Changes in Cx43 and NaV1.5 expression precede the occurrence of substantial fibrosis in calcineurin-induced murine cardiac hypertrophy

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Fontes, Magda S C ^a   Raaijmakers, Antonia J A ^a   Van Doorn, Tessa ^a   Kok, Bart ^a   Nieuwenhuis, Sylvia ^a   Van Der Nagel, Roel ^a   Vos, Marc A ^a   De Boer, Teun P ^a   Van Rijen, Harold V M ^a   Bierhuizen, Marti F A ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CONNEXIN 43; MICRORNA 21; RNA; SODIUM CHANNEL NAV1.5; TRANSFORMING GROWTH FACTOR BETA1; CONNECTIVE TISSUE GROWTH FACTOR; CTGF PROTEIN, MOUSE; FIBRILLAR COLLAGEN; SCN5A PROTEIN, MOUSE; TGFB1 PROTEIN, MOUSE; TIMP1 PROTEIN, MOUSE; TISSUE INHIBITOR OF METALLOPROTEINASE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COL1A1 GENE; COL1A2 GENE; COL3A1 GENE; CONTROLLED STUDY; CTGF GENE; DISEASE ACTIVITY; FEMALE; GENE; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; IMMUNOREACTIVITY; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TGFB1 GENE; TIMP1 GENE; WILD TYPE; ANIMAL; C57BL MOUSE; CARDIOMEGALY; FIBROSIS; GENE EXPRESSION; GENETICS; HEART MUSCLE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; METABOLISM; NEWBORN; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; CALCINEURIN; CARDIOMEGALY; CONNECTIVE TISSUE GROWTH FACTOR; CONNEXIN 43; FEMALE; FIBRILLAR COLLAGENS; FIBROSIS; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCARDIUM; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84900312554     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087226     Document Type: Article

References (46)

1. Diedrichs H, Chi M, Boelck B, Mehlhorn U, Schwinger RH (2004) Increased regulatory activity of the calcineurin/NFAT pathway in human heart failure. Eur J Heart Fail 6: 3-9. (Pubitemid 38169598)
2. Haq S, Choukroun G, Lim H, Tymitz KM, del Monte F, et al. (2001) Differential activation of signal transduction pathways in human hearts with hypertrophy versus advanced heart failure. Circulation 103: 670-677. (Pubitemid 32144195)
3. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, et al. (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93: 215-228. (Pubitemid 28180855)
4. Kleber AG, Rudy Y (2004) Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol Rev 84: 431-488. (Pubitemid 38365490)
5. Fontes MS, van Veen TA, de Bakker JM, van Rijen HV (2012) Functional consequences of abnormal Cx43 expression in the heart. Biochim Biophys Acta 1818: 2020-2029.
6. Severs NJ, Bruce AF, Dupont E, Rothery S (2008) Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res 80: 9-19.
7. Borlak J, Thum T (2003) Hallmarks of ion channel gene expression in end-stage heart failure. FASEB J 17: 1592-1608. (Pubitemid 37100061)
8. Shang LL, Pfahnl AE, Sanyal S, Jiao Z, Allen J, et al. (2007) Human heart failure is associated with abnormal C-terminal splicing variants in the cardiac sodium channel. Circ Res 101: 1146-1154. (Pubitemid 350146441)
9. Valdivia CR, Chu WW, Pu J, Foell JD, Haworth RA, et al. (2005) Increased late sodium current in myocytes from a canine heart failure model and from failing human heart. J Mol Cell Cardiol 38: 475-483. (Pubitemid 40331938)
10. Soltysinska E, Olesen SP, Christ T, Wettwer E, Varro A, et al. (2009) Transmural expression of ion channels and transporters in human nondiseased and end-stage failing hearts. Pflügers Arch 459: 11-23.
11. Rook MB, Evers MM, Vos MA, Bierhuizen MF (2012) Biology of cardiac sodium channel Nav1.5 expression. Cardiovasc Res 93: 12-23.
12. Creemers EE, Pinto YM (2011) Molecular mechanisms that control interstitial fibrosis in the pressure-overloaded heart. Cardiovasc Res 89: 265-272.
13. V1.5, Cx40 and Cx43 is reduced by different mechanisms. J Mol Cell Cardiol 45: 373-384.
14. van Veen TA, van Rijen HV, Wiegerinck RF, Opthof T, Colbert MC, et al. (2002) Remodeling of gap junctions in mouse hearts hypertrophied by forced retinoic acid signaling. J Mol Cell Cardiol 34: 1411-1423. (Pubitemid 35244418)
15. Sweat F, Puchter H, Rosenthal SI (1964) Sirius Red F3Ba as a stain for connective tissue. Arch Pathol 1964: 69-72.
16. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
17. de Boer TP, van Veen TA, Bierhuizen MF, Kok B, Rook MB, et al. (2007) Connexin43 repression following epithelium-to-mesenchyme transition in embryonal carcinoma cells requires Snail1 transcription factor. Differentiation 75: 208-218. (Pubitemid 46426620)
18. Teunissen BE, Jansen AT, Mutsaers NA, Vuerhard MJ, Vos MA, et al. (2007) Primary structure, organization, and expression of the rat connexin45 gene. DNA Cell Biol 26: 108-115. (Pubitemid 46363876)
19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
20. Fieller EC (1940) The Biological Standardization of Insulin. Suppl to J R Statist Soc 7: 1-64.
21. R Core Team (2012) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. pp. ISBN 3-900051-900007-900050, The R project for statistical computing website. Available: http://www.R-project.org/. Accessed 2013 Dec 30.
22. Arnolds DE, Liu F, Fahrenbach JP, Kim GH, Schillinger KJ, et al. (2012) TBX5 drives Scn5a expression to regulate cardiac conduction system function. J Clin Invest 122: 2509-2518.
23. Guo J, Zhan S, Somers J, Westenbroek RE, Catterall WA, et al. (2006) Decrease in density of INa is in the common final pathway to heart block in murine hearts overexpressing calcineurin. Am J Physiol Heart Circ Physiol 291: H2669-2679. (Pubitemid 44904066)
24. Marquez-Rosado L, Solan JL, Dunn CA, Norris RP, Lampe PD (2012) Connexin43 phosphorylation in brain, cardiac, endothelial and epithelial tissues. Biochim Biophys Acta 1818: 1985-1992.
25. Hatanaka K, Kawata H, Toyofuku T, Yoshida K (2004) Down-regulation of connexin43 in early myocardial ischemia and protective effect by ischemic preconditioning in rat hearts in vivo. Jpn Heart J 45: 1007-1019. (Pubitemid 40528871)
26. Thum T (2012) MicroRNA therapeutics in cardiovascular medicine. EMBO Mol Med 4: 3-14.
27. van Rooij E, Olson EN (2012) MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat Rev Drug Discov 11: 860-872.
28. Small EM, Olson EN (2011) Pervasive roles of microRNAs in cardiovascular biology. Nature 469: 336-342.
29. Anderson C, Catoe H, Werner R (2006) MIR-206 regulates connexin43 expression during skeletal muscle development. Nucleic Acids Res 34: 5863-5871. (Pubitemid 44941165)
30. Fabritz L, Hoogendijk MG, Scicluna BP, van Amersfoorth SC, Fortmueller L, et al. (2011) Load-reducing therapy prevents development of arrhythmogenic right ventricular cardiomyopathy in plakoglobin-deficient mice. J Am Coll Cardiol 57: 740-750.
31. Oxford EM, Musa H, Maass K, Coombs W, Taffet SM, et al. (2007) Connexin43 remodeling caused by inhibition of plakophilin-2 expression in cardiac cells. Circ Res 101: 703-711. (Pubitemid 47494101)
32. Li J, Patel VV, Kostetskii I, Xiong Y, Chu AF, et al. (2005) Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ Res 97: 474-481. (Pubitemid 41298178)
33. Chu G, Carr AN, Young KB, Lester JW, Yatani A, et al. (2002) Enhanced myocyte contractility and Ca2+ handling in a calcineurin transgenic model of heart failure. Cardiovasc Res 54: 105-116.
34. Lombardi R, Betocchi S, Losi MA, Tocchetti CG, Aversa M, et al. (2003) Myocardial collagen turnover in hypertrophic cardiomyopathy. Circulation 108: 1455-1460. (Pubitemid 37176451)
35. Pauschinger M, Doerner A, Remppis A, Tannhauser R, Kuhl U, et al. (1998) Differential myocardial abundance of collagen type I and type III mRNA in dilated cardiomyopathy: effects of myocardial inflammation. Cardiovasc Res 37: 123-129. (Pubitemid 28122624)
36. Daniels A, van Bilsen M, Goldschmeding R, van der Vusse GJ, van Nieuwenhoven FA (2009) Connective tissue growth factor and cardiac fibrosis. Acta Physiol (Oxf) 195: 321-338.
37. Ruiz-Ortega M, Rodriguez-Vita J, Sanchez-Lopez E, Carvajal G, Egido J (2007) TGF-beta signaling in vascular fibrosis. Cardiovasc Res 74: 196-206.
38. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, et al. (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456: 980-984.
39. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, et al. (2008) Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 105: 13027-13032.
40. Duisters RF, Tijsen AJ, Schroen B, Leenders JJ, Lentink V, et al. (2009) miR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circ Res 104: 170-178.
41. Matkovich SJ, Wang W, Tu Y, Eschenbacher WH, Dorn LE, et al. (2010) MicroRNA-133a protects against myocardial fibrosis and modulates electrical repolarization without affecting hypertrophy in pressure-overloaded adult hearts. Circ Res 106: 166-175.
42. Adam O, Lohfelm B, Thum T, Gupta SK, Puhl SL, et al. (2012) Role of miR-21 in the pathogenesis of atrial fibrosis. Basic Res Cardiol 107: 278.
43. Patrick DM, Montgomery RL, Qi X, Obad S, Kauppinen S, et al. (2010) Stress-dependent cardiac remodeling occurs in the absence of microRNA-21 in mice. J Clin Invest 120: 3912-3916.
44. Jansen JA, van Veen TA, de Jong S, van der Nagel R, van Stuijvenberg L, et al. (2012) Reduced Cx43 expression triggers increased fibrosis due to enhanced fibroblast activity. Circ Arrhythm Electrophysiol 5: 380-390.
45. Camelliti P, Green CR, LeGrice I, Kohl P (2004) Fibroblast network in rabbit sinoatrial node: structural and functional identification of homogeneous and heterogeneous cell coupling. Circ Res 94: 828-835. (Pubitemid 38451745)
46. Leoni AL, Gavillet B, Rougier JS, Marionneau C, Probst V, et al. (2010) Variable Na(v)1.5 protein expression from the wild-type allele correlates with the penetrance of cardiac conduction disease in the Scn5a(+/2) mouse model. PLoS One 5: e9298.