Fkbp12.6 mice display temporal gender differences in cardiac Ca2+-signalling phenotype upon chronic pressure overload

Canadian Journal of Physiology and Pharmacology

Volumn 89, Issue 11, 2011, Pages 769-782

  Prévilon, Miresta ^a   Pezet, Mylène ^b   Semprez, Fannie ^a   Mercadier, Jean Jacques ^a   Rouet Benzineb, Patricia ^a,b,c  

^a INSERM   (France)

^b BICHAT HOSPITAL   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Akt; Ca2+ calmodulin dependent kinase ii; Calcineurin; Calcium handling protein; Cardiac hypertrophy; Fkbp12.6; Glycogen synthase kinase 3 ; Heart failure; Pressure overload

Indexed keywords

BRAIN NATRIURETIC PEPTIDE; CALCINEURIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 12.6; MESSENGER RNA; MYOSIN HEAVY CHAIN BETA; RYANODINE RECEPTOR 2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; CALCIUM SIGNALING; CHANNEL GATING; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HEART FAILURE; HEART LEFT VENTRICLE FUNCTION; HEART LEFT VENTRICLE HYPERTROPHY; HEART LEFT VENTRICLE OVERLOAD; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; SURVIVAL RATE; SYSTOLIC DYSFUNCTION; THORACIC AORTA SURGERY;

ANIMALS; AORTA, THORACIC; CALCINEURIN; CALCIUM; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GENE EXPRESSION PROFILING; GLYCOGEN SYNTHASE KINASE 3; HEART; HEART FAILURE; HOMEODOMAIN PROTEINS; HUMANS; HYPERTROPHY, LEFT VENTRICULAR; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MICE; MICE, TRANSGENIC; NATRIURETIC PEPTIDE, BRAIN; PHENOTYPE; RANDOM ALLOCATION; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SEX FACTORS; SIGNAL TRANSDUCTION; TACROLIMUS BINDING PROTEINS; VENTRICULAR PRESSURE;

EID: 80055116401     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: None     Document Type: Article

References (62)

1. Anderson, M.E. 2009. CaMKII and a failing strategy for growth in heart. J. Clin. Invest. 119(5): 1082-1085. doi:10.1172/JCI39262.
2. Anderson, M.E., Brown, J.H., and Bers, D.M. 2011. CaMKII in myocardial hypertrophy and heart failure. J. Mol. Cell. Cardiol., In press. doi:10.1016/j.yjmcc.2011.01.012.
3. 2+-ATPase (SERCA2) gene promoter activity is decreased in response to severe left ventricular pressure-overload hypertrophy in rat hearts. J. Mol. Cell. Cardiol. 31(4): 919-926. doi:10.1006/jmcc.1998.0932.
4. Barik, S. 2006. Immunophilins: for the love of proteins. Cell. Mol. Life Sci. 63(24): 2889-2900. doi:10.1007/s00018-006-6215-3.
5. Barry, W.H., and Bridge, J.H. 1993. Intracellular calcium homeostasis in cardiac myocytes. Circulation, 87(6): 1806-1815.
6. Berenji, K., Drazner, M.H., Rothermel, B.A., and Hill, J.A. 2005. Does load-induced ventricular hypertrophy progress to systolic heart failure? Am. J. Physiol. Heart Circ. Physiol. 289(1): H8-H16. doi:10.1152/ajpheart.01303.2004.
7. Bers, D.M. 2006. Altered cardiac myocyte Ca regulation in heart failure. Physiology (Bethesda), 21: 380-387.
8. Bers, D.M. 2008. Calcium cycling and signalling in cardiac myocytes. Annu. Rev. Physiol. 70(1): 23-49. doi:10.1146/annurev.physiol.70.113006.100455.
9. 2+-calmodulin-dependent protein kinase II regulation of cardiac excitation-transcription coupling. Heart Rhythm, 8(7): 1101-1104. doi:10.1016/j.hrthm.2011.01.030.
10. Bueno, O.F., and Molkentin, J.D. 2002. Involvement of extracellular signal-regulated kinases 1/2 in cardiac hypertrophy and cell death. Circ. Res. 91(9): 776-781. doi:10.1161/01.RES.0000038488. 38975.1A.
11. 2+/calmodulin-dependent protein kinase II in vivo. Mol. Endocrinol. 17(2): 183-192. doi:10.1210/me.2002-0350.
12. Dorn, G.W., II, and Force, T. 2005. Protein kinase cascades in the regulation of cardiac hypertrophy. J. Clin. Invest. 115(3): 527-537.
13. Du, X.J. 2004. Gender modulates cardiac phenotype development in genetically modified mice. Cardiovasc. Res. 63(3): 510-519. doi:10.1016/j.cardiores.2004.03.027.
14. Fedak, P.W., Verma, S., Weisel, R.D., Skrtic, M., and Li, R.K. 2005. Cardiac remodeling and failure: from molecules to man (Part III). Cardiovasc. Pathol. 14(3): 109-119. doi:10.1016/j.carpath.2005. 03.004.
15. Fliegner, D., Schubert, C., Penkalla, A., Witt, H., Kararigas, G., Dworatzek, E., et al. 2010. Female sex and estrogen receptor-beta attenuate cardiac remodeling and apoptosis in pressure overload. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298(6): R1597-R1606. doi:10.1152/ajpregu.00825.2009.
16. Gellen, B., Fernández-Velasco, M., Briec, F., Vinet, L., LeQuang, K., Rouet-Benzineb, P., et al. 2008. Conditional FKBP12.6overexpression in mouse cardiac myocytes prevents triggered ventricular tachycardia through specific alterations in excitation- contraction coupling. Circulation, 117(14): 1778-1786. doi:10.1161/CIRCULATIONAHA.107.731893.
17. Guo, T., Cornea, R.L., Huke, S., Camors, E., Yang, Y., Picht, E., et al. 2010. Kinetics of FKBP12.6binding to ryanodine receptors in permeabilized cardiac myocytes and effects on Ca sparks. Circ. Res. 106(11): 1743-1752. doi:10.1161/CIRCRESAHA.110. 219816.
18. Hardt, S.E., and Sadoshima, J. 2002. Glycogen synthase kinase-3 beta: a novel regulator of cardiac hypertrophy and development. Circ. Res. 90(10): 1055-1063. doi:10.1161/01.RES.0000018952. 70505.F1.
19. 2+ exchanger protein levels and diastolic function of failing human myocardium. Circulation, 99(5): 641-648.
20. Heineke, J., and Molkentin, J.D. 2006. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat. Rev. Mol. Cell Biol. 7(8): 589-600. doi:10.1038/nrm1983.
21. Hu, P., Zhang, D., Swenson, L., Chakrabati, G., Abel, E.D., and Litwin, S.E.2003. Minimally invasive aortic banding in mice: effects of altered cardiomycyte insulin signaling duirn pressure overload. Am. J. Heart Cric. Physiol.285(3): H1261-H1269.
22. Huang, F., Shan, J., Reiken, S., Wehrens, X.H.T., and Marks, A.R. 2006. Analysis of calstabin 2 (FKBP12.6)-ryanodine receptor interactions: Rescue of heart failure by calstabin 2 in mice. Proc. Natl. Acad. Sci. U.S.A. 103(9): 3456-3461. doi:10.1073/pnas. 0511282103.
23. Hunter, S., and Robson, S.C. 1992. Adaptation of the maternal heart in pregnancy. Br. Heart J. 68(6): 540-543. doi:10.1136/hrt.68.12.540.
24. Kararigas, G., Fliegner, D., Gustafsson, J.A., and Regitz-Zagrosek, V. 2011. Role of the estrogen/estrogen-receptor-beta axis in the genomic response to pressure overload-induced hypertrophy. Physiol. Genomics, 43(8): 438-446. doi:10.1152/physiolgenomics.00199.2010.
25. Kehat, I., and Molkentin, J.D. 2010. Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation, 122(25): 2727-2735. doi:10.1161/CIRCULATIONAHA. 110.942268.
26. Kemi, O.J., Haram, P.M., Loennechen, J.P., Osnes, J.B., Skomedal, T., Wisloff, U., and Ellingsen, O. 2005. Moderate vs. high exercise intensity: differential effects on aerobic fitness, cardiomyocyte contractility, and endothelial function. Cardiovasc. Res. 67(1): 161-172. doi:10.1016/j.cardiores.2005.03.010.
27. Kiriazis, H., Sato, Y., Kadambi, V.J., Schmidt, A.G., Gerst, M.J., Hoit, B.D., and Kranias, E.G. 2002. Hypertrophy and functional alterations in hyperdynamic phospholamban-knockout mouse hearts under chronic aortic stenosis. Cardiovasc. Res. 53(2):372-381. doi:10.1016/S0008-6363(01)00487-4.
28. Kumar, R., Adams, B., Musiyenko, A., Shulyayeva, O., and Barik, S. 2005. The FK5O6-binding protein of the malaria parasite, Plasmodium falciparum, is a FK506-sensitive chaperone with FK506-indenpendant calcineurin-inhibitory activity. Mol. Biochem. Parasitol. 141(2): 163-173. doi:10.1016/j.molbiopara.2005. 02.007.
29. Lam, E., Martin, M.M., Timerman, A.P., Sabers, C., Fleischer, S., Lukas, T., et al. 1995. A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor. J. Biol. Chem. 270(44): 26511-26522. doi:10.1074/jbc.270.44.26511.
30. Leinwand, L.A. 2003. Sex is a potent modifier of the cardiovascular system. J. Clin. Invest. 112(3): 302-307.
31. Li, Y.H., Reddy, A.K., Taffet, G.E., Michael, L.H., Entman, M.L., and Hartley, C.J. 2003. Doppler evaluation of peripheral vascular adaptations to transverse aortic banding in mice. Ultrasound Med. Biol. 29(9): 1281-1289. doi:10.1016/S0301-5629(03)00986-4.
32. Liu, J.O. 2003. Endogenous protein inhibitors of calcineurin. Biochem. Biophys. Res. Commun. 311(4): 1103-1109. doi:10.1016/j.bbrc.2003.10.020.
33. Loberg, R.D., Vesely, E., and Brosius, F.C., III. 2002. Enhanced Glycogen synthase kinase-3 beta activity mediates hypoxiainduced apoptosis of vascular smooth muscle cells and is prevented by glucosee transport and metabolism. J. Biol. Chem. 277(44): 41667-41673. doi:10.1074/jbc.M206405200.
34. MacDonnell, S.M., Weisser-Thomas, J., Kubo, H., Hanscome, M., Liu, Q., Jaleel, N., et al. 2009. CaMKII negatively regulates calcineurin-NFAT signalling in cardiac myocyte. Circ. Res. 105 (4): 316-325. doi:10.1161/CIRCRESAHA.109.194035.
35. Maier, L.S., and Bers, D.M. 2002. Calcium, calmodulin, and calciumcalmodulin kinase II: heartbeat to heartbeat and beyond. J. Mol. Cell. Cardiol. 34(8): 919-939. doi:10.1006/jmcc.2002.2038.
36. Manabe, I., Shindo, T., and Nagai, R. 2002. Gene expression in fibroblasts and fibrosis involvement in cardiac hypertrophy. Circ. Res. 91(12): 1103-1113. doi:10.1161/01.RES.0000046452.67724.B8.
37. Marks, A.R., Marx, S.O., and Reiken, S. 2002. Regualtion of ryanodine receptors via macromolecular complexes: a role for leucine/isoleucine zippers. Trends Cardiovasc. Med.12(4): 166-170.
38. Michael, A., Hag, S., Chen, X., Hsich, E., Cui, L., Walters, B., Shao, Z., et al.2004. Glycogen synthase kinase-3b regulates growth, calcium homeostasis, and diastolic function in the heart. J. Biol. Chem.279(20): 21383-21393. doi:10.1074/jbc.M401413200.
39. Molkentin, J.D., Lu, J.F., Antos, C.L., Markham, B., Richardson, J., Robbins, J., et al. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell, 93(2): 215-228. doi:10.1016/S0092-8674(00)81573-1.
40. Moore, R.L., and Palmer, B.M. 1999. Exercise training and cellular adaptations of normal and diseased hearts. Exerc. Sport Sci. Rev. 27: 285-315. doi:10.1249/00003677-199900270-00011.
41. Patten, R.D., and Karas, R.H. 2006. Estrogen replacement and cardiomyocyte protection. Trends Cardiovasc. Med. 16(3): 69-75. doi:10.1016/j.tcm.2006.01.002.
42. Pollick, C., Hale, S.L., and Kloner, R.A. 1995. Echocardiographic and cardiac Doppler assessment of mice. J. Am. Soc. Echocardiogr. 8(5 Pt. 1): 602-610. doi:10.1016/S0894-7317(05)80373-6.
43. Prasad, A.M., and Inesi, G. 2011. Silencing calcineurine A subunit reduces SERCA expression in cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 300(1): H173-H180. doi:10.1152/ajpheart.00841.2010.
44. Prévilon, M., Pezet, M., Dachez, C., Mercadier, J.J., and Rouet-Benzineb, P. 2010. Sequential alterations in Akt, GSK3b and calcineurin signalling in the mouse left ventricles after thoracic aortic constriction. Can. J. Physiol. Pharmacol. 88(11): 1093-1101. doi:10.1139/Y10-087.
45. Regitz-Zagrosek, V., and Seeland, U. 2011. Sex and gender differences in myocardial hypertrophy and heart failure. Wien. Med. Wochenschr. 161(5-6): 109-116. doi:10.1007/s10354-011-0892-8.
46. Rockman, H.A., Ross, R.S., Harris, A.N., Knowlton, K.U., Steinhelper, M.E., Field, L.J., et al. 1991. Segregation of atrialspecific and inducible expression of an atrial natriuretic factor transgene in an in vivo murine model of cardiac hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 88(18): 8277-8281. doi:10.1073/pnas.88.18.8277.
47. Ronkainen, V.P., Skoumal, R., and Tavi, P. 2011. Hypoxia and HIF-1 suppress SERCA2a expression in embryonic cardiac myocytes through two interdependent hypoxia response elements. J. Mol. Cell. Cardiol. 50(6): 1008-1016. doi:10.1016/j.yjmcc.2011.02. 017.
48. Sachan, N., Dey, A., Rotter, D., Grinsfelder, D.B., Battiprolu, P.K., Sikder, D., et al. 2011. Sustained hemodynamic stress disrupts normal circadian rhythms in calcineurin-dependent signaling and protein phosphorylation in the heart. Circ. Res. 108(4): 437-445. doi:10.1161/CIRCRESAHA.110.235309.
49. Seidler, T., Teucher, N., Hellenkamp, K., Unsold, B., Grebe, C., Kramps, P., et al. 2011. Limitations of BP12.6-directed treatment strategies for maladaptive cardiac remodeling and heart failure. J. Mol. Cell. Cardiol. 50(1): 33-42. doi:10.1016/j.yjmcc.2010.08.016.
50. 2+ release from the sarcoplasmic reticulum. Circ. Res. 81(6): 1034-1044.
51. Skavdahl, M., Steenbergen, C., Clark, J., Myers, P., Demianenko, T., Mao, L., et al. 2005. Estrogen receptor-b mediates male-female difference in the development of pressure overload hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 228: H469-H476.
52. Takimoto, E., Yao, A., Toko, H., Takano, H., Shimoyama, M., Sonoda, M., et al. 2002. Sodium calcium exchanger plays a key role in alteration of cardiac function in response to pressure overload. FASEB J. 16(3): 373-378. doi:10.1096/fj.01-0735com.
53. Teiger, E., Than, V.D., Richard, L., Wisnewsky, C., Tea, B.S., Gaboury, L., et al. 1996. Apoptosis in pressure overload induced heart hypertrophy in the rat. J. Clin. Invest. 97(12): 2891-2897. doi:10.1172/JCI118747.
54. Vinet, L., Rouet-Benzineb, P., Marniquet, X., Pellegrin, N., Mangin, L., Louedec, L., et al. 2008. Chronic doxycycline exposure accelerates left ventricular hypertrophy and progression to heart failure in mice after thoracic aorta constriction. Am. J. Physiol. Heart Circ. Physiol. 295(1): H352-H360. doi:10.1152/ajpheart.01101.2007.
55. Wankerl, M., Boheler, K.R., Fiszman, M.Y., and Schwartz, K. 1996. Molecular cloning and analysis of the human cardiac sarco(endo) plasmic reticulum Ca(2+)-ATPase (SERCA2) gene promoter. J. Mol. Cell. Cardiol. 28(10): 2139-2150. doi:10.1006/jmcc.1996.0206.
56. Wehrens, X.H., and Marks, A.R. 2004. Molecular determinants of altered contractitlity in heart failure. Ann. Med. 36(Suppl. 1): 70-80. doi:10.1080/17431380410032481.
57. Weinberg, E.O., Mirotsou, M., Gannon, J., Dzau, V.J., Lee, R.T., and Pratt, R.E. 2003. Sex dependence and temporal dependence of the left ventricular genomic response to pressure overload. Physiol. Genomics, 12(2): 113-127.
58. Wilkins, B.J., Dai, Y.S., Bueno, O.F., Parsons, S.A., Xu, J., Plank, D. M., et al. 2004. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ. Res. 94(1): 110-118. doi:10.1161/01.RES.0000109415.17511.18.
59. Witt, H., Schubert, C., Jaekel, J., Fliegner, D., Penkalla, A., Tiemann, K., et al. 2008. Sex-specific pathways in early cardiac response to pressure overload in mice. J. Mol. Med. 86(9): 1013-1024. doi:10.1007/s00109-008-0385-4.
60. Xin, H.B., Senbonmatsu, T., Cheng, D.S., Wang, Y.X., Copello, J.A., Ji, G.J., et al.2002. Oestrogens protects FKBP null mice from cardiac hypertrophy. Nature 416(6878): 334-338.
61. Yano, M., Kobayashi, S., Kohno, M., Doi, M., Tokuhisa, T., Okuda, S., et al.2003. FKBP12.6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure. Circulation 107(3): 477-484.
62. 2+/calmodulin-dependent protein kinase II in cardiac hypertrophy and heart failure. Cardiovasc. Res. 63(3): 476-486. doi:10.1016/j.cardiores.2004. 04.026.