Role of MAP kinases in nitric oxide induced muscle-derived adult stem cell apoptosis

Cell Biology International

Volumn 33, Issue 7, 2009, Pages 711-719

  Bironaite, D ^a   Baltriukiene, D ^a   Uralova, N ^a   Stulpinas, A ^a   Bukelskiene, V ^a   Imbrasaite, A ^a   Kalvelyte, A ^a  

^a VILNIUS UNIVERSITY   (Lithuania)

Author keywords

Heart; MAPK; NO; Signaling; Stem cells

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 3,3 BIS(2 AMINOETHYL) 1 HYDROXY 2 OXOTRIAZENE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; PROTEIN C JUN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; GROWTH INHIBITION; HEART FAILURE; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MUSCLE CELL; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; RABBIT; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL TRANSPLANTATION;

ADULT STEM CELLS; ANIMALS; APOPTOSIS; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLES; NITRIC OXIDE DONORS; NITROSO COMPOUNDS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-JUN; RABBITS; SIGNAL TRANSDUCTION;

EID: 67649262219     PISSN: 10656995     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cellbi.2009.03.007     Document Type: Article

References (78)

1. Albina J.E., Cui S., Mateo R., and Reichner J.S. Nitric oxide-mediated apoptosis in murine peroitoneal macrophages. J Immunol 150 (1993) 5080-5085
2. Andreka P., Zang J., Dougherty C., Slepak T.I., Webster K.A., and Bishopric N.H. Cytoprotection by Jun kinase during nitric oxide-induced cardiac myocyte apoptosis. Circ Res 88 (2001) 305-312
3. Babu G.J., Lalli J.M., Sussman M.A., Sadoshima J., and Periasamy M. Phosphorylation of elk-1 by MEK/ERK pathway is necessary for c-fos gene activation during cardiac myocyte hypertrophy. J Mol Cell Cardiol 32 (2000) 1447-1457
4. Bironaite D.A., Imbrasaite A., Stulpinas A., and Kalvelyte V. Modulation of c-Jun expression in leukemic cells undergoing apoptosis after chemotherapeutic treatment. Biologija 4 (2003) 47-50
5. Borutaitė V., Morkūnienė R., and Brown G.C. Nitric oxide donors, nitrosithiols and mitochondrial respiration inhibitors induce caspase activation by different mechanisms. FEBS Lett 467 (2000) 155-159
6. Bukelskienė V., Baltriukienė D., Bironaitė D., Imbrasaitė A., Širmenis R., Balčiūnas M., et al. Muscle-derived primary stem cell lines for heart repair. Semin Cardiol 11 (2006) 1-7
7. Callsen D., and Brune B. Role of mitogen-activated protein kinases in S-nitrosoglutathione-induced macrophage apoptosis. Biochemistry 38 (1999) 2279-2286
8. Cano E., and Mahadevan L.C. Parallel signal processing among mammalian MAPKs. Trends Biochem Sci 20 (1995) 117-122
9. Choi J., Yip-Schneider M., Albertin F., Wiesenauer C., Wang Y., and Schmidt C.M. The effect of Doxorubicin on MEK-ERK signaling predicts its efficacy in HCC. J Surg Res (2008)
10. Choukroun G., Hajjar R., Fry S., Del Monte F., Haq S., Guerrero J.L., et al. Regulation of cardiac hypertrophy in vivo by the stress-activated protein kinases/c-Jun NH(2)-terminal kinases. J Clin Invest 104 (1999) 391-398
11. Christopherson K.S., and Bredt D.S. Nitric oxide in excitable tissues: physiological roles and disease. J Clin Invest 100 (1997) 2424-2429
12. Cicconi S., Ventura N., Pastore D., Bonini P., Di Nardo P., Lauro R., et al. Characterization of apoptosis signal transduction pathways in HL-5 cardiomyocytes exposed to ischemia/reperfusion oxidative stress model. J Cell Physiol 195 (2003) 27-37
13. Cohen P. The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trends Cell Biol 7 (1997) 353-361
14. Communal C., Colucci W.S., and Singh K. p38 mitogen-activated protein kinase pathway protects adult rat ventricular myocytes against beta-adrenergic receptor-stimulated apoptosis. Evidence for Gi-dependent activation. J Biol Chem 275 (2000) 19395-19400
15. Cui S., Reichner J.S., Mateo R.B., and Albina J.E. Activated murine macrophages induce apoptosis in tumor cells through nitric oxide-dependent or - independent mechanisms. Cancer Res 54 (1994) 2462-2467
16. De Windt L.J., Lim H.W., Taigen T., Wencker D., Condorelli G., Dorn II G.W., 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
17. Dougherty C.J., Kubasiak L.A., Prentice H., Andreka P., Bishopric N.H., and Webster K.A. Activation of c-Jun N-terminal kinase promotes survival of cardiac myocytes after oxidative stress. Biochem J 362 (2002) 561-571
18. Fehsel K., Kroncke K.D., Meyer K.L., Huber H., Wahn V., and Kolb-Bachofen V. Nitric oxide induces apoptosis in mouse thymocytes. J Immunol 155 (1995) 2858-2865
19. Garrington T.P., and Johnson G.L. Organization and regulation of mitogen activated protein kinase signaling pathways. Curr Opin Cell Biol 11 (1999) 211-218
20. Gill C., Mestril R., and Samali A. Losing heart: the role of apoptosis in heart disease. A novel therapeutic target?. FASEB J 16 (2002) 135-146
21. Gupta S., Campbell D., Derijard B., and Davis R.J. Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267 (1995) 389-393
22. Gustafsson A.B., and Gottlieb R.A. Mechanisms of apoptosis in the heart. J Clin Immunol 23 (2003) 447-459
23. Hall J.P., Merithew E., and Davis R.J. c-Jun N-terminal kinase (JNK) repression during the inflammatory response? Just say NO. Proc Natl Acad Sci U S A 97 26 (2000) 14022-14024
24. He H., Li H.L., Lin A., and Gottlieb R.A. Activation of the JNK pathway is important for cardiomyocytes death in response to stimulated ischemis. Cell Death Differ 6 (1999) 987-989
25. Holly T.A., Drincic A., Byun Y., Nakamura S., Harris K., Klocke F.J., et al. Caspase inhibition reduces myocyte cell death induced by myocardial ischemia and reperfusion in vivo. J Mol Cell Cardiol 31 (1999) 1709-1715
26. Ing D.J., Zang J., Dzau V.J., Webster K.A., and Bishopric N.H. Modulation of cytokine-induced cardiac myocyte apoptosis by nitric oxide, Bak, and Bcl-x. Circ Res 84 (1999) 21-33
27. Iwai-Kanai E., Hasegawa K., Fujita M., Araki M., Yamazume T., Adachi S., et al. Basic fibroblast growth factor protects cardiac myocytes from iNOS-mediated apoptosis. J Cell Physiol 190 (2002) 54-62
28. Iwase H., Robin E., Guzy R.D., Mungai P.T., Vanden Hoek T.L., Chandel N.S., et al. Nitric oxide during ischemia attenuates oxidant stress and cell death during ischemia and reperfusion in cardiomyocytes. Free Radic Biol Med 43 (2007) 590-599
29. Johnson N.L., Gardner A.M., Diener K.M., Lange-Carter C.A., Gleavy J., Jarpe M.B., et al. Signal transduction pathway regulated by mitogen-activated/extracellular response kinase kinase kinase induced cell death. J Biol Chem 271 (1996) 3229-3237
30. Kaiser R.A., Bueno O.F., Lips D.J., Doevendans P.A., Jones F., Kimball T.F., et al. Targeted inhibition of p38 mitogen-activated protein kinase antagonizes cardiac injury and cell death following ischemia reperfussion in vivo. J Biol Chem 279 (2004) 15524-15530
31. Kim Y.M., Kim T.H., Chung H.T., Talanian R.V., Yin X.M., and Billar T.R. Nitric oxide prevents tumor necrosis factor alpha-induced rat hepatocyte apoptosis by the interruption of mitochondrial apoptotic signaling through S-nitrosylation of caspase-8. Hepatology 32 (2000) 770-778
32. Kim S.J., Hwang S.G., Shin D.Y., Kang S.S., and Chun J.S. p38 kinase regulates nitric oxide-induced apopotosis of articular chondrocytes by accumulatin p53 via NFkB-dependent transcription and stabilization by serine 15 phosphorylation. J Biol Chem 277 (2002) 33501-33508
33. Kitta K., Day R.M., Kim Y., Torregroza I., Evans T., and Suzuki Y.J. Hepatocyte growth factor induces GATA-4 phosphorylation and cell survival in cardiac muscle cells. J Biol Chem 278 (2003) 4705-4712
34. Kolch W., Heidecker G., Kochs G., Hummel R., Vahidi H., Mischak H., et al. Protein kinase Cα activates Raf-1 by direct phosphorylation. Nature 364 (1993) 249-252
35. Lawler J.M., and Songt W. Specificity of antioxidant enzyme inhibition in skeletal muscle to reactive nitrogen specias donors. Biochem Biophys Res Comm 294 (2002) 1093-1100
36. Ley R., Balmanno K., Hadfield K., Weston C., and Cook S.J. Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein. Bim J Biol Chem 278 (2003) 18811-18816
37. Li R.K., Weisel R.D., Mickle D.A., Jia Z.Q., Kim E.J., Sakai T., et al. Autologous porcine heart cell transplantation improved heart function after a myocardial infarction. J Thorac Cardiovasc Surg 119 (2000) 62-68
38. Liang Q., Bueno O.F., Wilkins B.J., Kuan C.Y., Xia Y., and Molkentin J.D. c-Jun N-terminal kinases (JNK) antagonize cardiac growth through crosstalk with calcineurin-NFAT signaling. EMBO J 22 (2003) 5079-5089
39. Liebermann D.A., Gregory B., and Hoffman B. AP-1 (Fos/Jun) transcription factors in hematopoietic differentiation and apoptosis. Int J Oncol 12 (1998) 685-700
40. Mackay K., and Mochly-Rosen D. An inhibitor of p38 mitogen-activated protein kinase protects neonatal cardiac myocytes from ischemia. J Biol Chem 274 (1999) 6272-6279
41. Mackay K., and Mochly-Rosen D. Involvement of a p38 mitogen-activated protein kinase phosphatase in protecting neonatal rat cardiac myocytes from ischemia. J Mol Cell Cardiol 32 (2000) 1585-1588
42. Mayr M., Hu Y., Hainaut H., and Xu Q. Mechanical stress-induced DNA damage and rac-p38MAPK signal pathways mediate p53-dependent apoptosis in vascular smooth muscle cells. FASEB J 16 (2002) 1423-1425
43. Mercille S., and Massie B. Induction of apoptosis in nutrient-deprived cultures of hybridoma and myeloma cells. Biotechnol Bioeng 44 (1994) 1140-1154
44. Minamino T., Yujiri T., Terada N., Taffet G.E., Michael L.H., Johnson G.L., et al. MEKK1 is essential for cardiac hypertrophy and dysfunction induced by Gq. Proc Natl Acad Sci U S A 99 (2002) 3866-3871
45. Molkentin J.D., and Dorn II G.W. Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu Rev Physiol 63 (2001) 391-426
46. Müller-Ehmsen J., Whittaker P., Kloner R.A., Sakoda T., Long T.I., Laird P.W., et al. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. J Mol Cell Cardiol 36 (2002) 107-116
47. Nelson D.P., Setser E., Hall D.G., Schwartz S.M., Hewitt T., Klevitsky R., et al. Proinflammatory consequences of transgenic fas ligand expression in the heart. J Clin Invest 105 (2000) 1199-1208
48. Nishimoto S., and Nishida E. MAPK signalling: ERK5 versus ERK1/2. EMBO Rep 7 (2006) 782-786
49. Otsu K., Yamashita N., Nishida K., Hirotani S., Yamaguchi O., Watanabe T., et al. Disruption of a single copy of the p38α MAP kinase gene leads to cardioprotection against ischemia-reperfusion. Biochem Biophys Res Commun 302 (2003) 56-60
50. Párrizas M., Saltiel A.R., and LeRoith D. Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 3′-kinase and mitogen-activated protein kinase pathways. J Biol Chem 272 (1997) 154-161
51. Peter M.E., and Krammer P.H. The CD95 (APO-1/Fas) DISC and beyond. Cell Death Differ 10 (2003) 26-35
52. Potapova O., Basu S., Mercola D., and Holbrook N.J. Protective role for c-Jun in the cellular response to DNA damage. J Biol Chem 276 (2001) 28546-28553
53. Price M.A., Cruzalegui F.H., and Treisman R. The p38 and ERK MAP kinase pathways cooperate to activate Ternary Complex Factors and c-fos transcription in response to UV light. EMBO J 15 (1996) 6552-6563
54. Radi R., Peluffo G., Alvarez M.N., Naviliat M., and Cayota A. Unraveling peroxynitrite formation in biological systems. Free Radic Biol Med 30 (2001) 463-488
55. Remondino A., Kwon S.H., Communal C., Pimentel D.R., Sawyer D.B., Singh K., et al. b-adrenergic receptor-stimulated apoptosis in cardiac myocytes is mediated by reactive oxygen species/c-Jun NH2-terminal kinase-dependent activation of the mitochondrial pathway. Circ Res 92 (2003) 136-138
56. Sabbah H.N., and Sharov V.G. Apoptosis in heart failure. Prog Cardiovasc Dis 40 (1998) 549-562
57. Sabbah H.N., Sharov V.G., and Goldstein S. Programmed cell death in the progression of heart failure. Ann Med 1 (1998) 33-38
58. Sharov V.G., Todor A., Suzuki G., Morita H., Tanhehco E.J., and Sabbah H.N. Hypoxia, angiotensin-II, and norepinephrine mediated apoptosis is stimulus specific in canine failed cardiomyocytes: a role for p38 MAPK, Fas-L and cyclin D1. Eur J Heart Fail 5 (2003) 121-129
59. Shaulian E., and Karin M. AP-1 in cell proliferation and survival. Oncogene 20 (2001) 2390-2400
60. Sheng Z., Knowlton K., Chen J., Hoshijima M., Brown J.H., and Chien K.R. Cardiotrophin-1 (CT-1) inhibition of cardiac myocyte apoptosis via a mitogen-activated protein kinase-dependent pathway. Divergence from downstream CT-1 signals for myocardial cell hypertrophy. J Biol Chem 272 (1997) 5783-5791
61. Shinmura K., Tang X.L., Takano H., Hill M., and Bolli R. Nitric oxide donors attenuate myocardial stunning in conscious rabbits. Am J Physiol 277 (1999) H2495-H2503
62. Shinoda C., Maruyama M., Fujishita T., Dohkan J., Oda H., Shinoda K., et al. Doxorubicin induces expression of multidrug resistance-associated protein 1 in human small cell lung cancer cell lines by the c-jun N-terminal kinase pathway. Int J Cancer 117 (2005) 21-31
63. Steenbergen C., Afsari C.A., Petranka J.G., Collins J., Martin K., Bennett L., et al. Alteration in apoptotic signaling in human idiopathic cardiomyopathic hearts in failure. Am J Physiol Heart Circ Physiol 284 (2003) H268-H276
64. Steenbergen C. The role of p38 mitogen-activated protein kinase in myocardial ischemia/reperfusion injury; relationship to ischemic preconditioning. Basic Res Cardiol 97 (2002) 276-285
65. Stefanelli C., Pignatti C., Tantini B., Stanic I., Bonavita F., Muscari C., et al. Nitric oxide can function as either a killer molecule or an antiapoptotic effector in cardiomyocytes. Biochim Biophys Acta 1450 (1999) 406-413
66. Stewart C.E. The physiology of stem cells: potential for the elderly patient. J Musculoskelet Neuronal Interact 4 (2004) 179-183
67. Sugden P.H., and Bogoyevitch M. Intracellular signaling through protein kinases in the heart. Cardiovasc Res 30 (1995) 478-492
68. Sugden P.H. Signaling pathways in cardiac myocyte hypertrophy. Ann Med 33 (2001) 611-622
69. Sun W., Kesavan K., Schaefer B.C., Garrington T.P., Ware M., Johnson N.L., et al. MEKK2 associates with the adapter protein Lad/RIBP and regulates the MEK5-BMK1/ERK5 pathway. J Biol Chem 276 (2001) 5093-5100
70. Taimor G., Rakow A., and Piper H.M. Transcription activator protein 1 (AP-1) mediates NO induced apoptosis of adult cardiomyocytes. FASEB J 15 (2001) 2518-2520
71. Tournier C., Hess P., Yang D.D., Xu J., Turner T.K., Nimnual A., et al. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288 (2000) 870-874
72. Usuki F., Fujita E., and Sasagawa N. Methylmercury activates ASK1/JNK signaling pathways, leading to apoptosis due to both mitochondria- and endoplasmic reticulum (ER)-generated processes in myogenic cell lines. Neurotoxicology 29 1 (2008) 22-30
73. Warne P.H., Viciana P.R., and Downward J. Direct interaction of Ras and the amino-terminal region of Raf-1 in vitro. Nature 364 (1993) 352-355
74. Widmann C., Gibson S., Jarpe M.B., and Johnson G.L. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79 (1999) 143-180
75. Wollert K.C., Fiedler B., Gambaryan S., Smolenski A., Heineke J., Butt E., et al. Gene transfer of cGMPdependent protein kinase I enhances the antihypertrophic effects of nitric oxide in cardiomyocytes. Hypertension 39 (2002) 87-92
76. Xia Z., Dickens M., Raingeaud J., Davis R.J., and Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270 5240 (1995) 1326-1331
77. Yamamoto K., Ichijo H., and Korsmeyer S.J. Bcl-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol Cell Biol 19 (1999) 8469-8478
78. Zhou H.Z., Karliner J.S., and Gray M.O. Moderate alcohol consumption induces sustained cardiac protection by activating PKCε and Akt. Am J Physiol Heart Circ Physiol 283 (2002) H165-H174