Nuclear pore rearrangements and nuclear trafficking in cardiomyocytes from rat and human failing hearts

Cardiovascular Research

Volumn 105, Issue 1, 2015, Pages 31-43

  Chahine, Mirna N ^a   Mioulane, Maxime ^a   Sikkel, Markus B ^a   O'Gara, Peter ^a   Dos Remedios, Cristobal G ^b   Pierce, Grant N ^c   Lyon, Alexander R ^a,d   Földes, Gábor ^a   Harding, Sian E ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF MANITOBA   (Canada)

^d ROYAL BROMPTON HOSPITAL   (United Kingdom)

Author keywords

Hypertrophy; Myocardial infarction; Myocytes; Nuclear transport; Signal transduction

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; EXPORTIN 1; KARYOPHERIN ALPHA; KARYOPHERIN BETA; LEPTOMYCIN B; MITOGEN ACTIVATED PROTEIN KINASE P38; NUCLEOPORIN; PHENYLEPHRINE; PROTEIN P62; TRICHOSTATIN A; HISTONE DEACETYLASE; NUCLEAR LOCALIZATION SIGNAL;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CELL SIZE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DOWN REGULATION; HEART FAILURE; HEART INFARCTION; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; HUMAN; HUMAN TISSUE; INVESTIGATIVE PROCEDURES; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR SIZE; NUCLEOCYTOPLASMIC TRANSPORT; OBSERVATIONAL STUDY; PRIORITY JOURNAL; RAT; UPREGULATION; ACTIVE TRANSPORT; ANIMAL; BIOLOGICAL MODEL; CARDIOMEGALY; DISEASE MODEL; MALE; METABOLISM; NUCLEAR PORE; PATHOLOGY; SPRAGUE DAWLEY RAT;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CARDIOMEGALY; CARDIOMYOPATHY, DILATED; DISEASE MODELS, ANIMAL; HEART FAILURE; HISTONE DEACETYLASES; HUMANS; MALE; MODELS, CARDIOVASCULAR; MYOCYTES, CARDIAC; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PORE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84929086575     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu218     Document Type: Article

References (38)

1. Zhang QJ, Chen HZ, Wang L, Liu DP, Hill JA, Liu ZP. The histone trimethyllysine demethylase JMJD2A promotes cardiac hypertrophy in response to hypertrophic stimuli in mice. J Clin Invest 2011;121:2447-2456.
2. Hill JA, Olson EN. Cardiac plasticity. N Engl J Med 2008;358:1370-1380.
3. Perez-Terzic C, Gacy AM, Bortolon R, Dzeja PP, Puceat M, Jaconi M, Prendergast FG, Terzic A. Directed inhibition of nuclear import in cellular hypertrophy. J Biol Chem 2001;276:20566-20571.
4. Kehat I, Molkentin JD. Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation 2010;122:2727-2735.
5. Olson EN, Schneider MD. Sizing up the heart: development redux in disease. Genes Dev 2003;17:1937-1956.
6. Gö rlich D, Mattaj IW. Nucleocytoplasmic transport. Science 2003;271:1513-1518.
7. Faustino RS, Cheung P, Richard MN, Dibrov E, Kneesch AL, Deniset JF, Chahine MN, Lee K, Blackwood D, Pierce GN. Ceramide regulation of nuclear protein import. J Lipid Res 2008;49:654-662.
8. Faustino RS, Stronger LN, Richard MN, Czubryt MP, Ford DA, Prociuk MA, Dibrov E, Pierce GN. RanGAP-mediated nuclear protein import in vascular smooth muscle cells is augmented by lysophosphatidylcholine. Mol Pharmacol 2007;71:438-445.
9. Chahine MN, PierceGN. Therapeutic targeting of nuclear protein import in pathological cell conditions. Pharmacol Rev 2009;61:358-372.
10. Cortés R, Roselló-Llet E, Rivera M, Martnez-Dolz L, Salvador A, Azorn I, Portolés M. Influence of heart failure on nucleocytoplasmic transport in human cardiomyocytes. Cardiovasc Res 2010;85:464-472.
11. Perez-Terzic C, Gacy AM, Bortolon R, Dzeja PP, Puceat M, Jaconi M, Prendergast FG, Terzic A. Structural plasticity of the cardiac nuclear pore complex in response to regulators of nuclear import. Circ Res 1999;84:1292-1301.
12. Hallhuber M, Burkard N, Wu R, Buch MH, Engelhardt S, Hein L, Neyses L, Schuh K, Ritter O. Inhibition of nuclear import of calcineurin prevents myocardial hypertrophy. Circ Res 2006;99:626-635.
13. Lyon AR, MacLeod KT, Zhang Y, Garcia E, Kanda GK, Lab MJ, Korchev YE, Harding SE, Gorelik J. Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart. Proc Natl Acad Sci USA 2009;106: 6854-6859.
14. Harding SE, Jones SM, O'Gara P, del Monte F, Vescovo G, Poole-Wilson PA. Isolated ventricular myocytes from failing and non-failing human heart; the relation of age and clinical status of patients to isoproterenol response. J Mol Cell Cardiol 1992;24: 549-564.
15. Harding SE, Vescovo G, Kirby M, Jones SM, Gurden J, Poole-Wilson PA. Contractile responses of isolated adult rat and rabbit cardiac myocytes to isoproterenol and calcium. J Mol Cell Cardiol 1988;20:635-647.
16. Fö ldes G, Mioulane M, Wright JS, Liu AQ, Novak P, Merkely B, Gorelik J, Schneider MD, Ali NN, Harding SE. Modulation of human embryonic stem cell-derived cardiomyocyte growth: a testbed for studying human cardiac hypertrophy? J Mol Cell Cardiol 2010;50: 367-376.
17. McKinsey TA, Kass DA. Small-molecule therapies for cardiac hypertrophy: moving beneath the cell surface. Nat Rev Drug Discov 2007;6:617-635.
18. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 2006;7:589-600.
19. Bartoli M, Claycomb WC. Transfer of macromolecules into living adult cardiomyocytes by microinjection. Mol Cell Biochem 1997;172:103-109.
20. Richard MN, Deniset JF, Kneesh AL, Blackwood D, Pierce GN. Mechanical stretching stimulates smooth muscle cell growth, nuclear protein import, and nuclear pore expression through mitogen-activated protein kinase activation. J Biol Chem 2007;282: 23081-23088.
21. Chahine MN, Blackwood DP, Dibrov E, Richard MN, Pierce GN. Oxidized LDL affects smooth muscle cell growth throughMAPK-mediated actions on nuclear protein import. J Mol Cell Cardiol 2009;46:431-441.
22. Chahine MN, Dibrov E, BlackwoodDP, PierceGN. Mechanical stretch enhances the oxidized LDL-induced growth, nuclear import and nuclear pore expression of smooth muscle cells through induction of endogenous HSP60 and ERK1/2 activation. Can J Plant Protect 2012;90:1559-1568.
23. Hasegawa Y, Iizuka-Kogo A, Akiyama T, Senda T. High expression of Pitx-2 in the ICATdeficient metanephros leads to developmental arrest. Acta Histochem Cytochem 2010;43: 51-59.
24. Lyon AR, Bannister ML, Collins T, Pearce E, Sepehripour AH, Dubb SS, Garcia E, O'Gara P, Liang L, Kohlbrenner E, Hajjar RJ, Peters NS, Poole-Wilson PA, Macleod KT, Harding SE. SERCA 2a gene transfer decreases sarcoplasmic reticulum calcium leak and reduces ventricular arrhythmias in a model of chronic heart failure. Circ Arrhythm Electrophysiol 2011;4:362-372.
25. Monovich L, Koch KA, Burgis R, Osimboni E, Mann T, Wall D, Gao J, Feng Y, Vega RB, Turner BA, Hood DB, Law A, Papst PJ, Koditek D, Chapo JA, Reid BG, Melvin LS, Pagratis NC, McKinsey TA. Suppression of HDAC nuclear export and cardiomyocyte hypertrophy by novel irreversible inhibitors of CRM1. Biochim Biophys Acta 2009; 1789:422-431.
26. del Monte F, O'Gara P, Poole-Wilson PA, Yacoub M, Harding SE. Cell geometry and contractile abnormalities of myocytes from failing human left ventricle. Cardiovasc Res 1995; 30:281-290.
27. Nikolaev VO, Moshkov A, Lyon AR, Miragoli M, Novak P, Paur H, Lohse MJ, Korchev YE, Harding SE, Gorelik J. Beta2-adrenergic receptor redistribution in heart failure changes cAMP compartmentation. Science 2010;327:1653-1657.
28. Simpson P. Stimulation of hypertrophy of cultured neonatal rat heart cells through an alpha 1-adrenergic receptor and induction of beating through an alpha 1-and beta 1-adrenergic receptor interaction. Circ Res 1985;56:884-894.
29. Behr TM, Nerurkar SS, Nelson AH, Coatney RW, Woods TN, Sulpizio A, Chandra S, Brooks DP, Kumar S, Lee JC, Ohlstein EH, Angermann CE, Adams JL, Sisko J, Sackner-Bernstein JD, Willette RN. Hypertensive end-organ damage and premature mortality are p38 mitogen-activated protein kinase-dependent in a rat model of cardiac hypertrophy and dysfunction. Circulation 2001;104:1292-1298.
30. Dash R, Schmidt AG, Pathak A, Gerst MJ, Biniakiewicz D, Kadambi VJ, Hoit BD, Abraham WT, Kranias EG. Differential regulation of p38 mitogen-activated protein kinase mediates gender-dependent catecholamine-induced hypertrophy. Cardiovasc Res 2003;57:704-714.
31. Kyoi S, Otani H, Matsuhisa S, Akita Y, Tatsumi K, Enoki C, Fujiwara H, Imamura H, Kamihata H, Iwasaka T. Opposing effect of p38 MAP kinase and JNK inhibitors on the development of heart failure in the cardiomyopathic hamster. Cardiovasc Res 2006;69: 888-898.
32. Liu YH, Wang D, Rhaleb NE, Yang XP, Xu J, Sankey SS, Rudolph AE, Carretero OA. Inhibition of p38 mitogen-activated protein kinase protects the heart against cardiac remodeling in mice with heart failure resulting from myocardial infarction. J Card Fail 2005; 11:74-81.
33. Wenzel S, Muller C, Piper HM, Schluter KD. p38 MAP-kinase in cultured adult rat ventricular cardiomyocytes: expression and involvement in hypertrophic signalling. Eur J Heart Fail 2005;7:453-460.
34. Petrich BG, Wang Y. Stress-activated MAP kinases in cardiac remodeling and heart failure: new insights from transgenic studies. Trends Cardiovasc Med 2004;14:50-55.
35. Wenzel S, Abdallah Y, Helmig S, Schafer C, Piper HM, Schluter KD. Contribution of PI 3-kinase isoforms to angiotensin II-and alpha-adrenoceptor-mediated signalling pathways in cardiomyocytes. Cardiovasc Res 2006;71:352-362.
36. Czubryt MP, Austria JA, Pierce GN. Hydrogen peroxide inhibition of nuclear protein import is mediated by the mitogen-activated protein kinase, ERK2. J Cell Biol 2000; 148:7-16.
37. Cao DJ, Wang ZV, Battiprolu PK, Jiang N, Morales CR, Kong Y, Rothermel BA, Gillette TG, Hill JA. Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc Natl Acad Sci USA 2011;108:4123-4128. s
38. Harrison BC, Roberts CR, HoodDB, SweeneyM, Gould JM, BushEW, McKinseyTA. The CRM1 nuclear export receptor controls pathological cardiac gene expression. Mol Cell Biol 2004; 24:10636-10649.