeyer H. Intrinsic diurnal variations in cardiac metabolism and contractile function. Circ Res. 2001;89:1199-1208.
20. Durgan DJ, Moore MW, Ha NP, Egbejimi O, Fields A, Mbawuike U, Egbejimi A, Shaw CA, Bray MS, Nannegari V, Hickson-Bick DL, Heird WC, Dyck JR, Chandler MP, Young ME. Circadian rhythms in myocardial metabolism and contractile function; influence of workload and oleate. Am J Physiol Heart Circ Physiol. 2007;293:H2385-H2393.
21. Antos CL, McKinsey TA, Frey N, Kutschke W, McAnally J, Shelton JM, Richardson JA, Hill JA, Olson EN. Activated glycogen synthase-3 beta suppresses cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A. 2002; 99:907-912.
22. Young ME, Razeghi P, Taegtmeyer H. Clock genes in the heart: characterization and attenuation with hypertrophy. Circ Res. 2001;88: 1142-1150.
23. Razeghi P, Young ME, Alcorn JL, Moravec CS, Frazier OH, Taegtmeyer H. Metabolic gene expression in fetal and failing human heart. Circulation. 2001;104:2923-2931.
24. Lemmer B. The importance of circadian rhythms on drug response in hypertension and coronary heart disease-from mice and man. Pharmacol Ther. 2006;111:629-651.
25. Collins HE, Rodrigo GC. Inotropic response of cardiac ventricular myocytes to beta-adrenergic stimulation with isoproterenol exhibits diurnal variation: involvement of nitric oxide. Circ Res. 2010;106:1244-1252.
26. Sanna B, Brandt EB, Kaiser RA, Pfluger P, Witt SA, Kimball TR, van Rooij E, De Windt LJ, Rothenberg ME, Tschop MH, Benoit SC, Molkentin JD. Modulatory calcineurin-interacting proteins 1 and 2 function as calcineurin facilitators in vivo. Proc Natl Acad Sci U S A. 2006;103:7327-7332.
27. Durgan DJ, Pulinilkunnil T, Villegas-Montoya C, Garvey ME, Frangogiannis NG, Michael LH, Chow CW, Dyck JR, Young ME. Short communication: ischemia/reperfusion tolerance is time-of-day-dependent: mediation by the cardiomyocyte circadian clock. Circ Res. 2010;106:546-550.
28. Witte K, Hu K, Swiatek J, Mussig C, Ertl G, Lemmer B. Experimental heart failure in rats: effects on cardiovascular circadian rhythms and on myocardial beta-adrenergic signaling. Cardiovasc Res. 2000;47: 350-358.
29. Gupta RC, Mishra S, Rastogi S, Imai M, Habib O, Sabbah HN. Cardiac SR-coupled PP1 activity and expression are increased and inhibitor 1 protein expression is decreased in failing hearts. Am J Physiol Heart Circ Physiol. 2003;285:H2373-H2381.
30. Sande JB, Sjaastad I, Hoen IB, Bokenes J, Tonnessen T, Holt E, Lunde PK, Christensen G. Reduced level of serine(16) phosphorylated phospholamban in the failing rat myocardium: a major contributor to reduced SERCA2 activity. Cardiovasc Res. 2002;53:382-391.
31. Martino TA, Sole MJ. Molecular time: an often overlooked dimension to cardiovascular disease. Circ Res. 2009;105:1047-1061.
32. Smolensky MH, Hermida RC, Ayala DE, Tiseo R, Portaluppi F. Administration-time-dependent effects of blood pressure-lowering medications: basis for the chronotherapy of hypertension. Blood Press Monit. 2010;15:173-180.