Heme oxygenase-1 inhibition of MAP kinases, calcineurin/NFAT signaling, and hypertrophy in cardiac myocytes

Cardiovascular Research

Volumn 63, Issue 3, 2004, Pages 545-552

  Tongers, Jörn ^a   Fiedler, Beate ^a   König, Danny ^a   Kempf, Tibor ^a   Klein, Gunnar ^a   Heineke, Jörg ^a   Kraft, Theresia ^a   Gambaryan, Stepan ^b   Lohmann, Suzanne M ^b   Drexler, Helmut ^a   Wollert, Kai C ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Calcium (cellular); Hypertrophy; MAP kinase; Second messengers; Signal transduction

Indexed keywords

BETA GALACTOSIDASE; CALCINEURIN; ENDOTHELIN 1; G PROTEIN COUPLED RECEPTOR; HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL ISOLATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; HEART INJURY; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART VENTRICLE HYPERTROPHY; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; RAT STRAIN; SIGNAL TRANSDUCTION; SURFACE PROPERTY;

ANIMALS; BILIVERDINE; CALCINEURIN; CARBON MONOXIDE; CELL SIZE; CELLS, CULTURED; DNA-BINDING PROTEINS; ENDOTHELIN-1; ENZYME INHIBITORS; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; MAP KINASE SIGNALING SYSTEM; MYOCYTES, CARDIAC; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 3242812018     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2004.04.015     Document Type: Article

References (49)

1. Mann D.L. Mechanisms and models in heart failure. A combinatorial approach. Circulation. 100:1999;999-1008
2. Molkentin J.D., Dorn I.G. Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu. Rev. Physiol. 63:2001;391-426
3. Sugden P.H., Clerk A. Regulation of the ERK subgroup of MAP kinase cascades through G protein-coupled receptors. Cell. Signal. 9:1997;337-351
4. Sugden P.H., Clerk A. Stress-responsive mitogen-activated protein kinases (c-Jun N-terminal kinases and p38 mitogen-activated protein kinases) in the myocardium. Circ. Res. 83:1998;345-352
5. Bueno O.F., van Rooij E., Molkentin J.D., Doevendans P.A., De Windt L.J. Calcineurin and hypertrophic heart disease. Novel insights and remaining questions. Cardiovasc. Res. 53:2002;806-821
6. Molkentin J.D. Calcineurin-NFAT signaling regulates the cardiac hypertrophic response in coordination with the MAPKs. Cardiovasc. Res. 63:2004;467-475. this issue
7. Crabtree G.R. Generic signals and specific outcomes. Signaling through Ca2+, calcineurin, and NF-AT. Cell. 96:1999;611-614
8. Yamamoto K., Ohki R., Lee R.T., Ikeda U., Shimada K. Peroxisome proliferator-activated receptor gamma activators inhibit cardiac hypertrophy in cardiac myocytes. Circulation. 104:2001;1670-1675
9. Bueno O.F., De Windt L.J., Lim H.W., et al. The dual-specificity phosphatase MKP-1 limits the cardiac hypertrophic response in vitro and in vivo. Circ. Res. 88:2001;88-96
10. Calderone A., Thaik C.M., Takahashi N., Chang D.L., Colucci W.S. Nitric oxide, atrial natriuretic peptide, and cyclic GMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts. J. Clin. Invest. 101:1998;812-818
11. Wollert K.C., Fiedler B., Gambaryan S., et al. Gene transfer of cGMP-dependent protein kinase I enhances the antihypertrophic effects of nitric oxide in cardiomyocytes. Hypertension. 39:2002;87-92
12. Fiedler B., Lohmann S.M., Smolenski A., et al. Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes. Proc. Natl. Acad. Sci. U. S. A. 99:2002;11363-11368
13. Wollert K.C., Drexler H. Regulation of cardiac remodeling by nitric oxide. Focus on cardiac myocyte hypertrophy and apoptosis. Heart Fail. Rev. 7:2002;317-325
14. Ryter S.W., Otterbein L.E., Morse D., Choi A.M. Heme oxygenase/carbon monoxide signaling pathways. Regulation and functional significance. Mol. Cell. Biochem. 234-235:2002;249-263
15. Maines M.D. The heme oxygenase system. A regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37:1997;517-554
16. McCoubrey W.K. Jr., Huang T.J., Maines M.D. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur. J. Biochem. 247:1997;725-732
17. Otterbein L.E., Bach F.H., Alam J., et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6:2000;422-428
18. Brouard S., Otterbein L.E., Anrather J., et al. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J. Exp. Med. 192:2000;1015-1026
19. Duckers H.J., Boehm M., True A.L., et al. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat. Med. 7:2001;693-698
20. Stocker R., Yamamoto Y., McDonagh A.F., Glazer A.N., Ames B.N. Bilirubin is an antioxidant of possible physiological importance. Science. 235:1987;1043-1046
21. Otterbein L.E., Choi A.M. Heme oxygenase. Colors of defense against cellular stress. Am. J. Physiol., Lung Cell. Mol. Physiol. 279:2000;L1029-L1037
22. Clark J.E., Foresti R., Sarathchandra P., et al. Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction. Am. J. Physiol. 278:2000;H643-H651
23. Yet S.F., Tian R., Layne M.D., et al. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ. Res. 89:2001;168-173
24. Yoshida T., Maulik N., Ho Y.S., Alam J., Das D.K. H(mox-1) constitutes an adaptive response to effect antioxidant cardioprotection. A study with transgenic mice heterozygous for targeted disruption of the heme oxygenase-1 gene. Circulation. 103:2001;1695-1701
25. Choi A.M. Heme oxygenase-1 protects the heart. Circ. Res. 89:2001;105-107
26. Melo L.G., Agrawal R., Zhang L., et al. Gene therapy strategy for long-term myocardial protection using adeno-associated virus-mediated delivery of heme oxygenase gene. Circulation. 105:2002;602-607
27. Nakamura K., Fushimi K., Kouchi H., et al. Inhibitory effects of antioxidants on neonatal rat cardiac myocyte hypertrophy induced by tumor necrosis factor-alpha and angiotensin II. Circulation. 98:1998;794-799
28. Hirotani S., Otsu K., Nishida K., et al. Involvement of nuclear factor-kappaB and apoptosis signal-regulating kinase 1 in G-protein-coupled receptor agonist-induced cardiomyocyte hypertrophy. Circulation. 105:2002;509-515
29. Sabri A., Hughie H.H., Lucchesi P.A. Regulation of hypertrophic and apoptotic signaling pathways by reactive oxygen species in cardiac myocytes. Antioxid. Redox Signal. 5:2003;731-740
30. Shubeita H.E., McDonough P.M., Harris A.N., et al. Endothelin induction of inositol phospholipid hydrolysis, sarcomere assembly, and cardiac gene expression in ventricular myocytes. A paracrine mechanism for myocardial cell hypertrophy. J. Biol. Chem. 265:1990;20555-20562
31. Heineke J., Kempf T., Kraft T., et al. Downregulation of cytoskeletal muscle LIM protein by nitric oxide. Impact on cardiac myocyte hypertrophy. Circulation. 107:2003;1424-1432
32. Wollert K.C., Taga T., Saito M., et al. Cardiotrophin-1 activates a distinct form of cardiac muscle cell hypertrophy. Assembly of sarcomeric units in series VIA gp130/leukemia inhibitory factor receptor-dependent pathways. J. Biol. Chem. 271:1996;9535-9545
33. Wollert K.C., Studer R., von Bulow B., Drexler H. Survival after myocardial infarction in the rat. Role of tissue angiotensin-converting enzyme inhibition. Circulation. 90:1994;2457-2467
34. Markert T., Vaandrager A.B., Gambaryan S., et al. Endogenous expression of type II cGMP-dependent protein kinase mRNA and protein in rat intestine. Implications for cystic fibrosis transmembrane conductance regulator. J. Clin. Invest. 96:1995;822-830
35. Smolenski A., Bachmann C., Reinhard K., et al. Analysis and regulation of vasodilator-stimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J. Biol. Chem. 273:1998;20029-20035
36. Graef I.A., Mermelstein P.G., Stankunas K., et al. L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons. Nature. 401:1999;703-708
37. Liu X.M., Chapman G.B., Wang H., Durante W. Adenovirus-mediated heme oxygenase-1 gene expression stimulates apoptosis in vascular smooth muscle cells. Circulation. 105:2002;79-84
38. Begum N., Sandu O.A., Ito M., Lohmann S.M., Smolenski A. Active Rho kinase (ROK-alpha ) associates with insulin receptor substrate-1 and inhibits insulin signaling in vascular smooth muscle cells. J. Biol. Chem. 277:2002;6214-6222
39. De Windt L.J., Lim H.W., Taigen T., et al. Calcineurin-mediated hypertrophy protects cardiomyocytes from apoptosis in vitro and in vivo. An apoptosis-independent model of dilated heart failure. Circ. Res. 86:2000;255-263
40. Motterlini R., Clark J.E., Foresti R., et al. Carbon monoxide-releasing molecules. Characterization of biochemical and vascular activities. Circ. Res. 90:2002;E17-E24
41. Morita T., Perrella M.A., Lee M.E., Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc. Natl. Acad. Sci. U. S. A. 92:1995;1475-1479
42. Ingi T., Cheng J., Ronnett G.V. Carbon monoxide. An endogenous modulator of the nitric oxide-cyclic GMP signaling system. Neuron. 16:1996;835-842
43. Motterlini R., Gonzales A., Foresti R., et al. Heme oxygenase-1-derived carbon monoxide contributes to the suppression of acute hypertensive responses in vivo. Circ. Res. 83:1998;568-577
44. Clark J.E., Naughton P., Shurey S., et al. Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circ. Res. 93:2003;e2-e8
45. Soff G.A., Cornwell T.L., Cundiff D.L., Gately S., Lincoln T.M. Smooth muscle cell expression of type I cyclic GMP-dependent protein kinase is suppressed by continuous exposure to nitrovasodilators, theophylline, cyclic GMP, and cyclic AMP. J. Clin. Invest. 100:1997;2580-2587
46. Huang C., Ding M., Li J., et al. Vanadium-induced nuclear factor of activated T cells activation through hydrogen peroxide. J. Biol. Chem. 276:2001;22397-22403
47. Seki T., Naruse M., Naruse K., et al. Induction of heme oxygenase produces load-independent cardioprotective effects in hypertensive rats. Life Sci. 65:1999;1077-1086
48. Raju V.S., Imai N., Liang C.S. Chamber-specific regulation of heme oxygenase-1 (heat shock protein 32) in right-sided congestive heart failure. J. Mol. Cell. Cardiol. 31:1999;1581-1589
49. Grabellus F., Schmid C., Levkau B., et al. Reduction of hypoxia-inducible heme oxygenase-1 in the myocardium after left ventricular mechanical support. J. Pathol. 197:2002;230-237