Pro-inflammatory cytokines stimulate mitogen-activated protein kinase subfamilies, increase phosphorylation of c-Jun and ATF2 and upregulate c-Jun protein in neonatal rat ventricular myocytes

Journal of Molecular and Cellular Cardiology

Volumn 31, Issue 12, 1999, Pages 2087-2099

  Clerk, Angela ^a   Harrison, Joanne G ^a   Long, Carlin S ^b   Sugden, Peter H ^a  

^a IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^b DENVER HEALTH AND HOSPITAL AUTHORITY   (United States)

Author keywords

Interleukin 1 ; Intracellular signalling; p38 mitogen activated protein kinases; Pro inflammatory cytokines; Stress activated protein kinases c Jun N terminal kinases; Transcription factors; Tumour necrosis factor

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CYTOKINE; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHORBOL ESTER; PROTEIN C JUN; PROTEIN KINASE C INHIBITOR; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HEART CELL CULTURE; HEART VENTRICLE WALL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RAT;

ANIMALIA;

EID: 0033387191     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmcc.1999.1040     Document Type: Article

References (92)

1. Alessi DR. The protein kinase C inhibitors Ro 318220 and GF 109203X are equally potent inhibitors of MAPKAPK kinase-1β (Rsk-2) and p70 S6 kinase. FEBS Lett. 402:1997;121-123.
2. Bankers F, Kalli KR, McKean DJ. Interleukin-1 signal transduction. Life Sci. 59:1996;61-83.
3. Binetruy B, Smeal T, Karin M. Ha-Ras augments c-Jun activity and stimulates phosphorylation of its activation domain. Nature. 351:1991;122-127.
4. Blum A, Miller H. Role of cytokines in heart failure. Am Heart J. 135:1998;181-186.
5. Bogoyevitch MA, Glennon PE, Sugden PH. Endothelin-1, phorbol esters and phenylephrine stimulate MAP kinase activities in ventricular cardiomyocytes. FEBS Lett. 317:1993a;271-275.
6. Bogoyevitch MA, Parker PJ, Sugden PH. Characterization of protein kinase C isotype expression in adult rat heart. Protein kinase C- ε is a major isotype present, and it is activated by phorbol esters, epinephrine and endothelin. Circ Res. 72:1993b;757-767.
7. Bogoyevitch MA, Glennon PE, Andersson MB, Clerk A, Lazou A, Marshall CJ, Parker PJ, Sugden PH. Endothelin-1 and fibroblast growth factors stimulate the mitogen-activated protein kinase signaling cascade in cardiac myocytes. The potential role of the cascade in the integration of two signaling pathways leading to myocyte hypertrophy. J Biol Chem. 269:1994;1110-1119.
8. Bogoyevitch MA, Ketterman AJ, Sugden PH. Cellular stresses activate c-Jun N-terminal protein kinases (JNKs) in ventricular myocytes cultured from neonatal rat hearts. J Biol Chem. 270:1995a;29710-29717.
9. Bogoyevitch MA, Clerk A, Sugden PH. Activation of the mitogen-activated protein kinase cascade by pertussis toxin-sensitive and -insensitive pathways in cultured ventricular cardiomyocytes. Biochem J. 309:1995b;437-443.
10. Bogoyevitch MA, Gillespie-Brown J, Ketterman AJ, Fuller SJ, Ben-Levy R, Ashworth A, Marshall CJ, Sugden PH. Stimulation of the stress-activated mitogen-activated protein kinases subfamilies in perfused heart. p38/RK (HOG-1-related) kinases and c-Jun N-terminal kinases (JNK/SAPKs) are activated by ischemia-reperfusion. Circ Res. 79:1996;161-172.
11. Bossy-Wetzel E, Bakiri L, Yaniv M. Induction of apoptosis by the transcription factor c-Jun. EMBO J. 16:1997;1695-1709.
12. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:1976;248-254.
13. Carpenter CL, Cantley LC. Phosphoinositide kinases. Curr Opin Cell Biol. 8:1996;153-158.
14. Chien KR, Knowlton KU, Zhu H, Chien S. Regulation of cardiac gene expression during myocardial growth and hypertrophy: molecular studies of an adaptive physiologic response. FASEB J. 5:1991;3037-3046.
15. Clerk A, Bogoyevitch MA, Andersson MB, Sugden PH. Differential activation of protein kinase C isoforms by endothelin-1 and phenylephrine, and subsequent stimulation of p42 and p44 mitogen-activated protein kinases in ventricular myocytes cultured from neonatal rat hearts. J Biol Chem. 269:1994;32848-32857.
16. Clerk A, Michael A, Sugden PH. The G protein coupled receptor agonists, endothelin-1 and phenylephrine, stimulate p38 mitogen-activated protein kinase pathway in neonatal rat ventricular myocytes. J Cell Biol. 142:1998a;523-535.
17. Clerk A, Fuller SJ, Michael A, Sugden PH. Stimulation of "stress-regulated" mitogen-activated protein kinases (SAPKs/JNKs and p38-MAPKs) in perfused rat hearts by oxidative and other stresses. J Biol Chem. 273:1998b;7228-7234.
18. Clerk A, Sugden PH. Cell stress-induced phosphorylation of ATF2 and c-Jun transcription factors in rat ventricular myocytes. Biochem J. 325:1997;801-810.
19. Clerk A, Sugden PH. The p38-MAPK inhibitor, SB203580, inhibits cardiac stress-activated protein kinases/c-Jun N-terminal kinases (SAPKs/JNKs). FEBS Lett. 426:1998;93-96.
20. Coffer PJ, Jin J, Woodgett JR. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem J. 335:1998;1-13.
21. Cohen P. The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trends Cell Biol. 7:1997;353-361.
22. 1phase of the cell cycle is determined by the duration of mitogen-activated protein kinase activation. Mol Cell Biol. 19:1999;330-341.
23. Devary Y, Gottlieb RA, Smeal T, Karin M. The mammalian ultraviolet response element is triggered by activation of src tyrosine kinases. Cell. 71:1992;1081-1091.
24. Dignam JD, Lebowvitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1983;1475-1489.
25. Domin J, Waterfield MD. Using structure to define the function of phosphoinositide 3-kinase family members. FEBS Lett. 410:1997;91-95.
26. Eder J. Tumour necrosis factor α and interleukin 1 signalling: do MAPKK kinases connect it all? Trends Biochem Sci. 18:1997;319-322.
27. Force T, Pombo CM, Avruch JA, Bonventre JV, Kyriakis JM. Stress-activated protein kinases in cardiovascular disease. Circ Res. 78:1996;947-953.
28. Francis SE, Holden H, Holt CM, Duff GW. Interleukin-1 in myocardium and coronary arteries of patients with dilated cardiomyopathy. J Mol Cell Cardiol. 30:1998;215-223.
29. Frangogiannis NG, Youker KA, Rossen RD, GwechenÍberger M, Lindsey MH, Mendoza LH, Michael LH, Ballantyne CM, Smith CW, Entman ML. Cytokines and the microcirculation in ischemia and reperfusion. J Mol Cell Cardiol. 30:1998a;2567-2576.
30. Frangogiannis NG, Lindsey ML, Michael LH, Youker KA, Bressler RB, Mendoza LH, Spengler RN, Smith CW, Entman ML. Resident cardiac mast cells degranulate and release preformed TNF- α, initiating the cytokine cascade in experimental canine myocardial ischemia/reperfusion. Circulation. 98:1998b;699-710.
31. Freshney NW, Rawlinson L, Guesdon F, Jones E, Cowley S, Saklatvala J. Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of Hsp27. Cell. 78:1994;1039-1049.
32. Fritz G, Kaina B. Activation of c-Jun N-terminal kinase 1 by UV irradiation is inhibited by wortmannin without affecting c- jun expression. Mol Cell Biol. 19:1999;1768-1774.
33. 2-terminal kinases target the ubiquitination of their associated transcription factors. J Biol Chem. 272:1997;32163-32168.
34. Garrington TP, Johnson GL. Organization and regulation of mitogen-activated protein kinase pathways. Curr Opin Cell Biol. 11:1999;211-218.
35. Goedert M, Cuenda A, Craxton M, Jakes R, Cohen P. 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 J. 16:1997;3563-3571.
36. Guay J, Lambert H, Gingras-Breton G, Lavoie JN, Huot J, Landry J. Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci. 110:1997;357-368.
37. Gupta S, Campbell D, Dérijard B, Davis RJ. Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science. 267:1995;389-393.
38. Gupta S, Barrett T, Whitmarsh AJ, Cavanagh J, Sluss HK, Dérijard B, Davis RJ. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15:1996;2760-2770.
39. Han TH, Lamph WW, Prywes R. Mapping of the epidermal growth factor-, serum-, and phorbol ester-responsive sequence elements in the c- jun promoter. Mol Cell Biol. 12:1992;4472-4477.
40. Herskowitz A, Choi S, Ansari AA, Wesselingh S. Cytokine mRNA expression in postischemic/reperfused myocardium. Am J Pathol. 146:1995;419-428.
41. Huang C, Ma WY, Dong Z. The extracellular-signal-regulated protein kinases (Erks) are required for UV-induced AP-1 activation in JB6 cells. Oncogene. 18:1999;2828-2835.
42. Ing DJ, Zang J, Dzau VJ, Webster KA, Bishopric NH. Modulation of cytokine-induced cardiac myocyte apoptosis by nitric oxide, Bad, and Bcl-x. Circ Res. 84:1999;21-33.
43. 1-mediated response. J Biol Chem. 265:1990;13809-13817.
44. Johnson NL, Gardner AM, Diener KM, Lange-Carter CA, Gleavy J, Jarpe MB, Minden A, Karin M, Zon LI, Johnson GL. Signal transduction pathways regulated by mitogen-activated/extracellular response kinase kinase kinase induce cell death. J Biol Chem. 271:1996;3229-3237.
45. Kameshita I, Fujisawa H. A sensitive method for detection of calmodulin protein kinase II activity in sodium dodecyl sulfate - polyacrylamide gel. Anal Biochem. 183:1989;139-143.
46. Kapadia S, Dibbs Z, Kurrelmeyer K, Kaira D, Seta Y, Wang F, Bozkurt B, Oral H, Sivasubramanian N, Mann DL. The role of cytokines in the failing human heart. Cardiol Clin. 16:1998;645-656.
47. Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. J Biol Chem. 270:1995;16483-16486.
48. 2-terminal kinase and induction of apoptosis after detachment of epithelial cells. J Cell Biol. 139:1997;1017-1023.
49. Knight RJ, Buxton DB. Stimulation of c-Jun kinase and mitogen-activated protein kinase by ischemia and reperfusion in the perfused rat heart. Biochem Biophys Res Commun. 218:1996;83-88.
50. Kolomytkin OV, Marino AA, Sadasivan KK, Wolf RE, Albright JA. Intracellular signaling mechanisms of interleukin-1 β in synovial fibroblasts. Am J Physiol. 276:1999;C9-C15.
51. Krown KA, Page MT, Nguyen C, Zechner D, Gutierrez V, Comstock KL, Glembotski CC, Quintana PJE, Sabbadini RA. Tumor necrosis factor alpha-induced apoptosis in cardiac myocytes. Involvement of the sphingolipid signaling cascade in cardiac cell death. J Clin Invest. 98:1996;2854-2865.
52. Kubota T, McTiernan R, Frye CS, Slawson SE, Lemster BH, Koretsky AP, Demetris AJ, Feldman AM. Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-α Circ Res. 81:1997;627-635.
53. Kumar S, McDonnell PC, Gum RJ, Hand AT, Lee JC, Young PR. Novel homologues of CSBP/p38 MAP kinase: activation, substrate specificity and sensitivity to inhibition by pyridinyl imidazoles. Biochem Biophys Res Commun. 235:1997;533-538.
54. Kyriakis JM, Avruch J. Sounding the alarm: protein kinase cascades activated by stress and inflammation. J Biol Chem. 271:1996;24313-24316.
55. LaPointe MC, Isenovic E. Interleukin-1 β regulation of inducible nitric oxide synthase and cyclooxygenase-2 involves the p42/44 and p38 MAPK signaling pathways in cardiac myocytes. Hypertension. 33(1S):1999;276-282.
56. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J. Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol. 15:1995;505-516.
57. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, Green D, McNulty D, Blumenthal MJ, Heys RJ, Landvatter SW, Strickler JE, McLaughlin MM, Siemens IR, Fisher SM, Livi GP, White JR, Adams JL, Young PR. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature. 372:1994;739-746.
58. Lee JC, Young PR. Role of CSB/p38/RK stress response kinase in LPS and cytokine signaling mechanisms. J Leukocyte Biol. 59:1996;152-157.
59. Lenczowski JM, Dominguez L, Eder AM, King LB, Zacharchuk CM, Ashwell JD. Lack of a role for Jun kinase and AP-1 in Fas-induced apoptosis. Mol Cell Biol. 17:1997;170-181.
60. Leppä S, Saffrich R, Ansorge W, Bohmann D. Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation. EMBO J. 17:1998;4404-4413.
61. Levine B, Kalman J, Mayer L, Fillit HM, Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. N Engl J Med. 323:1990;236-241.
62. Livingstone C, Patel G, Jones N. ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO J. 14:1995;1785-1797.
63. Mann DL. Stress activated cytokines and the heart. Cytokine Growth Factor Rev. 7:1996;341-354.
64. Marte BM, Downward J. PKB/Akt: connecting phosphoinositide 3-kinase to cell survival and beyond. Trends Biochem Sci. 22:1997;355-358.
65. Musial A, Mandal A, Coroneos E, Kester M. Interleukin-1 and endothelin stimulate distinct species of diglycerides that differentially regulate protein kinase C in mesangial cells. J Biol Chem. 270:1995;21632-21638.
66. Oral H, Kapadia S, Nakano M, Torre-Amione G, Lee J, Lee-Jackson D, Young JB, Mann DL. Tumor necrosis factor- α and the failing human heart. Clin Cardiol. 18 (Suppl. 4):1995;IV20-27.
67. Palmer JN, Hartogensis WE, Patten M, Fortuin FD, Long CS. Interleukin-1 β induces cardiac myocyte growth but inhibits cardiac fibroblast proliferation in culture. J Clin Invest. 95:1995;2555-2564.
68. 1-adrenergic induced gene expression in cultured cardiac myocytes. J Biol Chem. 271:1996;21134-21141.
69. Platanias LC, Vogelzang NJ. Interleukin-1: biology, pathophysiology, and clinical prospects. Am J Med. 89:1990;621-629.
70. Pulverer BJ, Kyriakis JM, Avruch J, Nikolakaki E, Woodgett JR. Phosphorylation of c-jun mediated by MAP kinases. Nature. 353:1991;670-674.
71. Radler-Pohl A, Sachsenmaier C, Gebel S, Auer HP, Bruder JT, Rapp U, Angel P, Rahmsdorf HJ, Herrlich P. UV induced activation of AP-1 involves obligatory extranuclear steps including Raf-1 kinase. EMBO J. 12:1993;1005-1012.
72. 1-adrenergic receptor and ras activation and is associated within vitro and in vivo cardiac hypertrophy. J Biol Chem. 272:1997;14057-14061.
73. Roulston A, Reinhard C, Amiri P, Williams LT. Early activation of c-Jun N-terminal kinase and p38 kinase regulate cell survival in response to tumor necrosis factorα J Biol Chem. 273:1998;10232-10239.
74. Rouse J, Cohen P, Trigon S, Morange M, Alonso-Llamazares A, Zamanillo D, Hunt T, Nebreda AR. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell. 78:1994;1027-1037.
75. Schaeffer HT, Weber MJ. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol Cell Biol. 19:1999;2435-2444.
76. Seger R, Krebs EG. The MAPK signaling cascade. FASEB J. 9:1995;726-735.
77. Shan K, Kurrelmeyer K, Seta Y, Wang F, Dibbs Z, Deswal A, Lee-Jackson D, Mann DL. The role of cytokines in disease progression in heart failure. Curr Opin Cardiol. 12:1997;218-223.
78. Smeal T, Binetruy B, Mercola D, Birrer M, Karin M. Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73. Nature. 354:1991;494-496.
79. Smith SB, Johnson KS. Single step purification of polypeptides expressed in Escherichia coli as fusions with glutathione-S-transferase. Gene. 67:1988;31-40.
80. Stein B, Angel P, van Dam H, Ponta H, Herrlich P, van der Eb A, Rahmsdorf HJ. Ultraviolet-radiation induced c- jun gene transcription: two AP-1 like binding sites mediate the response. Photochem Photobiol. 55:1992;409-415.
81. 2+, and phospholipase A2 in endothelial cells postinfarction heart failure. Am J Physiol. 276:1999;H1493-H1501.
82. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA. 76:1979;4350-4354.
83. Treinies I, Paterson HF, Hooper S, Wilson R, Marshall CJ. Activated MEK stimulates expression of AP-1 components independently of phosphatidylinositol 3-kinase (PI3-kinase) but requires a PI3-kinase signal to stimulate DNA synthesis. Mol Cell Biol. 19:1999;321-329.
84. van Dam H, Wilhelm D, Herr I, Steffen A, Herrlich P, Angel P. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c- jun induction in response to genotoxic agents. EMBO J. 14:1995;1798-1811.
85. Vassalli P. The pathophysiology of tumor necrosis factors. Ann Rev Immunol. 10:1992;411-452.
86. 2-terminal kinase in ventricular muscle cells. J Biol Chem. 273:1998a;5423-5426.
87. Wang Y, Huang S, Sah VP, Ross J, Brown JH, Han J, Chien KR. Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J Biol Chem. 273:1998b;2161-2168.
88. Whitmarsh AJ, Yang S-H, Su MS-S, Sharrocks AD, Davis RJ. Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors. Mol Cell Biol. 17:1997;2360-2371.
89. Wisdom R, Johnson RS, Moore C. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J. 18:1999;188-197.
90. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 270:1995;1326-1331.
91. Yue P, Massie BM, Simpson PC, Long CS. Cytokine expression increases in non-myocyte from rats with postinfarction heart failure. Am J Physiol. 275:1998;H250-H258.
92. Zechner D, Thuerauf DJ, Hanford DS, McDonough PM, Glembotski CC. A role for the p38 mitogen-activated protein kinase pathway in myocardial cell growth, sarcomeric organization, and cardiac-specific gene expression. J Cell Biol. 139:1997;115-127.