Role of the stress-activated protein kinases in endothelin-induced cardiomyocyte hypertrophy

Journal of Clinical Investigation

Volumn 102, Issue 7, 1998, Pages 1311-1320

  Choukroun, Gabriel ^a   Hajjar, Roger ^a   Kyriakis, John M ^a   Bonventre, Joseph V ^a   Rosenzweig, Anthony ^a   Force, Thomas ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

c Jun NH2 terminal kinase; Cardiomyocyte; Endothelin; Hypertrophy; Stress activated protein kinase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ATRIAL NATRIURETIC FACTOR; ENDOTHELIN 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE INHIBITOR;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; ENZYME ACTIVATION; GENE TRANSFER; HEART FAILURE; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STRESS;

EID: 0032190461     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI3512     Document Type: Article

References (63)

1. Force, T., C.M. Pombo, J.A. Avruch, J.V. Bonventre, and J.M. Kyriakis. 1996. Stress-activated protein kinases in cardiovascular disease. Circ. Res. 78: 947-953.
2. Kyriakis, J.M., and J. Avruch. 1996. Sounding the alarm: protein kinase cascades activated by stress and inflammation. J. Biol. Chem. 271:24313-24316.
3. Lenormand, P., C. Sardet, G. Pages, G. L'Allemain, A. Brunet, and J. Pouyssegur. 1993. Growth factors induce nuclear translocation of MAP kinases (p42 and p44) but not of their activator MAP kinase kinase (p45) in fibroblasts. J. Cell Biol. 122:1079-1088.
4. Hunter, J.J., N. Tanaka, H.A. Rockman, J. Ross, Jr., and K.R. Chien. 1995. Ventricular expression of the MLC-2v-ras fusion gene induces cardiac hypertrophy and selective diastolic dysfunction in transgenic mice. J. Biol. Chem. 270:23173-23178.
5. Thorburn, A., J. Thorburn, S.Y. Chen, S. Powers, H.E. Shubeita, J.R. Feramisco, and K.R. Chien. 1993. H-Ras dependent pathways can activate morphological and genetic markers of cardiac hypertrophy. J. Biol. Chem. 268: 2244-2249.
6. Thorburn, J., M. McMahon, and A. Thorburn. 1994. Raf-1 kinase activity is necessary and sufficient for gene expression changes but not sufficient for cellular morphology changes associated with cardiac myocyte hypertrophy. J. Biol. Chem. 269:30580-30586.
7. Post, G.R., D. Goldstein, D.J. Thuerauf, C.C. Glembotski, and J.H. Brown. 1996. Dissociation of p44 and p42 mitogen-activated protein kinase activation from receptor-induced hypertrophy in neonatal rat ventricular myocytes. J. Biol. Chem. 271:8452-8457.
8. Thorburn, J., J.A. Frost, and A. Thorburn. 1994. Mitogen-activated protein kinases mediate changes in gene expression, but not cytoskeletal organization associated with cardiac muscle cell hypertrophy. J. Cell Biol. 126:1565-1572.
9. Thorburn, J., S. Xu, and A. Thorburn. 1997. MAP kinase-and Rhodependent signals interact to regulate gene expression but not actin morphology in cardiac muscle cells. EMBO (Eur. Mol Biol. Organ.) J. 16:1888-1900.
10. Ramirez, M.T., V.P. Sah, X.L. Zhao, J.J. Hunter, K.R. Chien, and J.H. Brown. 1997. The MEKK-JNK pathway is stimulated by α1-adrenergic receptor and Ras activation and is associated with in vitro and in vivo cardiac hypertrophy. J. Biol. Chem. 272:14057-14061.
11. Bogoyevitch, M.A., J. Gillespie-Brown, A.J. Ketterman, S.J. Fuller, R. Ben-Levy, A. Ashworth, C.J. Marshall, and P.H. Sugden. 1996. Stimulation of the stress-activated mitogen-activated protein kinase subfamilies in perfused heart. Circ. Res. 79:162-173.
12. Zechner, D., D.J. Thuerauf, D.S. Hanford, P.M. McDonough, and C.C. Glembotski. 1997. A role for the p38 mitogen-activated protein kinase pathway in myocardial cell growth, sarcomeric organization, and cardiac-specific gene expression. J. Cell Biol. 139:115-127.
13. Wang, Y., S. Huang, V.P. Sah, J. Ross, J.H. Brown, J. Han, and K.R. Chien. 1998. Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J. Biol. Chem. 273:2161-2168.
14. 2-terminal kinase in ventricular muscle cells. J. Biol. Chem. 273:5423-5426.
15. Cohen, P. 1997. The search for physiological substrates of mitogen-and stress-activated protein kinases in mammalian cells. Trends Cell Biol. 7:353-361.
16. Sanchez, I., R.T. Hughes, B.J. Mayer, K. Yee, J.R. Woodgett, J. Avruch, J.M. Kyriakis, and L.I. Zon. 1994. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-jun. Nature. 372:794-797.
17. Verheij, M., R. Bose, X. Hua Lin, B. Yao, W.D. Jarvis, S. Grant, M.J. Birrer, E. Szabo, L.I. Zon, J.M. Kyriakis, et al. 1996. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 380: 75-79.
18. Zanke, B.W., K. Boudreau, E. Rubie, E. Winnett, L.A. Tibbies, L. Zon, J. Kyriakis, F.-F. Liu, and J.R. Woodgett. 1996. The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr. Biol. 6:606-613.
19. Ito, H., M. Hiroe, Y. Hirata, H. Fujisaka, S. Adachi, H. Akimoto, Y. Ohta, and F. Marumo. 1994. Endothelin ETa receptor antagonist blocks cardiac hypertrophy provoked by hemodynamic overload. Circulation. 89:2198-2203.
20. Arai, M., A. Yoguchi, T. Iso, T. Takahashi, S. Imai, K. Murata, and T. Suzuki. 1995. Endothelin-1 and its binding sites are upregulated in pressure overload cardiac hypertrophy. Am. J. Physiol. 268:H2084-H2091.
21. Sakai, S., T. Miyauchi, M. Kobayashi, K. Goto, and Y. Sugishita. 1996. Inhibition of myocardial endothelin pathway improves long-term survival in heart failure. Nature. 385:353-355.
22. Fraccarollo, D., K. Hu, P. Galuppo, P. Gaudron, and G. Ertl. 1997. Chronic endothelin receptor blockade attenuates progressive ventricular dilation and improves cardiac function in rats with myocardial infarction. Circulation. 96:3963-3973.
23. Hajjar, R.J., J.X. Kang, J.K. Gwathmey, and A. Rosenzweig. 1997. Physiological effects of adenoviral gene transfer of sarcoplasmic reticulum calcium ATPase in isolated rat myocytes. Circulation. 95:423-429.
24. Graham, F.L., and L. Prevec. 1991. Manipulation of adenoviral vectors. In Gene Transfer and Expression Protocols. E.J. Murray, editor. Humana Press, Inc., Clifton, NJ. 109-128.
25. Pombo, C.P., J.V. Bonventre, J. Avruch, J.R. Woodgett, J.M. Kyriakis, and T. Force. 1994. The stress-activated protein kinases (SAPKs) are major c-Jun amino-terminal kinases activated by ischemia and reperfusion. J. Biol. Chem. 269:26546-26551.
26. Pombo, C., J. Kehrl, I. Sanchez, P. Katz, J. Avruch, L. Zon, J. Woodgett, T. Force, and J. Kyriakis. 1995. Activation of the SAPK pathway by the human STE20 homolog germinal centre kinase. Nature. 377:750-754.
27. Kyriakis, J.M., P. Banerjee, E. Nikolakaki, T. Dai, E.A. Rubie, M.F. Ahmad, J. Avruch, and J.R. Woodgett. 1994. The stress-activated protein kinase subfamily of c-Jun kinases. Nature. 369:156-160.
28. Pombo, C.M., J.V. Bonventre, A. Molnar, J. Kyriakis, and T. Force. 1996. Activation of a human Ste20-like kinase by oxidant stress defines a novel stress response pathway. EMBO (Eur. Mol. Biol. Organ.) J. 15:4537-4546.
29. Lowry, O.H., N.J. Rosebrough, A.L. Farr, and R.J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
30. Bruder, J.T., and I. Kovesdi. 1997. Adenovirus infection stimulates the Raf/MAPK signalling pathway and induces interleukin-8 expression. J. Virol. 71:398-404.
31. Bokemeyer, D., A. Sorokin, M. Yan, N.G. Ahn, D.J. Templeton, and M.J. Dunn. 1996. Induction of mitogen-activated protein kinase phosphatase 1 by the stress-activated protein kinase signaling pathway but not by extracellular signal-regulated kinase in fibroblasts. J. Biol. Chem. 271:639-642.
32. Dickens, M., J.S. Rogers, J. Cavanagh, A. Raitano, Z. Xia, J.C. Halpern, M.E. Greenberg, C.L. Sawyers, and R.J. Davis. 1997. A cytoplasmic inhibitor of the JNK signal transduction pathway. Science. 277:693-696.
33. Alessandrini, A., H. Greulich, W. Huang, and R.L. Erikson. 1996. MEK1 phosphorylation site mutants activate Raf-1 in NIH3T3 cells. J. Biol. Chem. 271:31612-31618.
34. Goedert, M., A. Cuenda, M. Craxton, R. Jakes, and P. Cohen. 1997. Activation of the novel stress-activated protein kinase SAPK4 by cytokines and cellular stresses is mediated by SKK3 (MKK6); comparison of its substrate specificity with that of other SAP kinases. EMBO (Eur. Mol. Biol. Organ.) J. 16:3563-3571.
35. Whitmarsh, A.J., S.-H. Yang, M.-S. Su, A.D. Sharrocks, and R.J. Davis. 1997. Role of p38 and JNK mitogen-activated protein kinases in activation of ternary complex factors. Mol Cell. Biol. 17:2360-2371.
36. Komuro, I., and Y. Yazaki. 1993. Control of cardiac gene expression by mechanical stress. Annu. Rev. Phys. 55:55-75.
37. Pennica, D., K.J. Shaw, T.A. Swanson, M.W. Moore, D.L. Shelton, K.A. Zioncheck, A. Rosenthal, T. Taga, N.F. Paoni, and W.I. Wood. 1995. Cardiotrophin-1. Biological activities and binding to the leukemia inhibitory factor receptor/gp130 complex. J. Biol. Chem. 270:10915-10922.
38. Parker, T.G., and M.D. Schneider. 1990. Peptide growth factor can provoke "fetal" contractile protein gene expression in rat cardiac myocytes. J. Clin. Invest. 85:507-514.
39. Yamazaki, T., and Y. Yazaki. 1997. Is there a major involvement of the renin-angiotensin system in cardiac hypertrophy? Circ. Res. 81:639-642.
40. Shubita, H.E., P.M. McDonough, A.N. Harris, K.U. Knowlton, C.C. Glembotski, J.H. Brown, and K.R. Chien. 1990. Endothelin induction of inositol phospholipid hydrolysis, sarcomere assembly, and cardiac gene expression in ventricular myocytes. J. Biol. Chem. 265:20555-20562.
41. Sadoshima, J., Y. Xu, H.S. Slayter, and S. Izumo. 1993. Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell. 75:977-984.
42. Akhter, S.A., L.M. Luttrell, H.A. Rockman, G. Iaccarino, R.J. Lefkowitz, and W.J. Koch. 1998. Targeting the receptor-Gq interface to inhibit in vivo pressure overload myocardial hypertrophy. Science. 280:574-577.
43. Dérijard, B., M. Hibi, I.H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R.J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell. 76:1025-1037.
44. Han, J., J.D. Lee, L. Bibbs, and R.J. Ulevitch. 1994. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science. 265:808-811.
45. Sadoshima, J., and S. Izumo. 1993. Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes: potential involvement of an autocrine/paracrine mechanism. EMBO (Eur. Mol. Biol. Organ.) J. 12:1681-1692.
46. Bogoyevitch, M.A., A.J. Ketterman, and P.H. Sugden. 1995. Cellular stresses differentially activate c-Jun N-terminal protein kinases and extracellular signal-regulated protein kinases in cultured ventricular myocytes. J. Biol. Chem. 270:29710-29717.
47. Komuro, I., S. Kudo, T. Yamazaki, Y. Zou, I. Shiojima, and Y. Yazaki. 1996. Mechanical stretch activates the stress-activated protein kinases in cardiac myocytes. FASEB (Fed. Am. Soc. Exp. Biol.) J. 10:631-636.
48. 2-terminal kinase in cultured cardiac myocytes of neonatal rats. Circ. Res. 80:139-146.
49. 2-terminal kinases. Mol. Cell. Biol. 16:648-656.
50. Thorburn, J., M. Carlson, S.J. Mansour, K.R. Chien, N.G. Ahn, and A. Thorhurn. 1995. Inhibition of a signaling pathway in cardiac muscle cells by active mitogen activated protein kinase kinase. Mol. Biol. Cell. 6:1479-1490.
51. Marshall, C. 1995. Specificity of receptor tyrosine kinase signalling: transient versus sustained extracellular signal-regulated kinase activation. Cell. 80:179-185.
52. Nemoto, S., S. Zelin, and A. Lin. 1998. Opposing effects of Jun kinase and p38 mitogen-activated protein kinases on cardiomyocyte hypertrophy. Mol. Cell. Biol. 18:3518-3526.
53. Natesan, S., V.M. Rivera, E. Molinari, and M. Gilman. 1997. Transcriptional squelching re-examined. Nature. 390:349-350.
54. Gill, G., and M. Ptashne. 1988. Negative effect of the transcriptional activator GAL4. Nature. 334:721-724.
55. Molkentin, J.D., J.R. Lu, C.L. Antos, B. Markham, J. Richardson, J. Robbins, S.R. Grant, and E.N. Olson. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 93:215-228.
56. Chen, L., J.N.M. Glover, P.G. Hogan, A. Rao, and S.C. Harrison. 1998. Structure of the DNA-binding domains from NFAT, Fos, and Jun bound specifically to DNA. Nature. 392:42-48.
57. Pulverer, B., J.M. Kyriakis, J. Avruch, E. Nikolakaki, and J.R. Woodgett. 1991. Phosphorylation of c-jun mediated by MAP kinases. Nature. 353:670-674.
58. Karin, M. 1995. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270:16483-16486.
59. Matsuda, S., T. Moriguchi, S. Koyasu, and E. Nishida. 1998. T lymphocyte activation signals for interleukin-2 production involve activation of MKK6-p38 and MKK7-SAPK/JNK signaling pathways sensitive to cyclosporin A. J. Biol. Chem. 273:12378-12382.
60. Su, B., E. Jacinto, M. Hibi, T. Kallunki, M. Karin, and Y. Ben-Neriah. 1994. JNK is involved in signal integration during costimulation of T lymphocytes. Cell. 77:727-736.
61. Lee, Y., T. Shioi, H. Kasahara, S.M. Jobe, R.J. Wiese, B.E. Markham, and S. Izumo. 1998. The cardiac tissue-restricted homeobox protein Csx/Nkx2.5 physically associates with the zinc finger protein GATA4 and cooperatively activates atrial natriuretic factor gene expression. Mol. Cell. Biol. 18:3120-3129.
62. Durocher, D., C.Y. Chen, R.J. Ardati, R.J. Schwartz, and M. Nemer. 1996. The atrial natriuretic factor promoter is a downstream target for Nkx-2.5 in the myocardium. Mol. Cell. Biol. 16:4648-4655.
63. Molkentin, J.D., and E.N. Olson. 1997. GATA4: a novel transcriptional regulator of cardiac hypertrophy? Circulation. 96:3833-3835.