KMUP-1 attenuates endothelin-1-induced cardiomyocyte hypertrophy through activation of heme oxygenase-1 and suppression of the Akt/GSK-3β, calcineurin/NFATc4 and RhoA/ROCK pathways

Molecules

Volumn 20, Issue 6, 2015, Pages 10435-10449

  Liou, Shu Fen ^a   Hsu, Jong Hau ^b,c   Chen, You Ting ^d   Chen, Ing Jun ^d   Yeh, Jwu Lai ^d,e  

^a CHIA NAN UNIVERSITY OF PHARMACY AND SCIENCE   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^e NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

Author keywords

Cardiac hypertrophy; Endothelin 1; Heme oxygenase 1; KMUP 1; Reactive oxygen species

Indexed keywords

CALCINEURIN; ENDOTHELIN 1; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; HEME OXYGENASE 1; KMUP 1; MITOGEN ACTIVATED PROTEIN KINASE; PIPERIDINE DERIVATIVE; PROTEIN BINDING; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NFAT; XANTHINE DERIVATIVE;

ANIMAL; BIOLOGICAL MODEL; CARDIAC MUSCLE CELL; DRUG EFFECTS; ENZYME ACTIVATION; HYPERTROPHY; METABOLISM; PATHOLOGY; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CALCINEURIN; ENDOTHELIN-1; ENZYME ACTIVATION; GLYCOGEN SYNTHASE KINASE 3; HEME OXYGENASE-1; HYPERTROPHY; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; NFATC TRANSCRIPTION FACTORS; PIPERIDINES; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; RATS; REACTIVE OXYGEN SPECIES; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; XANTHINES;

EID: 84938371715     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules200610435     Document Type: Article

References (32)

1. Santulli, G. Epidemiology of Cardiovascular Disease in the 21st Century: Updated Numbers and Updated Facts. J. Cardiovasc. Dis. Res. 2013, 1, 1-2.
2. Menaouar, A.; Florian, M.; Wang, D.; Danalache, B.; Jankowski, M.; Gutkowska, J. Anti-hypertrophic effects of oxytocin in rat ventricular myocytes. Int. J. Cardiol. 2014, 175, 38-49.
3. Mishra, S.; Ling, H.; Grimm, M.; Zhang, T.; Bers, D.M.; Brown, J.H. Cardiac hypertrophy and heart failure development through Gq and CaM Kinase II signaling. J. Cardiovasc. Pharmacol. 2010, 56, 598-603.
4. Santulli, G.; Cipolletta, E.; Sorriento, D.; del Giudice, C.; Anastasio, A.; Monaco, S.; Maione, A.S.; Condorelli, G.; Puca, A.; Trimarco, B.; et al. CaMK4 Gene Deletion Induces Hypertension. J. Am. Heart Assoc. 2012, 1, e001081.
5. Yue, T.L.; Gu, J.L.; Wang, C.; Reith, A.D.; Lee, J.C.; Mirabile, R.C.; Kreutz, R.; Wang, Y.; Maleeff, B.; Parsons, A.A.; et al. Extracellular signal-regulated kinase plays an essential role in hypertrophic agonists, endothelin-1 and phenylephrineinduced cardiomyocyte hypertrophy. J. Biol. Chem. 2000, 275, 37895-37901.
6. Irukayama-Tomobe, Y.; Miyauchi, T.; Sakai, S.; Kasuya, Y.; Ogata, T.; Takanashi, M.; Iemitsu, M.; Sudo, T.; Goto, K.; Yamaguchi, I. Endothelin-1-induced cardiac hypertrophy is inhibited by activation of peroxisome proliferator-activated receptor-alpha partly via blockade of c-Jun NH2-terminal kinase pathway. Circulation 2004, 109, 904-910.
7. Shimojo, N.; Jesmin, S.; Zaedi, S.; Maeda, S.; Soma, M.; Aonuma, K.; Yamaguchi, I.; Miyauchi, T. Eicosapentanoic acid prevents endothelin-1-induced cardiomyocyte hypertrophy in vitro through the suppression of TGF-beta1 and phosphorylated JNK. Am. J. Physiol. Heart Circ. Physiol. 2006, 291, H835-H845.
8. Hunter, J.C.; Zeidan, A.; Javadov, S.; Kilić, A.; Rajapurohitam, V.; Karmazyn, M. Nitric oxide inhibits endothelin-1-induced neonatal cardiomyocyte hypertrophy via a RhoA-ROCK-dependent pathway. J. Mol. Cell. Cardiol. 2009, 47, 810-818.
9. Wang, N.; Guan, P.; Zhang, J.P.; Li, Y.Q.; Chang, Y.Z.; Shi, Z.H.; Wang, F.Y.; Chu, L. Fasudil hydrochloride hydrate, a Rho-kinase inhibitor, suppresses isoproterenol-induced heart failure in rats via JNK and ERK1/2 pathways. J. Cell. Biochem. 2011, 112, 1920-1929.
10. Wu, B.N.; Lin, R.J.; Lin, C.Y.; Shen, K.P.; Chiang, L.C.; Chen, I.J. A xanthine-based KMUP-1 with cyclic GMP enhancing and K+ channels opening activities in rat aortic smooth muscle. Br. J. Pharmacol. 2001, 134, 265-274.
11. Wu, B.N.; Chen, C.W.; Liou, S.F.; Yeh, J.L.; Chung, H.H.; Chen, I.J. Inhibition of proinflammatory tumor necrosis factor-{alpha}-induced inducible nitric-oxide synthase by xanthine-based 7-[2-[4-(2-chlorobenzene)piperazinyl]ethyl]-1,3-dimethylxanthine (KMUP-1) and 7-[2-[4-(4-nitrobenzene)piperazinyl]ethyl]-1,3-dimethylxanthine (KMUP-3) in rat trachea: The involvement of soluble guanylate cyclase and protein kinase G. Mol. Pharmacol. 2006, 70, 977-985.
12. Liu, C.M.; Lo, Y.C.; Wu, B.N.; Wu, W.J.; Chou, Y.H.; Huang, C.H.; An, L.M.; Chen, I.J. cGMP-enhancing- and alpha1A/alpha1D-adrenoceptor blockade-derived inhibition of Rho-kinase by KMUP-1 provides optimal prostate relaxation and epithelial cell anti-proliferation efficacy. Prostate 2007, 67, 1397-1410.
13. Liu, C.M.; Lo, Y.C.; Tai, M.H.; Wu, B.N.; Wu, W.J.; Chou, Y.H.; Chai, C.Y.; Huang, C.H.; Chen, I.J. Piperazine-designed alpha 1A/alpha 1D-adrenoceptor blocker KMUP-1 and doxazosin provide down-regulation of androgen receptor and PSA in prostatic LNCaP cells growth and specifically in xenografts. Prostate 2009, 69, 610-623.
14. Yeh, J.L; Hsu, J.H.; Wu, P.J; Liou, S.F.; Liu, C.P.; Chen, I.J.; Wu, B.N.; Dai, Z.K.; Wu, J.R. KMUP-1 attenuates isoprenaline-induced cardiac hypertrophy in rats through NO/cGMP/PKG and ERK1/2/calcineurin A pathways. Br. J. Pharmacol. 2010, 159, 1151-1160.
15. Liu, C.P.; Dai, Z.K.; Huang, C.H.; Yeh, J.L.; Wu, B.N.; Wu, J.R.; Chen, I.J. Endothelial nitric oxide synthase-enhancing G-protein coupled receptor antagonist inhibits pulmonary artery hypertension by endothelin-1-dependent and endothelin-1-independent pathways in a monocrotaline model. Kaohsiung J. Med. Sci. 2014, 30, 267-278.
16. Bueno, O.F.; Molkentin, J.D. Involvement of extracellular signal-regulated kinases 1/2 in cardiac hypertrophy and cell death. Circ. Res. 2002, 91, 776-781.
17. Afanas'ev, I. ROS and RNS signaling in heart disorders: Could antioxidant treatment be successful? Oxid. Med. Cell. Longev. 2011, 2011, 293769.
18. Tocchetti, C.G.; Molinaro, M.; Angelone, T.; Lionetti, V.; Madonna, R.; Mangiacapra, F.; Moccia, F.; Penna, C.; Sartiani, L.; Quaini, F.; et al. Nitroso-Redox Balance and Modulation of Basal Myocardial Function: an Update from the Italian Society of Cardiovascular Research (SIRC). Curr. Drug Targets 2015, in press.
19. Hirotani, S.; Otsu, K.; Nishida, K.; Higuchi, Y.; Morita, T.; Nakayama, H.; Yamaguchi, O.; Mano, T.; Matsumura, Y.; Ueno, H.; et al. Involvement of nuclear factor-kappaB and apoptosis signal-regulating kinase 1 in G-protein-coupled receptor agonist- induced cardiomyocyte hypertrophy. Circulation 2002, 105, 509-515.
20. Yang, H.Y.; Liu, J.C.; Chen, Y.L.; Chen, C.H.; Lin, H.; Lin, J.W.; Chiu, W.T.; Chen, J.J.; Cheng, T.H. Inhibitory effect of trilinolein on endothelin-1-induced c-fos gene expression in cultured neonatal rat cardiomyocytes. Naunyn Schmiedeberg's Arch. Pharmacol. 2005, 372, 160-167.
21. Laskowski, A.; Woodman, O.L.; Cao, A.H.; Drummond, G.R.; Marshall, T.; Kaye, D.M.; Ritchie, R.H. Antioxidant actions contribute to the antihypertrophic effects of atrial natriuretic peptide in neonatal rat cardiomyocytes. Cardiovasc. Res. 2006, 72, 112-123.
22. Tongers, J.; Fiedler, B.; König, D.; Kempf, T.; Klein, G.; Heineke, J.; Kraft, T.; Gambaryan, S.; Lohmann, S.M.; Drexler, H.; et al. Heme oxygenase-1 inhibition of MAP kinases, calcineurin/NFAT signaling, and hypertrophy in cardiac myocytes. Cardiovasc. Res. 2004, 63, 545-552.
23. Li, R.; Zheng, W.; Pi, R.; Gao, J.; Zhang, H.; Wang, P.; Le, K.; Liu, P. Activation of peroxisome proliferator-activated receptor-alpha prevents glycogen synthase 3beta phosphorylation and inhibits cardiac hypertrophy. FEBS Lett. 2007, 581, 3311-3316.
24. Maillet, M, van Berlo, J.H.; Molkentin, J.D. Molecular basis of physiological heart growth: fundamental concepts and new players. Nat. Rev. Mol. Cell. Biol. 2013, 14, 38-48.
25. Wilkins, B.J.; Dai, Y.S.; Bueno, O.F.; Parsons, S.A.; Xu, J.; Plank, D.M.; Jones, F.; Kimball, T.R.; Molkentin, J.D. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ. Res. 2004, 94, 110-118.
26. Marx, S.O.; Marks, A.R. Dysfunctional ryanodine receptors in the heart: new insights into complex cardiovascular diseases. J. Mol. Cell. Cardiol. 2013, 58, 225-231.
27. Yuan, Q.; Chen, Z.; Santulli, G.; Gu, L.; Yang, Z.G.; Yuan, Z.Q.; Zhao, Y.T., Xin, H.B.; Deng, K.Y.; Wang, S.Q.; et al. Functional role of Calstabin2 in age-related cardiac alterations. Sci. Rep. 2014, 4, 7425, doi:10.1038/srep07425.
28. Dong, M.; Ding, W.; Liao, Y.; Liu, Y.; Yan, D.; Zhang, Y.; Wang, R.; Zheng, N.; Liu, S.; Liu, J. Polydatin prevents hypertrophy in phenylephrine induced neonatal mouse cardiomyocytes and pressure-overload mouse models. Eur. J. Pharmacol. 2015, 746, 186-197.
29. Yan, L.; Zhang, J.D.; Wang, B.; Lv, Y.J.; Jiang, H.; Liu, G.L.; Qiao, Y.; Ren, M.; Guo, X.F. Quercetin inhibits left ventricular hypertrophy in spontaneously hypertensive rats and inhibits angiotensin II-induced H9C2 cells hypertrophy by enhancing PPAR-γ expression and suppressing AP-1 activity. PLoS ONE 2013, 8, e72548.
30. Hilfiker-Kleiner, D.; Hilfiker, A.; Castellazzi, M.; Wollert, K.C.; Trautwein, C.; Schunkert, H.; Drexler, H. JunD attenuates phenylephrine-mediated cardiomyocyte hypertrophy by negatively regulating AP-1 transcriptional activity. Cardiovasc. Res. 2006, 71, 108-117.
31. Sorriento, D.; Santulli, G.; Fusco, A.; Anastasio, A.; Trimarco, B.; Iaccarino, G. Intracardiac injection of AdGRK5-NT reduces left ventricular hypertrophy by inhibiting NF-kappaB-dependent hypertrophic gene expression. Hypertension 2010, 56, 696-704.
32. Wang, B.; Shravah, J.; Luo, H.; Raedschelders, K.; Chen, D.D.; Ansley, D.M. Propofol protects against hydrogen peroxide-induced injury in cardiac H9c2 cells via Akt activation and Bcl-2 up-regulation. Biochem. Biophys. Res. Commun. 2009, 389, 105-111.