Stimulation of the stress-activated mitogen-activated protein kinase subfamilies in perfused heart: p38/RK mitogen-activated protein kinases and c-Jun N-terminal kinases are activated by ischemia/reperfusion

Circulation Research

Volumn 79, Issue 2, 1996, Pages 162-173

  Bogoyevitch, Marie A ^a   Gillespie Brown, Judith ^a   Ketterman, Albert J ^a   Fuller, Stephen J ^a   Ben Levy, Rachel ^a   Ashworth, Alan ^a   Marshall, Christopher J ^a   Sugden, Peter H ^a,b  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

c Jun N terminal kinase; ischemia reperfusion; mitogen activated protein kinase; p38 reactivating kinase; stress activated mitogen activated protein kinase

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; ONCOPROTEIN; PROTEIN KINASE ACTIVATOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HEART PERFUSION; HEART VENTRICLE WALL; MALE; MITOGENESIS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION REGULATION;

EID: 0030036727     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.79.2.162     Document Type: Article

References (108)

1. 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. 1991;5:3037-3046.
2. Jennings RB, Reimer KA. The cell biology of acute myocardial ischemia. Annu Rev Med. 1991;42:225-246.
3. Ferrari R, Ceconi C, Curello C, Alfieri O, Visioli O. Myocardial damage during ischaemia and reperfusion. Eur Heart J. 1994;14(suppl G):25-30.
4. Olivetti G, Capasso JM, Meggs LG, Sonnenblick EH, Anversa P. Cellular basis of chronic ventricular remodeling after myocardial infarction in rats. Circ Res. 1991;68:856-869.
5. Gerdes AM, Kellerman SE, Moore JA, Muffly KE, Clark LC, Reaves PY, Malec KB, McKeown PP, Schocken DD. Structural remodeling of cardiac myocytes in patients with ischemic cardiomyopathy. Circulation. 1992;86:426-430.
6. Brand T, Sharma HS, Fleischmann KE, Duncker DJ, McFalls EO, Verdouw PD, Schaper W. Proto-oncogene expression in porcine myocardium subjected to ischemia and reperfusion. Circ Res. 1992;71:1351-1360.
7. Webster KA, Discher DJ, Bishopric NH. Induction and nuclear accumulation of fos and jun proto-oncogenes in hypoxic cardiac myocytes. J Biol Chem. 1993;268:16852-16858.
8. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. I986;74:1124-1136.
9. Parratt JR. Protection of the heart by ischaemic preconditioning: mechanisms and possibilities for pharmacological exploitation. Trends Pharmacol Sci. 1994;15:19-25.
10. Davis RJ. MAPKs: new JNK expands the group. Trends Biochem Sci. 1994;19:470-473.
11. Cano E, Mahadevan LC. Parallel signal processing among mammalian MAPKs. Trends Biochem Sci. 1995;20:117-122.
12. Marshall CJ. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr Opin Gen Dev. I994;4:82-89.
13. Cobb MH, Goldsmith EJ. How MAP kinases are regulated. J Biol Chem. 1995;270:14843-14846.
14. Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 1995;80:179-185.
15. Seger R, Krebs EG. The MAPK signaling cascade. FASEB J. 1995;9:726-735.
16. Sugden PH, Bogoyevitch MA. Intracellular signalling through protein kinases in the heart. Cardiovasc Res. 1995;30:478-492.
17. Bogoyevitch MA, Sugden PH. The role of protein kinases in adaptational growth of the heart. Int J Biochem Cell Biol. 1996;28:1-12.
18. Kyriakis JM, Avruch J. pp54 Microtubule-associated protein 2 kinase: a novel serine/threonine kinase regulated by phosphorylation and stimulated by poly-L-lysine. J Biol Chem. 1990;265:17355-17363.
19. Dérijard B, Hibi M, Wu L-H, Barrett T, Su B, Karin M, Davis R. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell. 1994;76:1025-1037.
20. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, Ahmad MF, Avruch J, Woodgett JR. The stress-activated protein kinase subfamily of c-Jun kinases. Nature. 1994;369:156-160.
21. Sluss HK, Barrett T, Dérijard B, Davis RJ. Signal transduction by tumor necrosis factor mediated by JNK protein kinases. Mol Cell Biol. 1994;14:8376-8384.
22. Gupta S, Campbell D, Dérijard B, Davis RJ. Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science. 1995;267:389-393.
23. Hibi M, Lin A, Minden A, Karin M. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 1993;7:2135-2148.
24. ras, Raf-1, and MAP kinase kinase. J Biol Chem. 1994;269:31836-31844.
25. Cano E, Hazzalin CA, Mahadevan LC. Anisomycin-activated protein kinases p45 and p55 but not mitogen-activated protein kinases ERK-1 and -2 are implicated in the induction of c-fos and c-jun. Mol Cell Biol. 1994;14:7352-7362.
26. Westwick JK, Weitzel C, Minden A, Karin M, Brenner DA. Tumor necrosis factor I stimulates AP-1 activity through prolonged activation of the c-Jun kinase. J Biol Chem. 1994;269:26396-26401.
27. Coso OA, Chiariello M, Kalinec G, Kyriakis JM, Woodgett J, Gutkind JS. Transforming G protein-coupled receptors potently activate JNK (SAPK): evidence for a divergence from the tyrosine kinase signaling pathway. J Biol Chem. 1995;270:5620-5624.
28. Bogoyevitch MA, Ketterman AJ, Sugden PH. Cellular stresses differentially activate the c-Jun N-terminal protein kinases (JNKs) and the extracellular signal-regulated protein kinases in cultured ventricular myocytes. J Biol Chem. 1995;270:29710-29717.
29. Han J, Lee J-D, Tobias PS, Ulevitch RJ. Endotoxin induces rapid protein tyrosine phosphorylation in 70Z/3 cells expressing CD14. J Biol Chem. 1993;268:25009-25014.
30. Han J, Lee J-D, Bibbs L, Ulevitch RJ. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science. 1994;265:808-811.
31. 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. 1994;78:1027-1037.
32. 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. 1994;78:1039-1049.
33. 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. 1994;372:739-746.
34. Doza YN, Cuenda A, Thomas GM, Cohen P, Nebreda AR. Activation of the MAP kinase homologue RK requires the phosphorylation of Thr-180 and Tyr-182 and both residues are phosphorylated in chemically-stressed KB cells. FEBS Lett. 1995;364:223-228.
35. Bogoyevitch MA, Glennon PE, Sugden PH. Endothelin-1, phorbol esters and phenylephrine stimulate MAP kinase activities in ventricular cardiomyocytes. FEBS Lett. 1993;317:271-275.
36. 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. 1994;269:1110-1119.
37. Thorburn J, Frost JA, Thorburn A. Mitogen-activated protein kinases mediate changes in gene expression, but not cytoskeletal organization associated with cardiac muscle hypertrophy. J Cell Biol. 1994;126:1565-1572.
38. Gillespie-Brown J, Fuller SJ, Bogoyevitch MA, Cowley S, Sugden PH. The mitogen-activated protein kinase kinase MEK1 stimulates a pattern of gene expression typical of the hypertrophic phenotype in rat ventricular cardiomyocytes. J Biol Chem. 1995;270:28092-28096.
39. TCF by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature. 1992;358:414-417.
40. Marais R, Wynne J, Treisman R. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell. 1993;73:381-393.
41. Gille H, Kortenjann M, Thomae O, Moomaw C, Slaughter C, Cobb MH, Shaw PE. ERK phosphorylation potentiates Elk-1-mediated ternary complex formation and transactivation. EMBO J. 1995;14:951-962.
42. Whitmarsh AJ, Shore P, Sharrocks AD, Davis RJ. Integration of MAP kinase signal transduction pathways at the serum response element. Science. 1995;269:403-407.
43. Livingstone C, Patel G, Jones N. ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO J. 1995;14:1785-1797.
44. 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. 1995;14:1798-1811.
45. Raingeaud J, Gupta S, Rogers JS, Dickens M, Ulevitch RJ, Davis RJ. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem. 1995;270:7420-7426.
46. Stokoe D, Campbell DG, Nakielny S, Hidaka H, Leevers SJ, Marshall C, Cohen P. MAPKAP kinase-2: a novel protein kinase activated by mitogen-activated protein kinase. EMBO J. 1992;11:3985-3994.
47. Stokoe D, Engel K, Campbell DG, Cohen P, Gaestel M. Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins. FEBS Lett. 1992;313:307-313.
48. Hendrick JP, Hartl F-U. Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem. 1993;62:349-384.
49. Andres J, Sharma HS, Knoll R, Stahl J, Sassen LMA, Verdouw PD, Schaper W. Expression of heat shock proteins in the normal and stunned porcine myocardium. Cardiovasc Res. 1993;27:1421-1429.
50. Lange-Carter CA, Pleiman CM, Gardner AM, Blumer KJ, Johnson GL. A divergence in the MAP kinase regulatory network denned by MEK kinase and Raf. Science. 1993;260:315-319.
51. Minden A, Lin A, McMahon M, Lange-Carter C, Dérijard B, Davis RJ, Johnson GL, Karin M. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science. 1994;266:1719-1723.
52. Yan M, Dai T, Deak JC, Kyriakis JM, Zon LI, Woodgett JR, Templeton DJ. Activation of stress-activated protein kinase by MEKK1 phosphorylation of its activator SEK1. Nature. 1994;372:798-800.
53. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem. 1976;72:248-254.
54. 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. 1993;72:757-767.
55. Kallunki T, Su B, Tsigelny I, Sluss HK, Dérijard B, Moore G, Davis R, Karin M. JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation. Genes Dev. 1994;8:2996-3007.
56. 1mediated response. J Biol Chem. 1990;265:13809-13817.
57. Mansour SJ, Matten WT, Hermann AS, Candia JM, Rong S, Fukasawa K, Van de Woude GF, Ahn NG. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science. 1994;265:966-970.
58. 1A-adrenergic receptor subtype mediates biochemical, molecular, and morphological features of cultured myocardial cell hypertrophy. J Biol Chem. 1993;268:15374-15380.
59. Lazou A, Bogoyevitch MA, Clerk A, Fuller SJ, Marshall CJ, Sugden PH. Regulation of the mitogen-activated protein kinase cascade in adult rat heart preparations in vitro. Circ Res. 1994;75:932-941.
60. Lin A, Minden A, Martinetto H, Claret F-X, Lange-Carter C, Mercurio F, Johnson GL, Karin M. Identification of a dual-specificity kinase that activates the Jun kinases and p38-Mpk2. Science. 1995;268:286-290.
61. Thorburn A, Thorburn J, Chen S-Y, Powers S, Shubeita HE, Feramisco JR, Chien KR. HRas-dependent pathways can activate morphological and genetic markers of cardiac muscle cell hypertrophy. J Biol Chem. 1993;268:2244-2249.
62. 1-adrenergic stimulation. J Biol Chem. 1994;269:13490-13496.
63. Thorburn J, McMahon M, Thorburn A. 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. 1994;269:30580-30586.
64. Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. J Biol Chem. 1995;270:16483-16486.
65. Knowlton KU, Baracchini E, Ross RS, Harris AN, Henderson SA, Evans SM, Glembotski CC, Chien KR. Co-regulation of the atrial natriuretic factor and cardiac myosin light chain-2 genes during α-adrenergic stimulation of neonatal rat ventricular cells: identification of cis sequences within an embryonic and a constitutive contractile protein gene which mediate inducible expression. J Biol Chem. 1991;266:7759-7768.
66. Hunter T, Karin M. The regulation of transcription by phosphorylation. Cell. 1992;70:375-387.
67. Karin M. Signal transduction from the cell surface to the nucleus through the phosphorylation of transcription factors. Curr Opin Cell Biol. 1994;6:415-424.
68. Binetruy B, Smeal T, Karin M. Ha-Ras augments c-Jun activity and stimulates phosphorylation of its activation domain. Nature. 1991;351:122-127.
69. Smeal T, Binetruy B, Mercola D, Grover-Bardwick A, Heidecker G, Rapp UR, Karin M. Oncoprotein-mediated signalling cascade stimulates c-Jun activity by phosphorylation of serines 63 and 73. Mol Cell Biol. 1992;12:3507-3513.
70. Avruch J, Zhang X, Kyriakis JM. Raf meets Ras: completing the framework of a signal transduction pathway. Trends Biochem Sci. 1994;19:279-283.
71. Burgering BMT, Bos JL. Regulation of Ras-mediated signalling: more than one way to skin a cat. Trends Biochem Sci. 1995;20:18-22.
72. Anversa P, Beghi C, Kikkawa Y, Olivetti G. Myocardial response to infarction in the rat: morphometric measurement of infarct size and myocyte cellular hypertrophy. Am J Pathol. 1985;118:484-492.
73. Anversa P, Beghi C, Kikkawa Y, Olivetti G. Myocardial infarction in rats: infarct size, myocyte hypertrophy and capillary growth. Circ Res. 1986;58:26-37.
74. Pfeffer JM, Fischer TA, Pfeffer MA. Angiotensin-converting enzyme inhibition and ventricular remodeling after myocardial infarction. Annu Rev Physiol. 1995;57:805-826.
75. 1-receptor-independent activation of protein kinase C in acute myocardial ischemia: mechanisms for sensitization of the adenylyl cyclase system. Circ Res. 1992;70:1304-1312.
76. Mitchell MB, Meng X, Ao L, Brown JM, Harken AH, Banerjee A. Preconditioning of isolated rat heart is mediated by protein kinase C. Circ Res. 1995;76:73-81.
77. Clerk A, Bogoyevitch MA, Fuller SJ, Lazou A, Parker PJ, Sugden PH. Expression of protein kinase C isoforms during cardiac ventricular development. Am J Physiol. 1995;269:H1087-H1097.
78. Pucéat M, Hilal-Dandan R, Strulovici B, Brunton LL, Brown JH. Differential regulation of protein kinase C isoforms in isolated neonatal and adult rat cardiomyocytes. J Biol Chem. 1994;269:16938-16944.
79. 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. 1994;269:32848-32857.
80. Bogoyevitch MA, Andersson MB, Gillespie-Brown J, Clerk A, Glennon PE, Fuller SJ, Sugden PH. Adrenergic receptor stimulation of the mitogen-activated protein kinase cascade and cardiac hypertrophy. Biochem J. 1996;314:115-121.
81. Minden A, Lin A, Smeal T, Dérijard B, Cobb M, Davis R, Karin M. c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases. Mol Cell Biol. 1994;14:6683-6688.
82. Su B, Jacinto E, Hibi M, Kallunki T, Karin M, Ben-Neriah Y. JNK is involved in signal transduction during co-stimulation of T lymphocytes. Cell. 1994;77:727-736.
83. Liu Y, Ytrehus K, Downey JM. Evidence that translocation of protein kinase C is a key event during ischemic preconditioning of rabbit myocardium. J Mol Cell Cardiol. 1994;26:661-668.
84. 1-Adrenergic agonists precondition rabbit ischemic myocardium independent of adenosine by direct activation of protein kinase C. Circ Res. 1994;75:576-585.
85. Ytrehus K, Liu Y, Downey JM. Preconditioning protects ischemic rabbit heart by protein kinase C activation. Am J Physiol. 1994;266:H1145-H1152.
86. Li Y, Kloner RA. Does protein kinase C play a role in ischemic preconditioning in rat hearts? Am J Physiol. 1995;268:H426-H431.
87. Clerk A, Gillespie-Brown J, Fuller SJ, Sugden PH. Stimulation of phosphatidylinositol hydrolysis, protein kinase C translocation, and mitogen-activated protein kinase activation by bradykinin in rat ventricular myocytes: dissociation from the hypertrophic response. Biochem J. 1996;307:109-118.
88. 1-adrenergic mechanism. Circ Res. 1993;73:656-670.
89. Wall TM, Sheehy R, Hartman JC. Role of bradykinin in myocardial preconditioning. J Pharmacol Exp Ther. 1994;270:681-689.
90. Goto M, Liu Y, Yang X-M, Ardell JL, Cohen MV, Downey JM. Role of bradykinin in protection of ischemic preconditioning in rabbit hearts. Circ Res. 1995;77:611-621.
91. Wang P, Gallagher KP, Downey JM, Cohen MV. Pretreatment with endothelin-1 mimics ischemic preconditioning against infarction in isolated rabbit heart. J Mol Cell Cardiol. 1996;28:579-588.
92. Przyklenk K, Sussman MA, Simkhovich BZ, Kloner RA. Does ischemic preconditioning trigger translocation of protein kinase C in the canine model? Circulation. 1995;92:1546-1557.
93. Mestril R, Dillmann WH. Heat shock proteins and protection against myocardial ischaemia. J Mol Cell Cardiol. 1995;27:45-52.
94. Marber MS, Mestril R, Chi SH, Sayen MR, Yellon DM, Dillmann WH. Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J Clin Invest. 1995;95:1446-1456.
95. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, Young PR, Lee JC. SB203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cell stresses and interleukin-1. FEBS Lett. 1995;364:229-233.
96. Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc Natl Acad Sci U S A. 1995;92:7686-7689.
97. Xu S, Dobbins D, Frost J, Dang A, Lange-Carter C, Cobb MH. MEKK1 phosphorylates MEK1 and MEK2 but does not cause activation of mitogen-activated protein kinase. Proc Natl Acad Sci U S A. 1995;92:6808-6812.
98. Moriguchi T, Kawasaki H, Matsuda S, Gotoh Y, Nishida E. Evidence for multiple activators for stress-activated protein kinases/c-Jun amino-terminal kinases: existence of novel activators. J Biol Chem. 1995;270:12969-12972.
99. Blank JL, Gerwins P, Elliot EM, Sather S, Johnson GL. Molecular cloning of mitogen-activated protein/ERK kinase kinases (MEKK) 2 and 3: regulation of sequential phosphorylation pathways involving mitogen-activated protein kinase and c-Jun kinase. J Biol Chem. 1996;271:5361-5368.
100. rdf-1. EMBO J. 1994;13:1610-1619.
101. Kharbanda S, Pandey P, Ren R, Mayer B, Zon L, Kufe D. c-Abl activation regulates induction of the SEK1/stress-activated protein kinase pathway in the cellular response to 1-β-D-arabinofuranosyl-cytosine. J Biol Chem. 1995;270:30278-30281.
102. Verheij M, Bose R, Lin XH, Yao B, Jarvis WD, Grant S, Birrer MJ, Szabo E, Zon LI, Kyriakis JM, Halmovitz-Friedman A, Fuks Z, Kolesnick RN. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 1996;380:75-79.
103. Johnson NL, Gardner AM, Diener KM, Lange-Carter CA, Gleavy J, Jarpe MB, Minde 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. 1996;271:3229-3237.
104. Pombo CM, Bonventre JV, Avruch J, Woodgett JR, Kyriakis JM, Force T. The stress-activated protein kinases are major c-Jun amino-terminal kinases activated by ischemia and reperfusion. J Biol Chem. 1994;269:26541-26546.
105. Morooka H, Bonventre JV, Pombo CM, Kyriakis JM, Force T. Ischemia and reperfusion enhance ATF-2 and c-Jun binding to cAMP response elements and to an AP-1 binding site from the c-jun promoter. J Biol Chem. 1995;270:30084-30092.
106. Treisman R. Ternary complex factors: growth factor regulated transcriptional activators. Curr Opin Gen Dev. 1994;4:96-101.
107. Sprenkle AB, Murray SF, Glembotski CC. Involvement of multiple cis elements in basal and α-adrenergic agonist-inducible atrial natriuretic factor transcription: roles for serum response elements and an SP-1-like element. Circ Res. 1995;77:1060-1069.
108. 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. 1996;218:83-88.